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The Physiological Control of Motoneuron Activity

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Abstract

The sections in this article are:

1 Patterns of Motor Output
1.1 Orderly Recruitment of Motor Units
1.2 Rate Modulation of Motor Units
2 Motoneuron Properties
2.1 The Ionic Basis of the Resting Potential
2.2 Determinants of Input Resistance
2.3 Threshold Behavior
2.4 Repetitive Discharge Behavior
2.5 Effects of Neuromodulators on Motoneuron Behavior
2.6 Motoneuron Models
3 Organization of Synaptic Inputs to the Motoneuron Pool
3.1 Transfer of Synaptic Current to the Soma
3.2 Effective Synaptic Currents
3.3 Distribution of Effective Synaptic Current from Identified Input Systems
3.4 Effects of Synaptic Inputs on Motoneuron Discharge
3.5 Summation of Synaptic Inputs
4 The Motoneuron Pool and its Muscle as a Neural System
4.1 Mechanical Properties of Motor Units
4.2 Single Motor Unit Input‐Output Function
4.3 Input‐Output Function of the Motoneuron Pool
4.4 Mechanisms Controlling Motor Outflow
5 Summary
Figure 1. Figure 1.

Recruitment and rate‐modulation patterns in human subjects. A, Recruitment order in four different human subjects for wrist extension of the extensor digitorum communis muscle . Relation between peak torque of the spike triggered average twitch and recruitment threshold. Symbols indicate different data for four different subjects. Correlation coefficients: subject CT (open circles): 0.63; PB (filled circles): 0.61; SR (filled triangles): 0.37; TP (open squares): 0.50. B – D, Rate‐limiting patterns in human subjects in three different arm muscles: biceps brachii , brachialis , and extensor digitorum communis . In each case, the y‐axis is single‐unit discharge rate and the x‐axis is muscle force, with maximum indicated. The data in D were originally displayed on semilog coordinates and have been digitized and replotted on a linear scale like that of the other two studies.

Figure 2. Figure 2.

Anatomical features of motoneurons. A, Camera lucida drawing of an HRP‐filled cat medial gastrocnemius motoneuron (type FF), projected without perspective in the sagittal plane.

From Cullheim et al. .] B and C, Two different schematic plots of a single reconstructed dendritic tree. [From Rall et al. .] Distance scale is in units of electronic distance from the soma, calculated using a uniform specific membrane resistivity (Rm) of 11 kΩ·cm2 and cytoplasmic resistivity (Ri) of 70 Ω·cm. Individual dendritic segments are represented in B, while in C the entire dendritic tree has been collapsed into a single unbranched “equivalent” cable
Figure 3. Figure 3.

Relation of voltage range traversed during repetitive discharge to the voltage dependence of the persistent inward current recorded under voltage‐clamp conditions in the same cell. A, Voltage trajectories during repetitive discharge in the primary range (P) at the transition to thedary range (T) and at the upper end of the secondary range (S). Top of spikes (65 mV) are clipped. B and D, Voltage step commands (B) and the recorded membrane currents (after electronic subtraction of the leak current and the longest capacitative charging transient). (The baseline of traces 1 and 2 in the lower right panel are identical to those of traces 3–5 but have been shifted downward for clarity.). C, Average steady firing rate (f) vs. injected current (I) for the cell.

From Schwindt and Crill
Figure 4. Figure 4.

Bistable discharge behavior induced by intracellular injection of TMA (C) or by the intravenous injection of the serotonergic precursor 5‐HTP (D and F). A, I–V curves generated by a slow voltage‐clamp ramp before (control), during (B), and after (C) TMA injection. B, Response to a suprathreshold depolarizing current pulse obtained just after the (B) I–V curve in A. C, Response of the same motoneuron to injected current obtained after the (C) I–V curve in A. D. Bistable discharge behavior of a lumbar motoneuron in an acutely spinalized decerebrate cat following intravenous administration of 5‐HTP.E and F, Response of a motoneuron to triangular current injection before (E) and after (F) 5‐HTP administration.

From Hounsgaard et al. . From Schwindt and Crill . From Hounsgaard et al.
Figure 5. Figure 5.

Effects of active conductances on subthreshold behavior of motoneurons. A, Response of a passive neuron model to 250 ms injected current steps of different magnitude. The model consisted of a spherical soma (60 μm diameter) attached to a tapering, 16‐compartment dendritic cylinder with a total membrane surface area of 622,000 μm2. Specific membrane capacitance was 1 μF·cm−2 and specific membrane resistance varied from 2 kωcm2 in the soma up to 25 kΩ·cm2 in the distal dendritic compartments. A nonspecific electrode leak conductance of 100 nS was placed in the soma to represent impalement‐induced leak. All simulations were performed with Nodus software [DeShutter ] on a Macintosh computer. B, Effects of inserting active conductances on the somatic compartment. Three conductances were inserted: (1) a hyperpolarization‐activated mixed cation conductance, (2) a slow potassium conductance, and (3) a conductance mediating a persistent inward current. Their steady‐state voltage dependencies were specified by equations of the form: G(V) = Gmax/{1 + exp[(VVh)/S]} for the first, G(V) = Gmax/((1 + exp[(VhV)/S]})2 for the second, and G(V) = Gmax/ (1 + exp[(VhV)/S]) for the third conductance. Gmax is the maximum conductance and was equal to 500, 2,200, and 220 nS for the three conductances. Vh is the half‐activation voltage and had values of −75, −25, and −48 mV, whereas S affects the steepness of the activation curve and had values of 5.3, 15, and 3 mV−1. The conductance time constants were voltage independent and were set equal to 50, 40, and 20 ms. C, Voltage‐current plots for simulated voltage traces shown in A. D, Voltage‐current plots for simulated voltage traces shown in B. Filled and open circles represent voltages measured at two different times as indicated in B. E, Current‐voltage relation (curved line) calculated by summing the leak current in the passive model (straight line) with the current‐voltage relations of the three active conductances.

Figure 6. Figure 6.

Effects of activating all of the synaptic boutons on the effective membrane resistance of a dendritic compartment. The resting specific membrane resistance was 10 kΩ·cm2. The quantal conductance change was calculated by fitting an equation of the form: G(t) = A*t*exp(‐t/t) to published voltage‐clamp data (; cf. ) and then integrating conductance over time. The total synaptic conductance was calculated by multiplying this quantal conductance change (in Siemans‐seconds per quantum) times the quantal release rate (in quanta per second per bouton) times the bouton density (in boutons/cm2 assumed to be 5 million/cm2 for both excitatory and inhibitory boutons) to yield the conductance change per unit area (Siemans/cm2). The reciprocal of the sum of this value and the resting conductance yields the effective membrane resistance. Open circles, Effects of activating excitatory boutons alone. Filled circles, Effects of activating inhibitory boutons alone. Solid line, Effects of activating both excitatory and inhibitory boutons.

For a similar analysis, see Barrett
Figure 7. Figure 7.

Effective synaptic current vs. quantal release rate in a passive motoneuron model (same as that used in Fig. A). Excitatory synaptic boutons were assigned to each compartment with a density of 5/100 μm2. The quantal conductance change was the same as that used in Figure . The effective synaptic current is measured in the soma compartment with the soma clamped at different voltages relative to the resting potential.

Figure 8. Figure 8.

Measurement of effective synaptic current (IN). A and D, Membrane voltage responses of two triceps surae motoneurons to injected currents (lower traces) and synaptic current (solid bar). The experimental protocol consists of three 500 ms epochs (injected current alone, injected + synaptic current, and synaptic current alone), which are numbered and separated by vertical dotted lines. The mean resting potential (measured prior to current injection) has been subtracted from each trace and the traces have been digitally low‐pass‐filtered (100 Hz cutoff) for clarity. Voltage measurements are indicated for the bottom voltage trace in each set. Vi, steady‐state voltage response to injected current alone; Vi+s, steady‐state voltage response to synaptic and injected current; ΔVs, change in voltage due to synaptic current = Vi+s ‐ Vi. B and E, Steady‐state voltage responses vs. injected current (I). Solid lines indicate best linear fit to the data points. The effective synaptic current (IN) is taken to be equal in magnitude and opposite in sign to the current at which Vi+s = 0 (estimated from the zero intercept of the fit to Vi+s vs. I). The slope of the linear fit to Vi vs. I gives the steady‐state input resistance (RNSS), while the slope of the linear fit to Vi+s vs. I gives the steady‐state input resistance during synaptic activation (RNSYN). C and F, Dependence of steady‐state synaptic potential (ΔVs) on somatic membrane potential (Vi).

Adapted from Powers et al.
Figure 9. Figure 9.

Graphical representation of the magnitude and distribution of the effective synaptic currents at resting potential (IN) from five different input systems. The dark stippled band represents IN from homonymous la afferent fibers [Heckman and Binder ]; the stripped band represents IN from Ia‐inhibitory interneurons [Heckman and Binder ]; the black band represents the IN from Renshaw interneurons [Lindsay and Binder ]; the thick lines outline the IN from contralateral rubrospinal neurons [Powers et al. ]; and the light stippled band represents IN from ipsilateral Deiter's nucleus

Westcott et al.
Figure 10. Figure 10.

Firing rate modulation produced by steady‐state synaptic current. A and C, Responses of two different triceps surae motoneurons to injected current alone (thin voltage traces) and injected + synaptic current (thick voltage traces). Bottom traces are injected current; synaptic activation indicated by solid bar. The three experimental epochs are indicated by dotted lines. B and D, Instantaneous firing rate vs. time, calculated from the spike trains in A and C, and additional current alone and current + synaptic activation trials. The thin traces are the firing rate responses to injected current alone, while the current + synaptic activation responses are shown by the thick traces. The firing rate modulation produced by synaptic activation (ΔF) is equal to the difference in mean discharge rate (over the last 300 ms of current injection) between current + synaptic activation and current alone trials.

Modified from Powers et al.
Figure 11. Figure 11.

The summation of synaptic inputs. A, Linear summation of synaptic inputs generated by Ia afferents and by red nucleus stimulation. In each panel the upper voltage traces show the responses of an MG motoneuron to injected current alone; the lower traces show the responses to the same amount of injected current plus the steady‐state synaptic current. This MG cell had an f‐I slope of 1.2 imp·s−1·nA−1. The Ia effective synaptic current was estimated to be 5.8 nA at threshold, and as shown in the left panels, it produced an average increase of 7.8 imp/s in the motoneuron's steady‐state discharge. The predicted change was 7 imp/s. Stimulation within the contralateral red nucleus produced an estimated effective synaptic current at threshold of about 11.6 nA, which was predicted to produce an increase in the cell's firing rate of 14 imp/s. The actual measured change was 13.5 imp/s as shown in the middle panels. When the red nucleus was stimulated and the triceps surae muscles vibrated concurrently (right panels), the net effective synaptic current measured in the cell was 18.3 nA at rest, which was quite close to the algebraic sum of the two individual, effective synaptic currents (7.2 nA + 14.5 nA). Moreover, the observed change in the average firing rate produced by the concurrent stimulation (19.6 imp/s) was quite close to that predicted based on both the measured effective synaptic current (17.5 imp/s) and the algebraic sum of the changes in firing rate produced by the two inputs individually (21.3 imp/s). B, Nonlinear summation of the effects of synaptic inputs on motoneuron discharge. The left‐hand panel shows that activating homonymous Ia afferent fibers produced about a 14 imp/s increase in discharge rate in this MG motoneuron. As indicated in the middle panel, stimulating within the red nucleus had virtually no effect on the steady‐state firing rate of the same cell, although there is an indication of a transient inhibition at the onset. However, as shown on the right, when the Ia afferents and red nucleus were stimulated together, the total increase in firing rate was much less than that produced by the Ia afferents alone. C, Occlusion of excitatory synaptic inputs mediated by common interneurons. Stimulation of the sural nerve at 5 × T generated an effective synaptic current of 5.6 nA at threshold and a change in discharge of 7.3 imp/s in this MG motoneuron (right panel). In the same cell, stimulation within the red nucleus generated an effective synaptic current of 11.6 nA at threshold and a change in its discharge rate of 13.5 imp/s (left‐hand panel). However, when the two inputs were stimulated concurrently (right‐hand panel), the effective synaptic current and discharge rate modulation were no greater than those produced by red nucleus stimulation alone.

Figure 12. Figure 12.

Computer simulations of the input‐output function of the mammalian motoneuron pool. A, Representative single‐unit force‐current (F‐I) functions. Dashed lines indicate forces at the limits of the primary range of the motoneuron frequency‐current (f‐I) functions (i.e., threshold and at the transition to the secondary range). B, The whole pool input‐output function that results when a uniform input is applied to the single‐unit F‐I functions and their forces are linearly summed. C, The pool force‐length relation at various levels of synaptic input, with realistic recruitment and rate patterns. Dashed lines indicate force‐length relations that occur in the absence of the interaction between stimulus rate and optimal length. D, The pool force‐velocity functions at various levels of input, with realistic recruitment and rate patterns.

Data from in A and B from Heckman and Binder , in C and D from Heckman et al.
Figure 13. Figure 13.

Computer simulations of the effect of synaptic input on recruitment order. As random variance (i.e., noise) increased, the percentage of reversals generally increases. The uniform input allows recruitment to be specified by the intrinsic properties of the motor units. Only the rubrospinal combined excitation and inhibition gives a reversed sequence. Uniform distribution: thick line, filled squares; Ia input: thin line, open circles; vestibular input: open diamonds; rubrospinal excitation: open triangles; combined rubrospinal excitation and a constant 2 nA of rubrospinal inhibition: dashed line, open triangles; combined rubrospinal excitation, 2 nA of rubrospinal inhibition, and 2 nA of Ia excitation: dashed line with x's.

From Heckman and Binder
Figure 14. Figure 14.

Computer simulation of rate limiting, for comparison with the experimental data in Figure . See text for details of the “crossover” synaptic input organization used to produce this pattern, cf. Heckman and Binder .

Figure 15. Figure 15.

Computer simulations of input–output relations between synaptic input (y‐axis) to the motoneuron pool and muscle force (z‐axis) and velocity of shortening (x‐axis). Surface shading and y‐axis labels at upper left indicate the percentage of muscle force generated by type FF units. Single motor unit f‐I, F‐f, and F‐V functions based on the cat MG muscle . Lines labeled with various motor tasks indicate approximate ranges of forces (z‐axis) and velocities (x‐axis) measured in MG with chronically implanted devices. Force ranges were estimated from the peak during stance, which occurs in near isometric conditions as muscle velocity undergoes the transition between the extension and flexion phases of the stance

data from Walmsley et al. ]. Velocity ranges were taken from the peak velocities of shortening during the later portion of the stance phase, when rapid flexion is developing but the muscle is still active. Velocities for slow walking were taken from Weytjens (unpublished data). For faster speeds and jumping, velocities were estimated from the length records of Walmsley and colleagues . Jump heights ranged from about 0.5–1.2 m . Arrows for running and jumping indicate that the fastest velocities probably exceed the range of the figure, which falls well short of the maximum velocity for MG


Figure 1.

Recruitment and rate‐modulation patterns in human subjects. A, Recruitment order in four different human subjects for wrist extension of the extensor digitorum communis muscle . Relation between peak torque of the spike triggered average twitch and recruitment threshold. Symbols indicate different data for four different subjects. Correlation coefficients: subject CT (open circles): 0.63; PB (filled circles): 0.61; SR (filled triangles): 0.37; TP (open squares): 0.50. B – D, Rate‐limiting patterns in human subjects in three different arm muscles: biceps brachii , brachialis , and extensor digitorum communis . In each case, the y‐axis is single‐unit discharge rate and the x‐axis is muscle force, with maximum indicated. The data in D were originally displayed on semilog coordinates and have been digitized and replotted on a linear scale like that of the other two studies.



Figure 2.

Anatomical features of motoneurons. A, Camera lucida drawing of an HRP‐filled cat medial gastrocnemius motoneuron (type FF), projected without perspective in the sagittal plane.

From Cullheim et al. .] B and C, Two different schematic plots of a single reconstructed dendritic tree. [From Rall et al. .] Distance scale is in units of electronic distance from the soma, calculated using a uniform specific membrane resistivity (Rm) of 11 kΩ·cm2 and cytoplasmic resistivity (Ri) of 70 Ω·cm. Individual dendritic segments are represented in B, while in C the entire dendritic tree has been collapsed into a single unbranched “equivalent” cable


Figure 3.

Relation of voltage range traversed during repetitive discharge to the voltage dependence of the persistent inward current recorded under voltage‐clamp conditions in the same cell. A, Voltage trajectories during repetitive discharge in the primary range (P) at the transition to thedary range (T) and at the upper end of the secondary range (S). Top of spikes (65 mV) are clipped. B and D, Voltage step commands (B) and the recorded membrane currents (after electronic subtraction of the leak current and the longest capacitative charging transient). (The baseline of traces 1 and 2 in the lower right panel are identical to those of traces 3–5 but have been shifted downward for clarity.). C, Average steady firing rate (f) vs. injected current (I) for the cell.

From Schwindt and Crill


Figure 4.

Bistable discharge behavior induced by intracellular injection of TMA (C) or by the intravenous injection of the serotonergic precursor 5‐HTP (D and F). A, I–V curves generated by a slow voltage‐clamp ramp before (control), during (B), and after (C) TMA injection. B, Response to a suprathreshold depolarizing current pulse obtained just after the (B) I–V curve in A. C, Response of the same motoneuron to injected current obtained after the (C) I–V curve in A. D. Bistable discharge behavior of a lumbar motoneuron in an acutely spinalized decerebrate cat following intravenous administration of 5‐HTP.E and F, Response of a motoneuron to triangular current injection before (E) and after (F) 5‐HTP administration.

From Hounsgaard et al. . From Schwindt and Crill . From Hounsgaard et al.


Figure 5.

Effects of active conductances on subthreshold behavior of motoneurons. A, Response of a passive neuron model to 250 ms injected current steps of different magnitude. The model consisted of a spherical soma (60 μm diameter) attached to a tapering, 16‐compartment dendritic cylinder with a total membrane surface area of 622,000 μm2. Specific membrane capacitance was 1 μF·cm−2 and specific membrane resistance varied from 2 kωcm2 in the soma up to 25 kΩ·cm2 in the distal dendritic compartments. A nonspecific electrode leak conductance of 100 nS was placed in the soma to represent impalement‐induced leak. All simulations were performed with Nodus software [DeShutter ] on a Macintosh computer. B, Effects of inserting active conductances on the somatic compartment. Three conductances were inserted: (1) a hyperpolarization‐activated mixed cation conductance, (2) a slow potassium conductance, and (3) a conductance mediating a persistent inward current. Their steady‐state voltage dependencies were specified by equations of the form: G(V) = Gmax/{1 + exp[(VVh)/S]} for the first, G(V) = Gmax/((1 + exp[(VhV)/S]})2 for the second, and G(V) = Gmax/ (1 + exp[(VhV)/S]) for the third conductance. Gmax is the maximum conductance and was equal to 500, 2,200, and 220 nS for the three conductances. Vh is the half‐activation voltage and had values of −75, −25, and −48 mV, whereas S affects the steepness of the activation curve and had values of 5.3, 15, and 3 mV−1. The conductance time constants were voltage independent and were set equal to 50, 40, and 20 ms. C, Voltage‐current plots for simulated voltage traces shown in A. D, Voltage‐current plots for simulated voltage traces shown in B. Filled and open circles represent voltages measured at two different times as indicated in B. E, Current‐voltage relation (curved line) calculated by summing the leak current in the passive model (straight line) with the current‐voltage relations of the three active conductances.



Figure 6.

Effects of activating all of the synaptic boutons on the effective membrane resistance of a dendritic compartment. The resting specific membrane resistance was 10 kΩ·cm2. The quantal conductance change was calculated by fitting an equation of the form: G(t) = A*t*exp(‐t/t) to published voltage‐clamp data (; cf. ) and then integrating conductance over time. The total synaptic conductance was calculated by multiplying this quantal conductance change (in Siemans‐seconds per quantum) times the quantal release rate (in quanta per second per bouton) times the bouton density (in boutons/cm2 assumed to be 5 million/cm2 for both excitatory and inhibitory boutons) to yield the conductance change per unit area (Siemans/cm2). The reciprocal of the sum of this value and the resting conductance yields the effective membrane resistance. Open circles, Effects of activating excitatory boutons alone. Filled circles, Effects of activating inhibitory boutons alone. Solid line, Effects of activating both excitatory and inhibitory boutons.

For a similar analysis, see Barrett


Figure 7.

Effective synaptic current vs. quantal release rate in a passive motoneuron model (same as that used in Fig. A). Excitatory synaptic boutons were assigned to each compartment with a density of 5/100 μm2. The quantal conductance change was the same as that used in Figure . The effective synaptic current is measured in the soma compartment with the soma clamped at different voltages relative to the resting potential.



Figure 8.

Measurement of effective synaptic current (IN). A and D, Membrane voltage responses of two triceps surae motoneurons to injected currents (lower traces) and synaptic current (solid bar). The experimental protocol consists of three 500 ms epochs (injected current alone, injected + synaptic current, and synaptic current alone), which are numbered and separated by vertical dotted lines. The mean resting potential (measured prior to current injection) has been subtracted from each trace and the traces have been digitally low‐pass‐filtered (100 Hz cutoff) for clarity. Voltage measurements are indicated for the bottom voltage trace in each set. Vi, steady‐state voltage response to injected current alone; Vi+s, steady‐state voltage response to synaptic and injected current; ΔVs, change in voltage due to synaptic current = Vi+s ‐ Vi. B and E, Steady‐state voltage responses vs. injected current (I). Solid lines indicate best linear fit to the data points. The effective synaptic current (IN) is taken to be equal in magnitude and opposite in sign to the current at which Vi+s = 0 (estimated from the zero intercept of the fit to Vi+s vs. I). The slope of the linear fit to Vi vs. I gives the steady‐state input resistance (RNSS), while the slope of the linear fit to Vi+s vs. I gives the steady‐state input resistance during synaptic activation (RNSYN). C and F, Dependence of steady‐state synaptic potential (ΔVs) on somatic membrane potential (Vi).

Adapted from Powers et al.


Figure 9.

Graphical representation of the magnitude and distribution of the effective synaptic currents at resting potential (IN) from five different input systems. The dark stippled band represents IN from homonymous la afferent fibers [Heckman and Binder ]; the stripped band represents IN from Ia‐inhibitory interneurons [Heckman and Binder ]; the black band represents the IN from Renshaw interneurons [Lindsay and Binder ]; the thick lines outline the IN from contralateral rubrospinal neurons [Powers et al. ]; and the light stippled band represents IN from ipsilateral Deiter's nucleus

Westcott et al.


Figure 10.

Firing rate modulation produced by steady‐state synaptic current. A and C, Responses of two different triceps surae motoneurons to injected current alone (thin voltage traces) and injected + synaptic current (thick voltage traces). Bottom traces are injected current; synaptic activation indicated by solid bar. The three experimental epochs are indicated by dotted lines. B and D, Instantaneous firing rate vs. time, calculated from the spike trains in A and C, and additional current alone and current + synaptic activation trials. The thin traces are the firing rate responses to injected current alone, while the current + synaptic activation responses are shown by the thick traces. The firing rate modulation produced by synaptic activation (ΔF) is equal to the difference in mean discharge rate (over the last 300 ms of current injection) between current + synaptic activation and current alone trials.

Modified from Powers et al.


Figure 11.

The summation of synaptic inputs. A, Linear summation of synaptic inputs generated by Ia afferents and by red nucleus stimulation. In each panel the upper voltage traces show the responses of an MG motoneuron to injected current alone; the lower traces show the responses to the same amount of injected current plus the steady‐state synaptic current. This MG cell had an f‐I slope of 1.2 imp·s−1·nA−1. The Ia effective synaptic current was estimated to be 5.8 nA at threshold, and as shown in the left panels, it produced an average increase of 7.8 imp/s in the motoneuron's steady‐state discharge. The predicted change was 7 imp/s. Stimulation within the contralateral red nucleus produced an estimated effective synaptic current at threshold of about 11.6 nA, which was predicted to produce an increase in the cell's firing rate of 14 imp/s. The actual measured change was 13.5 imp/s as shown in the middle panels. When the red nucleus was stimulated and the triceps surae muscles vibrated concurrently (right panels), the net effective synaptic current measured in the cell was 18.3 nA at rest, which was quite close to the algebraic sum of the two individual, effective synaptic currents (7.2 nA + 14.5 nA). Moreover, the observed change in the average firing rate produced by the concurrent stimulation (19.6 imp/s) was quite close to that predicted based on both the measured effective synaptic current (17.5 imp/s) and the algebraic sum of the changes in firing rate produced by the two inputs individually (21.3 imp/s). B, Nonlinear summation of the effects of synaptic inputs on motoneuron discharge. The left‐hand panel shows that activating homonymous Ia afferent fibers produced about a 14 imp/s increase in discharge rate in this MG motoneuron. As indicated in the middle panel, stimulating within the red nucleus had virtually no effect on the steady‐state firing rate of the same cell, although there is an indication of a transient inhibition at the onset. However, as shown on the right, when the Ia afferents and red nucleus were stimulated together, the total increase in firing rate was much less than that produced by the Ia afferents alone. C, Occlusion of excitatory synaptic inputs mediated by common interneurons. Stimulation of the sural nerve at 5 × T generated an effective synaptic current of 5.6 nA at threshold and a change in discharge of 7.3 imp/s in this MG motoneuron (right panel). In the same cell, stimulation within the red nucleus generated an effective synaptic current of 11.6 nA at threshold and a change in its discharge rate of 13.5 imp/s (left‐hand panel). However, when the two inputs were stimulated concurrently (right‐hand panel), the effective synaptic current and discharge rate modulation were no greater than those produced by red nucleus stimulation alone.



Figure 12.

Computer simulations of the input‐output function of the mammalian motoneuron pool. A, Representative single‐unit force‐current (F‐I) functions. Dashed lines indicate forces at the limits of the primary range of the motoneuron frequency‐current (f‐I) functions (i.e., threshold and at the transition to the secondary range). B, The whole pool input‐output function that results when a uniform input is applied to the single‐unit F‐I functions and their forces are linearly summed. C, The pool force‐length relation at various levels of synaptic input, with realistic recruitment and rate patterns. Dashed lines indicate force‐length relations that occur in the absence of the interaction between stimulus rate and optimal length. D, The pool force‐velocity functions at various levels of input, with realistic recruitment and rate patterns.

Data from in A and B from Heckman and Binder , in C and D from Heckman et al.


Figure 13.

Computer simulations of the effect of synaptic input on recruitment order. As random variance (i.e., noise) increased, the percentage of reversals generally increases. The uniform input allows recruitment to be specified by the intrinsic properties of the motor units. Only the rubrospinal combined excitation and inhibition gives a reversed sequence. Uniform distribution: thick line, filled squares; Ia input: thin line, open circles; vestibular input: open diamonds; rubrospinal excitation: open triangles; combined rubrospinal excitation and a constant 2 nA of rubrospinal inhibition: dashed line, open triangles; combined rubrospinal excitation, 2 nA of rubrospinal inhibition, and 2 nA of Ia excitation: dashed line with x's.

From Heckman and Binder


Figure 14.

Computer simulation of rate limiting, for comparison with the experimental data in Figure . See text for details of the “crossover” synaptic input organization used to produce this pattern, cf. Heckman and Binder .



Figure 15.

Computer simulations of input–output relations between synaptic input (y‐axis) to the motoneuron pool and muscle force (z‐axis) and velocity of shortening (x‐axis). Surface shading and y‐axis labels at upper left indicate the percentage of muscle force generated by type FF units. Single motor unit f‐I, F‐f, and F‐V functions based on the cat MG muscle . Lines labeled with various motor tasks indicate approximate ranges of forces (z‐axis) and velocities (x‐axis) measured in MG with chronically implanted devices. Force ranges were estimated from the peak during stance, which occurs in near isometric conditions as muscle velocity undergoes the transition between the extension and flexion phases of the stance

data from Walmsley et al. ]. Velocity ranges were taken from the peak velocities of shortening during the later portion of the stance phase, when rapid flexion is developing but the muscle is still active. Velocities for slow walking were taken from Weytjens (unpublished data). For faster speeds and jumping, velocities were estimated from the length records of Walmsley and colleagues . Jump heights ranged from about 0.5–1.2 m . Arrows for running and jumping indicate that the fastest velocities probably exceed the range of the figure, which falls well short of the maximum velocity for MG
References
 1. Araki, T., and C. A. Terzuolo. Membrane currents in spinal motoneurons associated with the action potential and synaptic activity. J. Neurophysiol. 25: 772–789, 1962.
 2. Arvidsson, U., S. Cullheim, B. Ulfhake, G. W. Bennett, K. C. Fone, A. C. Cuello, A. A. Verhofstad, T. J. Visser, and T. Hokfelt. 5‐Hydroxytryptamine, substance P, and thyrotropin‐releasing hormone in the adult cat spinal cord segment L7: immunohistochemical and chemical studies. Synapse 6: 237–270, 1990.
 3. Bagust, J., S. Knott, D. M. Lewis, J. C. Luck, and R. A. Westerman. Isometric contractions of motor units in a fast twitch muscle of the cat. J. Physiol. (Land.) 231: 87–104, 1973.
 4. Bakels, R., and D. Kernell. Average but not continuous speed match between motoneurons and muscle units of rat tibialis anterior. J. Neurophysiol. 70: 1300–1306, 1993.
 5. Bakels, R., and D. Kernell. Matching between motoneurone and muscle unit properties in rat medial gastrocnemius. J. Physiol. (Lond.) 463: 307–324, 1993.
 6. Baldissera, F. Relationships between the spike components and the delayed depolarization in cat spinal neurones. J. Physiol. (Lond.) 259: 325–338, 1976.
 7. Baldissera, F. Impulse frequency encoding of the dynamic aspects of excitation. Arch. Ital. Biol. 122: 43–58, 1984.
 8. Baldissera, F., P. Campadelli, and L. Piccinelli. Neural encoding of input transients investigated by intracellular injection of ramp currents in cat α‐motoneurones. J. Physiol. (Land.) 328: 73–86, 1982.
 9. Baldissera, F., P. Campadelli, and L. Piccinelli. The dynamic response of cat gastrocnemius motor units investigated by ramp‐current injection into their motoneurones. J. Physiol. (Lond.) 387: 317–30, 1987.
 10. Baldissera, F., and B. Gustafsson. Afterhyperpolarization time course in lumbar motoneurones of the cat. Acta Physiol. Scand. 91: 512–527, 1974.
 11. Baldissera, F., and B. Gustafsson. Firing behaviour of a neuron model based on the afterhyperpolarization conductance time‐course and algebraical summation. Adaptation and steady state firing. Acta Physiol. Scand. 92: 27–47, 1974.
 12. Baldissera, F., and B. Gustafsson. Firing behaviour of a neuron model based on the afterhyperpolarization conductance time‐course. First interval firing. Acta Physiol. Scand. 91: 528–544, 1974.
 13. Baldissera, F., B. Gustafsson, and F. Parmiggiani. Saturating summation of the afterhyperpolarization conductance in spinal motoneurones: a mechanism for ‘secondary range’ repetitive firing. Brain Res. 146: 69–82, 1978.
 14. Baldissera, F., H. Hultborn, and M. Illert. Integration in spinal neuronal systems. In: Handbook of Physiology, The Nervous System, Motor Control, edited by V. B. Brooks. Bethesda, MD: Am. Physiol. Soc., 1981, p. 509–595.
 15. Barrett, R. F., J.N. Barrett, and W. R. Crill. Voltage‐sensitive outward currents in cat motoneurones. J. Physiol. (Lond.) 304: 251–276, 1980.
 16. Barrett, J. N. Motoneuron dendrites: role in synaptic integration. Federation Proc. 34: 1398–1407, 1975.
 17. Barrett, J. N., and W. E. Crill. Specific membrane properties of cat motoneurones. J. Physiol. (Lond.) 239: 301–324, 1974.
 18. Barrett, J. N., and W. E. Crill. Voltage clamp of cat motoneurone somata: properties of the fast inward current. J. Physiol. (Lond.) 304: 231–249, 1980.
 19. Bawa, P., M. D. Binder, P. Ruenzel, and E. Henneman. Recruitment order of motoneurons in stretch reflexes is highly correlated with their axonal conduction velocity. J. Neurophysiol. 52: 410–420, 1984.
 20. Bawa, P., and R. N. Lemon. Recruitment of motor units in response to transcranial magnetic stimulation in man. J. Physiol. (Lond.) 471: 445–464, 1993.
 21. Bayliss, D. A., M. Umemiya, and A. J. Berger. Serotonin inhibits N‐ and P‐type calcium channels and the after hyperpolarization in rat motoneurones. J. Physiol. (Lond.) 485: 635–647, 1995.
 22. Bayliss, D. A., F. Viana, M. C. Bellingham, and A. J. Berger. Characteristics and postnatal development of a hyperpolarization‐activated inward current in rat hypoglossal motoneurons in vitro. J. Neurophysiol. 71: 119–128, 1994.
 23. Bayliss, D. A., F. Viana, and A. J. Berger. Mechanisms underlying excitatory effects of thyrotropin‐releasing hormone on rat hypoglossal motoneurons in vitro. J. Neurophysiol. 68: 1733–1745, 1992.
 24. Berger, A. J., D. A. Bayliss, and F. Viana. Modulation of neonatal rat hypoglossal motoneuron excitability by serotonin. Neurosci. Lett. 143: 164–168, 1992.
 25. Bessou, P., F. Rmonet‐Dénand, and Y. Laporte. Relation entre la vitesse de conduction des fibres nerveuses mortices et le tempe de contraction de leurs unites motrices. C. R. Acad. Sci. Ser. D. 256: 5625–5627, 1963.
 26. Bigland, B., and O. C. J. Lippold. Motor unit activity in the voluntary contraction of human muscle. J. Physiol. (Lond.) 125: 322–335, 1954.
 27. Binder, M. D., P. Bawa, P. Ruenzel, and E. Henneman. Does orderly recruitment of motoneurons depend on the existence of different types of motor units? Neurosci. Lett. 36: 55–58, 1983.
 28. Binder, M. D., C. J. Heckman, and R. K. Powers. How different afferent inputs control motoneuron discharge and the output of the motoneuron pool. Curr. Opin. Neurohiol. 3: 1028–1034, 1993.
 29. Binder, M. D., and L. M. Mendell. The Segmental Motor System. New York: Oxford University Press, 1990.
 30. Binder, M. D., and R. K. Powers. Rffective synaptic currents generated in cat spinal motoneurones by activating descending and peripheral afferent fibres. In: Alpha and Gamma Motor Systems, edited by A. Taylor and M. Gladden. New York: Plenum Press, 1995.
 31. Binder‐Macleod, S. A., and H. P. Clamann. Force output of cat motor units stimulated with trains of linearly varying frequency. J. Neurophysiol. 61: 208–217, 1989.
 32. Bohmer, G., K. Schmid, and W. Schauer. Evidence for an involvement of NMDA and non‐NMDA receptors in synaptic excitation of phrenic motoneurons in the rabbit. Neurosci. Lett. 130: 271–274, 1991.
 33. Botterman, B. R., and T. C. Cope. Motor‐unit stimulation patterns during fatiguing contractions of constant tension. J. Neurophysiol. 60: 1198–1214, 1988.
 34. Botterman, B. R., G. A. Iwamoto, and W. J. Gonyea. Gradation of isometric tension by different activation rates in motor units of cat flexor carpi radialis muscle. J. Neurophysiol. 56: 494–506, 1986.
 35. Botterman, B. R., and K. E. Tansey. Recruitment order and discharge patterns among pairs of motor units evoked by brainstem stimulation. Soc. Neurosci. Abstr. 15: 919, 1989.
 36. Brannstrom, T. Quantitative synaptology of functionally different types of cat medial gastrocnemius alphamotoneurons. J. Comp. Neurol. 330: 439–454, 1993.
 37. Bras, H., J. Destombes, P. Gogan, and S. Tyc‐Dumont. The dendrites of single brain‐stem motoneurons intracellularly labelled with horseradish peroxidase in the cat. An ultra‐structural analysis of the synaptic covering and the micro‐environment. Neuroscience 22: 971–981, 1987.
 38. Bras, H., P. Gogan, and S. Tyc‐Dumont. The dendrites of single brain‐stem motoneurons intracellularly labelled with horseradish peroxidase in the cat. Morphological and electrical differences. Neuroscience 22: 947–970, 1987.
 39. Bras, H., S. Korogod, Y. Driencourt, P. Gogan, and S. Tyc‐dumont. Stochastic geometry and electronic architecture of dendritic arborization of brain stem motoneuron. Eur. J. Neurosci. 5: 1485–1493, 1993.
 40. Brismar, T. Slow mechanism for sodium permeability inactivation in myelinated nerve fibre of Xenopus laevis. J. Physiol. (Lond.) 270: 283–297, 1977.
 41. Brock, L. G., J. S. Coombs, and J. C. Eccles. Intracellular recording from antidromically activated motoneurons. J. Physiol. (Lond.) 122: 429–461, 1953.
 42. Brodin, L., H. G. Trav'en, A. Lansner, P. Wallén, O. Ekeberg, and S. Grillner. Computer simulations of N‐methyl‐d‐aspartate receptor‐induced membrane properties in a neuron model. J. Neurophysiol. 66: 473–484, 1991.
 43. Brooks, V. B. (Ed). Handbook of Physiology, The Nervous System, Motor Control. Bethesda, MD: Am. Physiol. Soc., 1981.
 44. Brownstone, R., and H. Hultborn. Regulated and intrinsic properties of the motoneurone: effect on input‐output relations. In: Muscle Afferents and Spinal Control of Movement, edited by L. Jami, E. Pierrot‐Deselligny, and D. Zytnicki. New York: Pergamon Press, 1992, p. 175–181.
 45. Brownstone, R. M., L. M. Jordan, D. J. Kriellaars, B. R. Noga, and S. J. Shefchyk. On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat. Exp. Brain Res., 90: 441–455, 1992.
 46. Buchanan, J. T., L. E. Moore, R. Hill, P. Wallén, and S. Grillner. Synaptic potentials and transfer functions of lamprey spinal neurons. Biol. Cybern. 67: 123–131, 1992.
 47. Burke, R. E. Composite nature of the monosynaptic excitatory postsynaptic potential. J. Neurophysiol. 30: 1114–1137, 1967.
 48. Burke, R. E. Motor unit types of cat triceps surae muscle. J. Physiol. (Lond.) 193: 141–160, 1967.
 49. Burke, R. E. Motor units: anatomy, physiology, and functional organization. In: Handbook of Physiology, The Nervous System, Motor Control, edited by V. B. Brooks. Bethesda, MD: Am. Physiol. Soc., 1981, p. 345–422.
 50. Burke, R. E. Motor unit types: some history and unsettled issues. In: The Segmental Motor System, edited by M. D. Binder and L. M. Mendell. New York: Oxford University Press, 1990, p. 207–221.
 51. Burke, R. E., R. P. Dum, J. W. Fleshman, L. L. Glenn, T. A. Lev, M. J. O'Donovan, and M. J. Pinter. A HRP study of the relation between cell size and motor unit type in cat ankle extensor motoneurons. J. Comp. Neurol. 209: 17–28, 1982.
 52. Burke, R. E., L. Fedina, and A. Lundberg. Spatial synaptic distribution of recurrent and group Ia inhibitory systems in cat spinal motoneurones. J. Physiol. (Lond.) 214: 305–326, 1971.
 53. Burke, R. E., J. W. Fleshman, and I. Segev. Factors that control the efficacy of group Ia synapses in alpha‐motoneurons. J. Physiol. (Paris) 83: 133–140, 1988.
 54. Burke, R. E., E. Jankowska, and G. ten Bruggencate. A comparison of peripheral and rubrospinal input to slow and fast twitch motor units of triceps surae. J. Physiol. (Lond.) 207: 709–732, 1970.
 55. Burke, R. E., and P. G. Nelson. Accommodation to current ramps in motoneurons of fast and slow twitch motor units. Int. J. Neurosci. 1: 347–356, 1971.
 56. Burke, R. E., P. Rudomin, and F. E. Zajac. The effect of activation history on tension production by individual muscle units. Brain Res. 109: 515–529, 1976.
 57. Burke, R. E., W. Z. Rymer, and J. V. Walsh. Relative strength of synaptic input from short‐latency pathways to motor units of defined type in cat medial gastrocnemius. J. Neurophysiol. 39: 447–458, 1976.
 58. Calancie, B., and P. Bawa. Firing patterns of human flexor carpi radialis motor units during the stretch reflex. J. Neurophysiol. 53: 1179–1193, 1985.
 59. Calancie, B., and P. Bawa. Limitations of the spike triggered averaging technique. Muscle Nerve 9: 78–93, 1986.
 60. Calancie, B., and P. Bawa. Motor unit recruitment in humans. In: The Segmental Motor System, edited by M. D. Binder and L. M. Mendell. New York: Oxford University Press, 1990, p. 75–95.
 61. Calancie, B., M. Nordin, U. Wallin, and K. E. Hagbarth. Motor‐unit responses in human wrist flexor and extensor muscles to transcranial cortical stimuli. J. Neurophysiol. 58: 1168–1185, 1987.
 62. Calvin, W. H. Three modes of repetitive firing and the role of threshold time course between spikes. Brain Res. 59: 341–346, 1974.
 63. Cameron, W. E., D. B. Averill, and A. J. Berger. Quantitative analysis of the dendrites of cat phrenic motoneurons stained intracellularly with horseradish peroxidase. J. Comp. Neurol. 231: 91–101, 1985.
 64. Capaday, C., and R. B. Stein. Difference in the amplitude of the human soleus H reflex during walking and running. J. Physiol. (Lond.) 392: 513–522, 1987.
 65. Capaday, C., and R. B. Stein. A method for simulating the reflex output of a motoneuron pool. J. Neurosci. Methods 21: 91–104, 1987.
 66. Carp, J. S. Physiological properties of primate lumbar motoneurons. J. Neurophysiol. 68: 1121–1132, 1992.
 67. Carp, J. S., R. K. Powers, and W. Z. Rymer. Alterations in motoneuron properties induced by acute dorsal spinal hemisection in the decerebrate cat. Exp. Brain Res. 83: 539–548, 1991.
 68. Catterall, W. A. Localization of sodium channels in cultured neural cells. J. Neurosci. 1: 777–783, 1981.
 69. Catterall, W. A. Cellular and molecular biology of voltage‐gated sodium channels. Physiol. Rev. 72: S15–S47, 1992.
 70. Chanaud, C. M., and J. M. Macpherson. Functionally complex muscles of the cat hindlimb. 3. Differential activation within biceps‐femoris during postural perturbations. Exp. Brain Res. 85: 271–280, 1991.
 71. Chanaud, C. M., C. A. Pratt, and G. E. Loeb. Functionally complex muscles of the cat hindlimb. 5. The roles of histochemical fiber‐type regionalization and mechanical heterogeneity in differential muscle activation. Exp. Brain Res. 85: 300–313, 1991.
 72. Chandler, S. H., C. Hsaio, T. Inoue, and L. J. Goldberg. Electrophysiological properties of guinea pig trigeminal motoneurons recorded in vitro. J. Neurophysiol. 71: 129–145, 1994.
 73. Clamann, H. P., A. C. Ngai, C. G. Kukulka, and S. J. Goldberg. Motor pool organization in monosynaptic reflexes: responses in three different muscles. J. Neurophysiol. 50: 725–742, 1983.
 74. Clamann, H. P., and T. B. Schelhorn. Nonlinear force addition of newly recruited motor units in the cat hindlimb. Muscle Nerve 11: 1079–1089, 1988.
 75. Clark, B. D., S. M. Dacko, and T. C. Cope. Cutaneous stimulation fails to alter motor unit recruitment in the decerebrate cat. J. Neurophysiol. 70: 1433–1439, 1993.
 76. Clements, J. D., P. G. Nelson, and S. J. Redman. Intracellular tetraethylammonium ions enhance group Ia excitatory post‐synaptic potentials evoked in cat motoneurones. J. Physiol. (Lond.) 377: 267–282, 1986.
 77. Clements, J. D., and S. J. Redman. Cable properties of cat spinal motoneurones measured by combining voltage clamp, current clamp and intracellular staining. J. Physiol. (Lond.) 409: 63–87, 1989.
 78. Connor, J. A., and C. F. Stevens. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J. Physiol. (Lond.) 213: 21–30, 1971.
 79. Conradi, S. Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult cat. Acta Physiol. Scand. Suppl. 332: 5–48, 1969.
 80. Conradi, S., J. Kellerth, C. Berthold, and C. Hammarberg. Electron microscopic studies of serially sectioned cat spinal α‐motoneurons: IV. Motoneurons innervating slow‐twitch (type S) units of the soleus muscle. J. Comp. Neurol. 184: 769–782, 1979.
 81. Coombs, J. S., D. R. Curtis, and J. C. Eccles. The generation of impulses in motoneurones. J. Physiol. (Lond.) 139: 232–249, 1957.
 82. Coombs, J. S., J. C. Eccles, and P. Fatt. The specific ionic conductances and the ionic movements across the moto‐neuronal membrane that produce the inhibitory postsynaptic potential. J. Physiol. (Land.) 130: 326–373, 1955.
 83. Cope, T. C., S. C. Bobine, M. Fournier, and V. R. Edgerton. Soleus motor units in chronic spinal transected cats: physiological and morphological alterations. J. Neurophysiol. 55: 1202–1220, 1986.
 84. Cope, T. C., and B. D. Clark. Motor‐unit recruitment in the decerebrate cat—several unit properties are equally good predictors of order. J. Neurophysiol. 66: 1127–1138, 1991.
 85. Cope, T. C., and B. D. Clark. Motor‐unit recruitment in self‐reinnervated muscle. J. Neurophysiol. 70: 1787–1796, 1993.
 86. Cordo, P. J., and W. Z. Rymer. Motor‐unit activation patterns in lengthening and isometric contractions of hindlimb extensor muscles in the decerebrate cat. J. Neurophysiol. 47: 782–796, 1982.
 87. Cullheim, S. Relations between cell body size, axon diameter and axon conduction velocity of cat sciatic α‐motoneurons stained with horseradish peroxidase. Neurosci. Lett. 8: 17–20, 1978.
 88. Cullheim, S., J. W. Fleshman, L. L. Glenn, and R. E. Burke. Membrane area and dendritic structure in type‐identified triceps surae alpha motoneurons. J. Comp. Neurol. 255: 68–81, 1987.
 89. Cullheim, S., J. W. Fleshman, L. L. Glenn, and R. E. Burke. Three‐dimensional architecture of dendritic trees in type‐identified alpha‐motoneurons. J. Comp. Neurol. 255: 82–96, 1987.
 90. Cullheim, S., and J. Kellerth. A morphological study of the axons and recurrent axon collaterals of cat α‐motoneurones supplying different functional types of muscle unit. J. Physiol. (Lond.) 281: 301–313, 1978.
 91. Davies, L., A. W. Wiegner, and R. R. Young. Variation in firing order of human soleus motoneurons during voluntary and reflex activation. Bram Res. 602: 104–110, 1993.
 92. De Luca, C. J., R. S. LeFever, M. P. McCue, and A. P. Xenakis. Behavior of human motor units in different muscles during linearly varying contractions. J. Physiol. (Lond.) 329: 113–128, 1982.
 93. DeShutter, E. Computer software for development and simulation of compartmental models of neurons. Comput. Biol. Med. 19: 71–81, 1989.
 94. Desmedt, J. E., and E. Godaux. Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle. J. Physiol. (Lond.) 264: 373–393, 1977.
 95. Devasahayam, S. R., and T. G. Sandercock. Velocity of shortening of single motor units from rat soleus. J. Neurophysiol. 67: 1133–1145, 1992.
 96. Dodge, F. A., and J. W. Cooley. Action potential of the motoneuron. IBM J. Res. Dev. 17: 219–229, 1973.
 97. Dum, R. P., and T. T. Kennedy. Synaptic organization of defined motor unit types in cat tibialis anterior. J. Neurophysiol. 43: 1631–1644, 1980.
 98. Durand, D. The somatic shunt cable model for neurons. Biophys. J. 46: 645–653, 1984.
 99. Durand, J. NMDA actions on rat abducens motoneurones. Eur. J. Neurosci. 3: 621–633, 1991.
 100. Durand, J. Synaptic excitation triggers oscillations during NMDA receptor activation in rat abducens motoneurons. Eur. J. Neurosci. 5: 1389–1397, 1993.
 101. Durand, J., I. Engberg, and S. Tyc‐Dumont. l‐Glutamate and N‐methyl‐d‐asparatate actions on membrane potential and conductance of cat abducens motoneurones. Neurosci. Lett. 79: 295–300, 1987.
 102. Eccles, J. C., R. M. Eccles, A. Iggo, and M. Ito. Distribution of recurrent inhibition among motoneurons. J. Physiol. (Lond.) 159: 479–499, 1961.
 103. Ekeberg, O., P. Wallén, A. Lansner, H. Trav'en, L. Brodin, and S. Grillner. A computer based model for realistic simulations of neural networks. I. The single neuron and synaptic interaction. Biol. Cybern. 65: 81–90, 1991.
 104. Eken, T., and O. Kiehn. Bistable firing properties of soleus motor units in unrestrained rats. Acta Physiol. Scand. 136: 383–394, 1989.
 105. Elliott, P., and D. I. Wallis. Serotonin and l‐norepinephrine as mediators of altered excitability in neonatal rat motoneurons studied in vitro. Neuroscience 47: 533–544, 1992.
 106. Emonet‐Denand, E, C. C. Hunt, J. Petit, and B. Pollin. Proportion of fatigue‐resistant motor units in hindlimb muscles of cat and their relation to axonal conduction velocity. J. Physiol. (Lond.) 400: 135–158, 1988.
 107. Emonet‐Denand, E., Y. Laporte, and U. Proske. Summation of tension in motor units of the soleus muscle of the cat. Neurosci. Lett. 116: 112–117, 1990.
 108. Endo, K., T. Araki, and Y. Kawai. Contra‐ and ipsilateral cortical and rubral effects on fast and slow spinal motoneurons of the cat. Brain Res. 88: 91–98, 1975.
 109. Engberg, I., I. Tarnawa, J. Durand, and M. Ouardouz. An analysis of synaptic transmission to motoneurons in the cat spinal cord using a new selective receptor blocker. Acta Physiol. Scand. 148: 97–100, 1993.
 110. Enoka, R., and D. G. Stuart. Henneman's “size principle”: current issues. Trends Neurosci. 7: 266–228, 1984.
 111. Finkel, A. S., and S.J. Redman. The synaptic current evoked in cat spinal motoneurones by impulses in single group la axons. J. Physiol. (Lond.) 342: 615–632, 1983.
 112. Fisher, N. D., and A. Nistri. Substance P and TRH share a common effector pathway in rat spinal motoneurones: an in vitro electrophysiological investigation. Neurosci. Lett. 153: 115–119, 1993.
 113. Flatman, J. A., J. Durand, I. Engberg, and J. D. C. Lambert. Blocking the monosynaptic EPSP in spinal cord motoneurones with inhibitors of amino‐acid excitation. Neurol. Neurobiol. 24: 285–292, 1987.
 114. Fleshman, J. W., J. B. Munson, G. W. Sypert, and W. A. Friedman. Rheobase, input resistance, and motor‐unit type in medial gastrocnemius motoneurons in the cat. J. Neurophysiol. 46: 1326–1338, 1981.
 115. Fleshman, J. W., I. Segev, and R. B. Burke. Electrotonic architecture of type‐identified alpha‐motoneurons in the cat spinal cord. J. Neurophysiol. 60: 60–85, 1988.
 116. Forsythe, I. D., and S. J. Redman. The dependence of motoneurone membrane potential on extracellular ion concentrations studied in isolated rat spinal cord. J. Physiol. (Lond.) 404: 83–99, 1988.
 117. Frankenhaeuser, B., and A. B. Vallbo. Accommodation in myelinated nerve fibres of Xenopus laevis as computed on the basis of voltage clamp data. Acta Physiol. Scand. 63: 1–20, 1964.
 118. Freund, H.‐J., H. J. Budingen, and V. Dietz. Activity of single motor units from human forearm muscles during voluntary isometric contractions. J. Neurophysiol. 38: 933–946, 1975.
 119. Friedman, W. A., G. W. Sypert, J. B. Munson, and J. W. Fleshman. Recurrent inhibition in type‐identified motoneurons. J. Neurophysiol. 46: 1349–1359, 1981.
 120. Fuglevand, A. J., D. A. Winter, and A. E. Patla. Models of recruitment and rate coding organization in motor‐unit pools. J. Neuropbysiol. 70: 2470–2488, 1993.
 121. Fukushima, K., B. W. Peterson, and V. J. Wilson. Vestibulospinal, reticulospinal and interstitiospinal pathways in the cat. Prog. Brain Res. 50: 121–136, 1979.
 122. Fulton, B. P., and K. Walton. Electrophysiological properties of neonatal rat motoneurones studied in vitro. J. Physiol. (Lond.) 370: 651–678, 1986.
 123. Fuortes, M. G. F., K. Frank, and M. C. Becker. Steps in the production of motoneuron spikes. J. Gen. Physiol. 40: 735–752, 1957.
 124. Fyffe, R. E. Spatial distribution of recurrent inhibitory synapses on spinal motoneurons in the cat. J. Neuropbysiol. 65: 1134–1149, 1991.
 125. Fyffe, R. E. W., F. J. Alvarez, J. C. Pearson, D. Harrington, and D. E. Dewey. Modulation of motoneuron activity: distribution of glycine receptors and serotonergic inputs on motoneuron dendrites. Psychologist 36: A11, 1993.
 126. Gardiner, P. F. Physiological properties of motoneurons innervating different muscle unit types in rat gastrocnemius. J. Neuropbysiol. 69: 1160–1170, 1993.
 127. Garnett, R., and J. A. Stephens. Changes in the recruitment threshold of motor units produced by cutaneous stimulation in man. J. Physiol. (Lond.) 311: 463–473, 1981.
 128. Gemperline, J. J. Disturbances of muscle activation in hemiparetic spasticity in man: an experimental and theoretical investigation into the contribution of abnormal motor unit discharge patterns to muscular weakness. Ph.D, Northwestern University, 1993.
 129. Gottleib, G. L., and G. C. Agarwal. Effects of initial conditions on the Hoffman reflex. J. Neurol. Neurosurg. Psychiatry 34: 226–230, 1971.
 130. Granit, R., D. Kernell, and Y. Lamarre. Algebraical summation in synaptic activation of motoneurones firing within the ‘primary range’ to injected currents. J. Physiol. (Lond.) 187: 379–399, 1966.
 131. Granit, R., D. Kernell, and G. K. Shortess. Quantitative aspects of repetitive firing of mammalian motoneurones, caused by injected currents. J. Physiol. (Lond.) 168: 911–931, 1963.
 132. Granit, R., J. E. Pascoe, and G. Steg. The behavior of tonic α and γ motoneurones during stimulation of recurrent collaterals. J. Physiol. (Lond.) 138: 381–400, 1957.
 133. Granit, R., and B. Renkin. Net depolarization and discharge rate of motoneurones, as measured by recurrent inhibition. J. Physiol. (Lond.) 158: 461–475, 1961.
 134. Grillner, S., T. Hongo, and S. Lund. The vestibulospinal tract. Effects on alpha‐motoneurones in the lumbosacral spinal cord in the cat. Exp. Brain Res. 10: 94–120, 1970.
 135. Grimby, L., and J. Hannerz. Disturbances of voluntary recruitment order of low and frequency motor units on blockades of proprioceptive afferent activity. Acta Physiol. Scand. 96: 207–216, 1976.
 136. Gustafsson, B. Afterpotentials and transduction properties in different types of central neurones. Arch. Ital. Biol. 122: 17–30, 1984.
 137. Gustafsson, B., and M. J. Pinter. An investigation of threshold properties among cat spinal alpha‐motoneurones. J. Physiol. (Lond.) 357: 453–483, 1984.
 138. Gustafsson, B., and M. J. Pinter. Relations among passive electrical properties of lumbar alpha‐motoneurones of the cat. J. Physiol. (Lond.) 356: 401–431, 1984.
 139. Gustafsson, B., and M. J. Pinter. Factors determining the variation of the afterhyperpolarization duration in cat lumbar alpha‐motoneurones. Brain Res. 326: 392–395, 1985.
 140. Gutman, A. M. Bistability of dendrites. Int. J. Neural Syst. 1: 291–304, 1991.
 141. Gydikov, A., and D. Kosarov. Physiological characteristics of the tonic and phasic motor units in human muscles. In: Motor Control, edited by A. Gydikov, N. Tankov, and D. Kosarov. New York: Plenum Press, 1973, p. 75–94.
 142. Harada, Y., and T. Takahashi. The calcium component of the action potential in spinal motoneurones of the rat. J. Physiol. (Lond.) 335: 89–100, 1983.
 143. Harrison, P. J. The relationship between the distribution of motor unit mechanical properties and the forces due to recruitment and to rate coding for the generation of muscle force. Brain Res. 264: 311–315, 1983.
 144. Harrison, P. J., and A. Taylor. Individual excitatory postsynaptic potentials due to muscle spindle Ia afferents in cat triceps surae motoneurones. J. Physiol. (Lond.) 312: 455–470, 1981.
 145. Heckman, C. J. Computer simulations of the effects of different synaptic input systems on the steady‐state input‐output structure of the motoneuron pool. J. Neuropbysiol. 71: 1717–1739, 1994.
 146. Heckman, C. J., and M. D. Binder. Analysis of effective synaptic currents generated by homonymous Ia afferent fibers in motoneurons of the cat. J. Neuropbysiol. 60: 1946–1966, 1988.
 147. Heckman, C. J., and M. D. Binder. Neural mechanisms underlying the orderly recruitment of motoneurons. In: The Segmental Motor System, edited by M. D. Binder and L. M. Mendell. New York: Oxford University Press, 1990, p. 182–204.
 148. Heckman, C. J., and M. D. Binder. Analysis of Ia‐inhibitory synaptic input to cat spinal motoneurons evoked by vibration of antagonist muscles. J. Neuropbysiol. 66: 1888–1893, 1991.
 149. Heckman, C. J., and M. D. Binder. Computer simulation of the steady‐state input‐output function of the cat medial gastrocnemius motoneuron pool. J. Neuropbysiol. 65: 952–967, 1991.
 150. Heckman, C. J., and M. D. Binder. Computer simulations of motoneuron firing rate modulation. J. Neuropbysiol. 69: 1005–1008, 1993.
 151. Heckman, C. J., and M. D. Binder. Computer simulations of the effects of different synaptic input systems on motor unit recruitment. J. Neuropbysiol. 70: 1827–1840, 1993.
 152. Heckman, C. J., J. F. Miler, M. Munson, and W. Z. Rymer. Differences between steady‐state and transient postsynaptic potentials elicited by stimulation of the sural nerve. Exp. Brain Res. 91: 167–170, 1992.
 153. Heckman, C. J., J. L. Weytjens, and G. E. Loeb. Effect of velocity and mechanical history on the forces of motor units in the cat medial gastrocnemius muscle. J. Neuropbysiol. 68: 1503–1515, 1992.
 154. Henneman, E. Comments on the logical basis of muscle control. In: The Segmental Motor System, edited by M. D. Binder and L. M. Mendell. New York: Oxford University Press, 1990, p. vi–x.
 155. Henneman, E., H. P. Clamann, J. D. Gillies, and R. D. Skinner. Rank order of motoneurons within a pool: law of combination. J. Neuropbysiol. 37: 1338–1349, 1974.
 156. Henneman, E., and L. M. Mendell. Functional organization of motoneuron pool and its inputs. In: Handbook of Physiology, The Nervous System, Motor Control, edited by V. B. Brooks. Bethesda, MD: Am. Physiol. Soc., 1981, p. 423–507.
 157. Henneman, E., and C B. Olson. Relations between structure and function in the design of skeletal muscle. J. Neurophysiol. 28: 581–598, 1965.
 158. Henneman, E., G. Somjen, and D. O. Carpenter. Excitability and inhibitability of motoneurons of different sizes. J. Neurophysiol. 28: 599–620, 1965.
 159. Hille, B. Ionic Channels of Excitable Membranes, 2nd ed. Sunderland, MA: Sinauer Associates, Inc., 1992.
 160. Hodgkin, A. L., and A. F. Huxley. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (Lond.) 116: 500–544, 1952.
 161. Hodgkin, A. L., and S. Nakajima. The effect of diameter on the electrical constants of frog skeletal muscle fibres. J. Physiol. (Lond.) 221: 105–120, 1972.
 162. Hoffer, J. A., N. Sugano, G. E. Loeb, W. B. Marks, M. J. O'Donovan, and C. A. Pratt. Cat hindlimb motoneurons during locomotion. II. Normal activity patterns. J. Neurophysiol. 57: 530–553, 1987.
 163. Hongo, X, E. Jankowska, and A. Lundberg. The rubrospinal tract. I. Effects on alpha‐motoneurones innervating hindlimb muscles in cats. Exp. Brain Res. 7: 344–364, 1969.
 164. Hounsgaard, J., H. Hultborn, B. Jespersen, and O. Kiehn. Bistability of alpha‐motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5‐hydroxytryptophan. J. Physiol. (Lond.) 405: 345–367, 1988.
 165. Hounsgaard, J., and O. Kiehn. Serotonin‐induced bistability of turtle motoneurones caused by a nifedipine‐sensitive calcium plateau otential. J. Physiol. (Lond.) 414: 265–282, 1989.
 166. Hounsgaard, J., O. Kiehn, and I. Mintz. Response properties of motoneurones in a slice preparation of the turtle spinal cord. J. Physiol. (Lond.) 398: 575–589, 1988.
 167. Hounsgaard, J., and J. Midtgaard. Dendrite processing in more ways than one. Trends Neurosci. 12: 313–315, 1989.
 168. Hounsgaard, J., and O. Kiehn. Calcium spikes and calcium plateaux evoked by differential polarization in dendrites of turtle mononeurones in vitro. J. Physiol. (Lond.) 468: 245–259, 1993.
 169. Howe, J. R., and J. M. Ritchie. Multiple kinetic components of sodium channel inactivation in rabbit Schwann cells. J. Physiol. (Lond.) 455: 529–566, 1992.
 170. Hultborn, H., R. Katz, and R. Mackel. Distribution of recurrent inhibition within a motor nucleus. II. Amount of recurrent inhibition in motoneurons to fast and slow units. Acta Physiol. Scand. 134: 363–374, 1988.
 171. Hultborn, H., and O. Kiehn. Neuromodulation of vertebrate motor neuron membrane properties. Curr. Opin. Neurobiol. 2: 770–775, 1992.
 172. Hultborn, H., S. Lindstrom, and H. Wigstrom. On the function of recurrent inhibition in the spinal cord. Exp. Brain Res. 37: 399–403, 1979.
 173. Iansek, R., and S. J. Redman. The amplitude, time course and charge of unitary excitatory post‐synaptic potentials evoked in spinal motoneurone dendrites. J. Physiol. (Lond.) 234: 665–688, 1973.
 174. Jack, J. J., S. J. Redman, and K. Wong. The components of synaptic potentials evoked in cat spinal motoneurones by impulses in single group Ia afferents. J. Physiol. (Lond.) 321: 65–96, 1981.
 175. Jack, J. J. B., D. Noble, and R. W. Tsien. Electric Current Flow in Excitable Cells. Oxford: Clarendon Press, 1975.
 176. Jacobs, B. L., and C. A. Fornal. 5‐HT and motor control: a hypothesis. Trends Neurosci. 6: 346–352, 1993.
 177. Jahr, C. E., and K. Yoshioka. Ia afferent excitation of motoneurones in the in vitro new‐born rat spinal cord is selectively antagonized by kynurenate. J. Physiol. (Lond.) 370: 515–530, 1986.
 178. Jankowska, E. Interneuronal relay in spinal pathways from proprioceptors. Prog. Neurobiol. 38: 335–378, 1992.
 179. Jodkowski, J. S., F. Viana, X E. Dick, and A. J. Berger. Repetitive firing properties of phrenic motoneurons in the cat. J. Neurophysiol. 60: 687–702, 1988.
 180. Joyce, G. C., P. M. H. Rack, and D. R. Westbury. The mechanical properties of cat soleus muscle during controlled lengthening and shortening movements. J. Physiol. (Lond.) 204: 461–474, 1969.
 181. Kalb, R. G., M. S. Lidow, M. J. Halsted, and S. Hockfield. N‐Methyl‐d‐aspartate receptors are transiently expressed in the developing spinal cord ventral horn. Proc. Natl. Acad. Sci. U. S. A. 89: 8502–8506, 1992.
 182. Kanda, K., R. E. Burke, and B. Walmsley. Differential control of fast and slow twitch motor units in the decerebrate cat. Exp. Brain. Res. 29: 57–74, 1977.
 183. Kanosue, K., M. Yoshida, K. Akazawa, and K. Fuji. The number of active motor units and their firing rates in voluntary contraction of human brachialis muscle. Jpn. J. Physiol. 29: 427–444, 1979.
 184. Katakura, N., and S. H. Chandler. An iontophoretic analysis of the pharmacologic mechanisms responsible for trigeminal motoneuronal discharge during masticatory‐like activity in the guinea pig. J. Neurophysiol. 63: 356–369, 1990.
 185. Katakura, N., and S. H. Chandler. Iontophoretic analysis of the pharmacologic mechanisms responsible for initiation and modulation of trigeminal motoneuronal discharge evoked by intra‐oral afferent stimulation. Brain Res. 549: 66–77, 1991.
 186. Kellerth, J., C. Berthold, and S. Conradi. Electron microscopic studies of serially sectioned cat spinal a‐motoneurons: III. Motoneurons innervating fast‐twitch (type FR) units of the gastrocnemius muscle. J. Comp. Neurol. 184: 755–768, 1979.
 187. Kellerth, J., S. Conradi, and C. Berthold. Electron microscopic studies of serially sectioned cat spinal α‐motoneurons: V. Motoneurons innervating fast‐twitch (type FF) units of the gastrocnemius muscle. J. Comp. Neurol. 214: 451–458, 1983.
 188. Kernell, D. The delayed depolarization in cat and rat motoneurons. Prog. Brain Res. 12: 42–55, 1964.
 189. Kernell, D. The adaptation and the relation between discharge frequency and current strength of cat lumbosacral motoneurones stimulated by long‐lasting injected currents. Acta Physiol. Scand. 65: 65–73, 1965.
 190. Kernell, D. High frequency repetitive firing of cat lumbosacral motoneurones stimulated by long‐lasting injected currents. Acta Physiol. Scand. 65: 74–86, 1965.
 191. Kernell, D. The limits of firing frequency in cat lumbosacral motoneurones possessing different time course of afterhy‐perpolarization. Acta Physiol. Scand. 65: 87–100, 1965.
 192. Kernell, D. Input resistance, electrical excitability and size of ventral horn cells in cat spinal cord. Science 152: 1637–1640, 1966.
 193. Kernell, D. The repetitive discharge of motoneurones. In: Muscular Afferents and Motor Control. Nobel Symp. I, edited by R. Granit. Stockholm: Almqvist and Wiksell, 1966, p. 351–362.
 194. Kernell, D. The repetitive impulse discharge of a simple neurone model compared to that of spinal motoneurones. Brain Res. 11: 685–687, 1968.
 195. Kernell, D. Synaptic conductance changes and the repetitive impulse discharge of spinal motoneurones. Brain Res. 15: 291–294, 1970.
 196. Kernell, D. Rhythmic properties of motoneurones innervating muscle fibres of different speed in m. gastrocnemius medialis of the cat. Brain Res. 160: 159–162, 1979.
 197. Kernell, D. Functional properties of spinal motoneurons and gradation of muscle force. Adv. Neurol. 39: 213–226, 1983.
 198. Kernell, D., O. Eerbeek, and B. A. Verhey. Relation between isometric force and stimulus rate in cat's hindlimb motor units of different twitch contraction time. Exp. Brain Res. 50: 220–227, 1983.
 199. Kernell, D., and H. Hultborn. Synaptic effects on recruitment gain: a mechanism of importance for the input‐output relations of motoneurone pools? Brain Res. 507: 176–179, 1990.
 200. Kernell, D., and A. W. Monster. Threshold current for repetitive impulse firing in motoneurones innervating muscle fibres of different fatigue sensitivity in the cat. Brain Res. 229: 193–196, 1981.
 201. Kernell, D., and A. W. Monster. Time course and properties of late adaptation in spinal motoneurones of the cat. Exp. Brain Res. 46: 191–196, 1982.
 202. Kernell, D., and H. Sjoholm. Repetitive impulse firing: comparisons between neurone models based on ‘voltage clamp equations’ and spinal motoneurones. Acta Physiol. Scand. 87: 40–56, 1973.
 203. Kernell, D., and B. Zwaagstra. Input conductance, axonal conduction velocity and cell size among hindlimb motoneurones of the cat. Brain Res. 204: 311–26, 1980.
 204. Kernell, D., and B. Zwaagstra. Dendrites of cat's spinal motoneurones: relationship between stem diameter and predicted input conductance. J. Physiol. (hand.) 413: 255–269, 1989.
 205. Kernell, D., and B. Zwaagstra. Size and remoteness: two relatively independent parameters of dendrites, as studied for spinal motoneurones of the cat. J. Physiol. (Lond.) 413: 233–254, 1989.
 206. Kiehn, O. Plateau potentials and active integration in the ‘final common pathway’ for motor behaviour. Trends Neurosci. 14: 68–73, 1991.
 207. Kiehn, O., E. Erdal, T. Eken, and T. Bruhn. Selective depletion of spinal monoamines changes for the soleus EMG from a tonic to a more phasic pattern J. Physiol. (Lond.) in press, 1995.
 208. Kiehn, O., and R. M. Harris‐Warrick. 5‐HT modulation of hyperpolarization‐activated inward current and calcium‐dependent outward current in a crustacean motor neuron. J. Neurophysiol. 68: 496–508, 1992.
 209. Kiehn, O., and R. M. Harris‐Warrick. Serotonergic stretch receptors induce plateau properties in a crustacean motor neuron by a dual‐conductance mechanism. J. Neurophysiol. 68: 485–495, 1992.
 210. Koch, C. Cable theory in neurons with active, linearized membranes. Biol. Cybern. 50: 15–33, 1984.
 211. Krnjević, K., Y. Lamour, J. F. MacDonald, and A. Nistri. Effects of some divalent cations on motoneurones in cats. Can. J. Physiol. Pharmacol. 57: 944–956, 1979.
 212. Krnjević, K., and A. Lisiewicz. Injections of calcium ions into spinal motoneurones. J. Physiol. (Lond.) 225: 363–390, 1972.
 213. Krnjević, K., E. Puil, and R. Werman. EGTA and motoneuronal after‐potentials. J. Physiol. (Lond.) 275: 199–223, 1978.
 214. Kukulka, C. G., and H. P. Clamann. Comparison of the recruitment and discharge properties of motor units in human brachial biceps and adductor pollicis during isometric contractions. Brain Res. 219: 45–55, 1981.
 215. Kuno, M., and R. Llinas. Enhancement of synaptic action in chromatolyzed motoneurones of the cat. J. Physiol. (Lond.) 210: 807–821, 1970.
 216. LaBella, L. A., J. P. Kehler, and D. A. McCrea. A differential synaptic input to the motor nuclei in triceps surae from the caudal and lateral cutaneous sural nerves. J. Neurophysiol. 61: 291–301, 1989.
 217. Larkman, P. M., and J. S. Kelly. Ionic mechanisms mediating 5‐hydroxytryptamine‐ and noradrenaline‐evoked depolarization of adult rat facial motoneurones. J. Physiol. (Lond.) 456: 473–490, 1992.
 218. Lev‐Tov, A., J. P. Miller, R. E. Burke, and W. Rall. Factors that control amplitude of EPSPs in dendritic neurons. J. Neurophysiol. 50: 399–412, 1983.
 219. Liddell, E. G. T., and C. S. Sherrington. Recruitment and some other factors of reflex inhibition. Proc. R. Soc. Lond. B 97: 488–518, 1925.
 220. Lindsay, A. D., and M. D. Binder. Distribution of effective synaptic currents underlying recurrent inhibition in cat triceps surae motoneurons. J. Neurophysiol. 65: 168–177, 1991.
 221. Lindsay, A. D., and J. L. Feldman. Modulation of respiratory activity of neonatal rat phrenic motoneurones by serotonin. J. Physiol. (Lond.) 461: 213–233, 1993.
 222. Matthews, P. B. C. Observations on the automatic compensation of reflex gain on varying the pre‐existing level of motor discharge in man. J. Physiol. (Lond.) 374: 73–90, 1986.
 223. Mayer, M. L., and G. L. Westbrook. The physiology of excitatory amino acids in the vertebrate central nervous system. Prog. Neurobiol. 28: 197–276, 1987.
 224. Milner‐Brown, H. S., R. B. Stein, and R. Yemm. The contractile properties of human motor units during voluntary isometric contractions. J. Physiol. (Lond.) 228: 285–306, 1973.
 225. Milner‐Brown, H. S., R. B. Stein, and R. Yemm. The orderly recruitment of human motor units during voluntary isometric contractions. J. Physiol. (Lond.) 230: 359–370, 1973.
 226. Monster, A. W. Firing rate behavior of human motor units during isometric voluntary contraction: relation to unit size. Brain Res. 171: 349–354, 1979.
 227. Monster, A. W., and H. Chan. Isometric force production by motor units of extensor digitorum communis muscle in man. J. Neurophysiol. 40: 1432–1443, 1977.
 228. Moore, J. A., and K. Appenteng. The membrane properties and firing characteristics of rat jaw‐elevator motoneurones. J. Physiol. (Lond.) 423: 137–153, 1990.
 229. Moore, J. A., and K. Appenteng. The morphology and electrical geometry of the rat jaw‐elevator motoneurones. J. Physiol. (Lond.) 440: 325–343, 1991.
 230. Moore, J. W., N. Stockbridge, and M. Westerfield. On the site of impulse initiation in a neurone. J. Physiol. (Lond.) 336: 301–311, 1983.
 231. Moore, J. W., and M. Westerfield. Action potential propagation and threshold parameters in inhomogeneous regions of squid axons. J. Physiol. (Lond.) 336: 301–311, 1983.
 232. Moore, L. E., and J. T. Buchanan. The effects of neurotransmitters on the integrative properties of spinal neurons in the lamprey. J. Exp. Biol. 175: 89–114, 1993.
 233. Moore, L. E., R. H. Hill, and S. Grillner. Voltage‐clamp frequency domain analysis of NMDA‐activated neurons. J. Exp. Biol. 175: 59–87, 1993.
 234. Moore, L. E., K. Yoshii, and B. N. Christensen. Transfer impedances between different regions of branched excitable cells. J. Neurophysiol. 59: 689–705, 1988.
 235. Mosfeldt‐Laursen, A., and J. C. Rekling. Electrophysiological properties of hypoglossal motoneurons of guinea‐pigs studied in vitro. Neuroscience 30: 619–637, 1989.
 236. Munson, J. B. Synaptic inputs to type‐identified motor units. In: The Segmental Motor System, edited by M. D. Binder and L. M. Mendell. New York: Oxford University Press, 1990, p. 291–307.
 237. Munson, J. B., J. W. Fleshman, and G. W. Sypert. Properties of single‐fiber spindle group II EPSPs in triceps surae motoneurons. J. Neurophysiol. 44: 713–725, 1980.
 238. Mynlieff, M., and K. G. Beam. Characterization of voltage‐dependent calcium currents in mouse motoneurons. J. Neurophysiol. 68: 85–92, 1992.
 239. Nardone, A., C. Romano, and M. Schieppati. Selective recruitment of high‐threshold human motor units during voluntary isotonic lengthening of active muscle. J. Physiol. (Land.) 409: 451–471, 1989.
 240. Nelson, P. G., and R. E. Burke. Delayed depolarization in cat spinal motoneurons. Exp. Neurol. 17: 16–26, 1967.
 241. Nelson, P. G., and K. Frank. Orthodromically produced changes in motoneuronal extracellular fields. J. Neurophysiol. 27: 928–941, 1964.
 242. Nicoll, A., A. Larkman, and C. Blakemore. Modulation of EPSP shape and efficacy by intrinsic membrane conductances in rat neocortical pyramidal neurons in vitro. J. Physiol. (Lond.) 468: 693–710, 1993.
 243. Nishimura, Y., P. C. Schwindt, and W. E. Crill. Electrical properties of facial motoneurons in brainstem slices from guinea pig. Brain Res. 502: 127–142, 1989.
 244. Nistri, A., N. D. Fisher, and M. Gumell. Block by the neuropeptide TRH of an apparently novel K+ conductance of rat motoneurones. Neurosci. Lett. 120: 25–30, 1990.
 245. Partridge, L. D., and L. A. Benton. Muscle, the motor, In: Handbook of Physiology, The Nervous System, Motor Control, edited by V. B. Brooks. Bethesda, MD: Am. Physiol. Soc., 1981, p. 43–106.
 246. Petit, J., M. Chua, and C. C. Hunt. Maximum shortening speed of motor units of various types in cat lumbrical muscles. J. Neurophysiol. 69: 442–448, 1993.
 247. Petit, J., G. M. Filippi, F. Emonet‐Denand, C. C. Hunt, and Y. Laporte. Changes in muscle stiffness produced by motor units of different types in peroneus longus muscle of cat. J. Neurophysiol. 63: 190–197, 1990.
 248. Pinco, M., and Lev‐Tov, A. Synaptic excitation of alphamotoneurons by dorsal root afferents in the neonatal rat spinal cord. J. Neurophysiol. 70: 406–417, 1993.
 249. Pinter, M. J., R. L. Curtis, and M. J. Hosko. Voltage threshold and excitability among variously sized cat hindlimb motoneurons. J. Neurophysiol. 50: 644–657, 1983.
 250. Powers, R. K. A variable‐threshold motoneuron model that incorporates time‐dependent and voltage‐dependent potassium and calcium conductances. J. Neurophysiol. 70: 246–262, 1993.
 251. Powers, R. K., and M. D. Binder. Determination of afferent fibers mediating oligosynaptic group I input to cat medial gastrocnemius motoneurons. J. Neurophysiol. 53: 518–529, 1985.
 252. Powers, R. K., and M. D. Binder. Distribution of oligosynaptic group I input to the cat medial gastrocnemius motoneuron pool. J. Neurophysiol. 53: 497–517, 1985.
 253. Powers, R. K., and M. D. Binder. Effects of low‐frequency stimulation on the tension‐frequency relations of fast‐twitch motor units in the cat. J. Neurophysiol. 66: 905–918, 1991.
 254. Powers, R. K., and M. D. Binder. Summation of motor unit tensions in the tibialis posterior muscle of the cat under isometric and nonisometric conditions. J. Neurophysiol. 66: 1838–1846, 1991.
 255. Powers, R. K., and M. D. Binder. Quantitative analysis of motoneurone firing rate modulation in response to simulated synaptic inputs. In: Alpha and Gamma Motor Systems, edited by A. Taylor and M. Gladden. New York: Plenum Press, in press, 1995.
 256. Powers, R. K., and M. D. Binder. Effective synaptic current and motoneuron firing rate modulation. J. Neurophysiol. 74: 793–801, 1995.
 257. Powers, R. K., F. R. Robinson, M. A. Konodi, and M. D. Binder. Summation of effective synaptic currents and firing rate modulation in cat triceps surae motoneurons produced by concurrent stimulation of different synaptic input systems. Soc. Neurosci. Abstr. 17: 645, 1991.
 258. Powers, R. K., F. R. Robinson, M. A. Konodi, and M. D. Binder. Effective synaptic current can be estimated from measurements of neuronal discharge. J. Neurophysiol. 68: 964–968, 1992.
 259. Powers, R. K., F. R. Robinson, M. A. Konodi, and M. D. Binder. Distribution of rubrospinal synaptic input to cat triceps surae motoneurons. J. Neurophysiol. 70: 1460–1468, 1993.
 260. Powers, R. K., and W. Z. Rymer. Effects of acute dorsal spinal hemisection on motoneuron discharge in the medial gastrocnemius of the decerebrate cat. J. Neurophysiol. 59: 1540–1556, 1988.
 261. Pratt, C. A., C. M. Chanaud, and G. E. Loeb. Functionally complex muscles of the cat hindlimb. 4. Intramuscular distribution of movement command signals and cutaneous reflexes in broad, bifunctional thigh muscles. Exp. Brain Res. 85: 281–299, 1991.
 262. Pratt, C. A., and G. E. Loeb. Functionally complex muscles of the cat hindlimb. 1. Patterns of activation across sartorius. Exp. Brain Res. 85: 243–256, 1991.
 263. Puil, E., B. Gimbarzevsky, and I. Spigelman. Primary involvement of K+ conductance in membrane resonance of trigeminal root ganglion neurons. J. Neurophysiol. 59: 77–89, 1988.
 264. Puil, E., H. Meiri, and Y. Yarom. Resonant behavior and frequency preferences of thalamic neurons. J. Neurophysiol. 71: 575–582, 1994.
 265. Rack, P. M. H., and D. R. Westbury. The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J. Physiol. (Lond.) 204: 443–460, 1969.
 266. Rajaofetra, N., J. L. Ridet, P. Poulat, L. Marlier, F. Sandillon, M. Geffard, and A. Privat. Immunocytochemical mapping of noradrenergic projections to the rat spinal cord with an antiserum against noradrenaline. J. Neurocytol. 21: 481–494, 1992.
 267. Rall, W. A statistical theory of monosynaptic input‐output relations. J. Cell. Comp. Physiol. 46: 373–412, 1955.
 268. Rall, W. Branching dendritic trees and motoneuron membrane resistivity. Exp. Neurol. 1: 491–527, 1959.
 269. Rall, W. Core conductor theory and cable properties of neurons. In: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons, edited by E. R. Kandel. Bethesda, MD: Am. Physiol. Soc., 1977, p. 39–97.
 270. Rall, W., R. E. Burke, W. R. Holmes, J. J. Jack, S. J. Redman, and I. Segev. Matching dendritic neuron models to experimental data. Physiol. Rev. 72, No. 4 (Suppl.): 5159–5186, 1992.
 271. Rall, W., R. E. Burke, T. G. Smith, P. G Nelson, and K. Frank. Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J. Neurophysiol. 30: 1169–1193, 1967.
 272. Rall, W., and C. C. Hunt. Analysis of reflex variability in terms of partially correlated excitability fluctuations in a population of motoneurons. J. Gen. Physiol. 39: 397–422, 1956.
 273. Redman, S. A. quantitative approach to the integrative function of dendrites. In: International Review of Physiology: Neurophysiology, edited by R. Porter. Baltimore: University Park Press, 1976, p. 1–35.
 274. Redman, S. J., E. M. McLachlan, and G. D. Hirst. Nonuniform passive membrane properties of rat lumbar sympathetic ganglion cells. J. Neurophysiol. 57: 633–644, 1987.
 275. Redman, S. J., and B. Walmsley. The time course of synaptic potentials evoked in cat spinal motoneurones at identified group Ia synapses. J. Physiol. (Lond.) 343: 117–133, 1983.
 276. Rekling, J. C. Interaction between thyrotropin‐releasing hormone (TRH) and NMDA‐receptor‐mediated responses in hypoglossal motoneurones. Brain Res. 578: 289–296, 1992.
 277. Richter, D. W., W. R. Schlue, K. H. Mauritz, and A. C. Nacimiento. Comparison of membrane properties of the cell body and the initial part of the axon of phasic motoneurones in the spinal cord of the cat. Exp. Brain Res. 21: 193–206, 1974.
 278. Riek, S., and P. Bawa. Recruitment of motor units in human forearm extensors. J. Neurophysiol. 68: 100–108, 1992.
 279. Romaiguere, P., J.‐P. Vedel, S. Pagni, and A. Zenatti. Physiological properties of the motor units of the wrist extensor muscles in man. Exp. Brain Res. 78: 51–61, 1989.
 280. Romaiguere, P., J. P. Vedel, and S. Pagni. Fluctuations in motor unit recruitment threshold during slow isometric contractions of wrist extensor muscles in man. Neurosci. Lett. 103: 50–55, 1989.
 281. Romaiguere, P., J. P. Vedel, and S. Pagni. Effects of tonic vibration reflex on motor unit recruitment in human wrist extensor muscles. Brain Res. 602: 32–40, 1993.
 282. Rose, P. K., and P. Brennan. Somatic shunts in neck motoneurons of the cat. Soc. Neurosci. Abstr. 15: 922, 1989.
 283. Rose, P. K., S. A. Keirstead, and S. J. Vanner. A quantitative analysis of the geometry of cat motoneurons innervating neck and shoulder muscles. J. Comp. Neurol. 238: 89–107, 1985.
 284. Rose, P. K., and H. M. Neuber. Morphology and frequency of axon terminals on the somata, proximal dendrites, and distal dendrites of dorsal neck motoneurons in the cat. J. Comp. Neurol. 307: 259–280, 1991.
 285. Rose, P. K., and S. J. Vanner. Differences in somatic and dendritic specific membrane resistivity of spinal motoneurons: an electrophysiological study of neck and shoulder motoneurons in the cat. J. Neurophysiol. 60: 149–166, 1988.
 286. Rosenblueth, A., N. Wiener, W. Pitts, and J. Garcia‐Ramos. A statistical analysis of synaptic excitation. J. Cell. Comp. Physiol. 34: 173–205, 1949.
 287. Rudomin, P. Presynaptic control of synaptic effectiveness of muscle spindle and tendon organ afferents in the mammalian spinal cord. In: The Segmental Motor System, edited by M. D. Binder and L. M. Mendell. New York: Oxford University Press, 1990, p. 349–380.
 288. Rudy, B. Diversity and ubiquity of K channels. Neuroscience 25: 729–749, 1988.
 289. Sah, P. Role of calcium influx and buffering in the kinetics of Ca(2+) activated K+ current in rat vagal motoneurons. J. Neurophysiol. 68: 2237–2247, 1992.
 290. Saha, S., K. Appenteng, and T. F. Batten. Light and electron microscopical localisation of 5‐HT‐immunoreactive boutons in the rat trigeminal motor nucleus. Brain Res. 559: 145–148, 1991.
 291. Sawczuk, A. Adaptation in sustained motoneuron discharge PhD., University of Washington, 1993.
 292. Sawczuk, A., and M. D. Binder. Reduction of Na+‐K+ activity does not reduce the late adaptation of motoneuron discharge. Soc. Neurosci. Abstr. 18: 512, 1992.
 293. Sawczuk, A., and M. D. Binder. Reduction of the AHP with Mn++ decreases the initial adaptation, but increases the late adaptation in rat hypoglossal motoneuron discharge. Physiologist 36: A23, 1993.
 294. Sawczuk, A., R. K. Powers, and M. D. Binder. Intrinsic properties of motoneurons: implications for muscle fatigue. In: Fatigue: Neural and Muscular Mechanisms, edited by S. Gandevia, R. Enoka, A. McComas, D. Stuart, and C. Thomas. New York: Plenum, 1995, p. 123–134.
 295. Sawczuk, A., R. K. Powers, and M. D. Binder. Spike‐frequency adaptation studied in hypoglossal motoneurons of the rat J. Neurophysiol. 73: 1799–1810, 1995.
 296. Schlue, W. R., D. W. Richter, K. H. Mauritz, and A. C. Nacimiento. Mechanisms of accommodation to linearly rising currents in cat spinal motoneurones. J. Neurophysiol. 37: 310–315, 1974.
 297. Schwindt, P. C. Membrane‐potential trajectories underlying motoneuron rhythmic firing at high rates. J. Neurophysiol. 36: 434–439, 1973.
 298. Schwindt, P. C., and W. E. Crill. A persistent negative resistance in cat lumbar motoneurons. Brain Res. 120: 173–178, 1977.
 299. Schwindt, P. C., and W. H. Calvin. Membrane potential trajectories between spikes underlying motoneuron rhythmic firing. J. Neurophysiol. 35: 311–325, 1972.
 300. Schwindt, P. C., and W. H. Calvin. Equivalence of synaptic and injected current in determining the membrane potential trajectory during motoneuron rhythmic firing. Brain Res. 59: 389–394, 1973.
 301. Schwindt, P. C., and W. H. Calvin. Nature of conductances underlying rhythmic firing in cat spinal motoneurons. J. Neurophysiol. 36: 955–973, 1973.
 302. Schwindt, P. C., and W. E. Crill. Effects of barium on cat spinal motoneurons studied by voltage clamp. J. Neurophysiol. 44: 827–846, 1980.
 303. Schwindt, P. C., and W. E. Crill. Properties of a persistent inward current in normal and TEA‐injected motoneurons. J. Neurophysiol. 43: 1700–1724, 1980.
 304. Schwindt, P. C., and W. E. Crill. Role of a persistent inward current in motoneuron bursting during spinal seizures. J. Neurophysiol. 43: 1296–1318, 1980.
 305. Schwindt, P. C., and W. E. Crill. Differential effects of TEA and cations on outward ionic currents of cat motoneurons. J. Neurophysiol. 46: 1–16, 1981.
 306. Schwindt, P. C., and W. E. Crill. Negative slope conductance at large depolarizations in cat spinal motoneurons. Brain Res. 207: 471–475, 1981.
 307. Schwindt, P. C., and W. E. Crill. Factors influencing motoneuron rhythmic firing: results from a voltage‐clamp study. J. Neurophysiol. 48: 875–890, 1982.
 308. Scott, R. H., H. A. Pearson, and A. C. Dolphin. Aspects of vertebrate neuronal voltage‐activated calcium currents and their regulation. Prog. Neurobiol. 36: 485–520, 1991.
 309. Scroggs, R. S., S. M. Todorovic, E. G. Anderson, and A. P. Fox. Variation in IH, IIR, and IIFAK between acutely isolated adult rat dorsal root ganglion neurons of different size. J. Neurophysiol. 71: 271–279, 1994.
 310. Segev, I., J. W. J. Fleshman, and R. E. Burke. Computer simulation of group Ia EPSPs using morphologically realistic models of cat alpha‐motoneurons. J. Neurophysiol. 64: 648–660, 1990.
 311. Sernagor, E., Y. Yarom, and R. Werman. Sodium‐dependent regenerative responses in dendrites of axotomized motoneurons in the cat. Proc. Natl. Acad. Sci. U. S. A. 83: 7966–7970, 1986.
 312. Shapovalov, A. I. Extrapyramidal monosynaptic and disynaptic control of mammalian alpha‐motoneurons. Brain Res. 40: 105–115, 1972.
 313. Shinoda, Y., T. Ohgaki, T. Futami, and Y. Sugiuchi. Structural basis for three‐dimensional coding in the vestibulospinal reflex. Ann. N. Y. Acad. Sci. 545: 216–227, 1988.
 314. Shinoda, Y., T. Ohgaki, T. Futami, and Y. Sugiuchi. Vestibular projections to the spinal cord: the morphology of single vestibulospinal axons. Prog. Brain Res. 76: 17–27, 1988.
 315. Slot, P. J., and T. Sinkjaer. Simulations of the alpha motoneuron pool electromyogram reflex at different preactivation levels in man. Biol. Cybern. 70: 351–358, 1994.
 316. Smith, J. L., B. Betts, V. R. Edgerton, and R. Zernicke. Rapid ankle extension during paw shakes: selective recruitment of fast ankle extensors. J. Neurophysiol. 43: 612–620, 1980.
 317. Spain, W. J., P. C. Schwindt, and W. E. Crill. Post‐inhibitory excitation and inhibition in layer V pyramidal neurones from cat sensorimotor cortex. J. Physiol. (Lond.) 434: 609–626, 1991.
 318. Spruston, N., and D. Johnston. Perforated patch‐clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J. Neurophysiol. 67: 508–529, 1992.
 319. Stafstrom, C. E., P. C. Schwindt, M. C. Chubb, and W. E. Crill. Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. J. Neurophysiol. 53: 153–170, 1985.
 320. Staley, K. J., T. S. Otis, and I. Mody. Membrane properties of dentate gyrus granule cells: comparison of sharp micro‐electrode and whole‐cell recordings. J. Neurophysiol. 67: 1346–1358, 1992.
 321. Stauffer, E. K., D. G. Watt, A. Taylor, R. M. Reinking, and D. G. Stuart. Analysis of muscle receptor connections by spike‐triggered averaging. 2. Spindle group II afferents. J. Neurophysiol. 39: 1393–1402, 1976.
 322. Stefani, E., and A. B. Steinbach. Resting potential and electrical properties of frog slow muscle fibers. Effect of different external solutions. J. Physiol. (Lond.) 203: 383–401, 1969.
 323. Stein, R. B., and R. Bertoldi. The size principle: A synthesis of neurophysiological data. In: Progress in Clinical Neurophysiology. Motor Unit Types, Recruitment and Plasticity in Health and Disease, edited by J. E. Desmedt. Basel: Karger, 1981, p. 85–96.
 324. Stephens, J. A., R. M. Reinking, and D. G. Stuart. The motor units of cat medial gastrocnemius: electrical and mechanical properties as a function of muscle length. J. Morphol. 146: 495–512, 1975.
 325. Stuart, G. J., and S. J. Redman. Voltage dependence of Ia reciprocal inhibitory currents in cat spinal motoneurones. J. Physiol. (Lond.) 420: 111–125, 1990.
 326. Sypert, G. W., and J. B. Munson. Basis of segmental motor control: motoneuron size or motor unit type? Neurosurgery 8: 608–621, 1981.
 327. Takahashi, T. Inward rectification in neonatal rat spinal motoneurones. J. Physiol. (Lond.) 423: 47–62, 1990.
 328. Takahashi, T. Membrane currents in visually identified motoneurones of neonatal rat spinal cord. J. Physiol. (Lond.) 423: 27–46, 1990.
 329. Takahashi, T., and A. J. Berger. Direct excitation of rat spinal motoneurones by serotonin. J. Physiol. (Lond.) 423: 63–76, 1990.
 330. Tanji, J., and M. Kato. Firing rate of individual motor units in voluntary contraction of abductor digiti minimi muscle in man. Exp. Neurol. 40: 771–783, 1973.
 331. Tax, A. A. M., and J. J. Denier van der Gon. A model for neural control of gradation of muscle force. Biol. Cybern. 65: 227–234, 1991.
 332. ter Haar Romeny, B. M., J. J. van der Gon, and C. C. Gielen. Relation between location of a motor unit in the human biceps brachii and its critical firing levels for different tasks. Exp. Neurol. 85: 631–650, 1984.
 333. Terzuolo, C. A., and T. Araki. An analysis of intra‐ versus extracellular potential changes associated with activity of single spinal motoneurons. Ann. N.Y. Acad. Sci. 94: 547–558, 1961.
 334. Thomas, C. K., B. Bigland‐Ritchie, G. Westling, and R. S. Johansson. A comparison of human thenar motor‐unit properties studied by intraneural motor‐axon stimulation and spike‐triggered averaging. J. Neurophysiol. 64: 1347–1351, 1990.
 335. Thomas, C. K., R. S. Johansson, G. Westling, and B. Bigland‐Ritchie. Twitch properties of human thenar motor units measured in response to intraneural motor‐axon stimulation. J. Neurophysiol. 64: 1339–1346, 1990.
 336. Thomas, C. K., B. H. Ross, and B. Calancie. Human motor‐unit recruitment during isometric contractions and repeated dynamic movements. J. Neurophysiol. 57: 311–324, 1987.
 337. Thomas, C. K., B. H. Ross, and R. B. Stein. Motor‐unit recruitment in human first dorsal interosseous muscle for static contractions in three different directions. J. Neurophysiol. 55: 1017–1029, 1986.
 338. Toft, E., T. Sinkjter, S. Andreassen, and K. Larsen. Mechanical and electromyographic responses to stretch of the human ankle extensors. J. Neurophysiol. 65: 1402–1410, 1991.
 339. Traub, R. D. Motoneurons of different geometry and the size principle. Biol. Cybern. 25: 163–176, 1977.
 340. Traub, R. D., and R. Llinas. The spatial distribution of ionic conductances in normal and axotomized motoneurons. Neuroscience 2: 829–849, 1977.
 341. Ulfhake, B., U. Arvidsson, S. Cullheim, T. Hokfelt, E. Brodin, A. Verhofstad, and T. Visser. An ultrastructural study of 5‐hydroxytryptamine‐, thyrotropin‐releasing hormone‐ and substance P‐immunoreactive axonal boutons in the motor nucleus of spinal cord segments L7–S1 in the adult cat. Neuroscience 23: 917–929, 1987.
 342. Ulfhake, B., and S. Cullheim. Postnatal development of cat hind limb motoneurons. III: changes in size of motoneurons supplying the triceps surae muscle. J. Comp. Neurol. 278: 103–20, 1988.
 343. Ulfhake, B., and J. O. Kellerth. A quantitative light microscopic study of the dendrites of cat spinal alpha‐motoneurons after intracellular staining with horseradish peroxidase. J. Comp. Neurol. 202: 571–583, 1981.
 344. Ulfhake, B., and J. O. Kellerth. A quantitative morphological study of HRP‐labelled cat alpha‐motoneurones supplying different hind limb muscles. Brain Res. 264: 1–19, 1983.
 345. Ulfhake, B., and J. O. Kellerth. Electrophysiological and morphological measurements in cat gastrocnemius and soleus alpha‐motoneurones. Brain Res. 307: 167–179, 1984.
 346. Umemiya, M., and A. Berger. Properties and function of low‐ and high‐voltage activated Ca2+ channels in hypoglossal motoneurons. J. Neurosci. 14: 5652–5660, 1994.
 347. Vallbo, A. B. Accommodation related to the inactivation of the sodium permeability in single myelinated nerve fibres from Xenopus laevis. Acta Physiol. Scand. 61: 429–444, 1964.
 348. van Zuylen, E. J., J. J. Denier van der Gon, and C. C. A. M. Gielen. Coordination and inhomogeneous activation of human arm muscles during isometric torques. J. Neurophysiol. 60: 1523–1548, 1988.
 349. Viana, F., D. A. Bayliss, and A. J. Berger. Calcium conductances and their role in the firing behavior of neonatal rat hypoglossal motoneurons. J. Neurophysiol. 69: 2137–2149, 1993.
 350. Viana, F., D. A. Bayliss, and A. J. Berger. Multiple potassium conductances and their role in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. J. Neurophysiol. 69: 2150–2163, 1993.
 351. Wallén, P., J. T. Buchanan, S. Grillner, R. H. Hill, J. Christenson, and T. Hokfelt. Effects of 5‐hydroxytryptamine on the after hyperpolarization, spike frequency regulation, and oscillatory membrane properties in lamprey spinal cord neurons. J. Neurophysiol. 61: 759–768, 1989.
 352. Wallén, P., O. Ekeberg, A. Lansner, K. Brodin, H. Traven, and S. Grillner. A computer‐based model for realistic simulations of neural networks. II. The segmental network generating locomotor rhythmicity in the lamprey J. Neurophysiol. 68: 1939–1350, 1992.
 353. Wallén, P., and S. Grillner. N‐Methyl‐d‐aspartate receptor‐induced, inherent oscillatory activity in neurons active during fictive locomotion in the lamprey. J. Neurosci. 7: 2745–2755, 1987.
 354. Walmsley, B., J. A. Hodgson, and R. E. Burke. Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats. J. Neurophysiol. 41: 1203–1216, 1978.
 355. Walmsley, B., and U. Proske. Comparison of stiffness of soleus and medial gastrocnemius muscle in cats. J. Neurophysiol. 46: 250–259, 1981.
 356. Walton, K., and B. P. Fulton. Ionic mechanisms underlying the firing properties of rat neonatal motoneurons studied in vitro. Neuroscience 19: 669–683, 1986.
 357. Westcott, S. L. Comparison of vestibulospinal synaptic input and Ia afferent synaptic input in cat triceps surae motoneurons. Ph.D, University of Washington, 1993.
 358. Westcott, S. L., R. K. Powers, F. R. Robinson, and M. D. Binder. Distribution of vestibulospinal synaptic input to cat triceps surae motoneurons. Exp. Brain Res. 107: in press, 1995.
 359. Westling, G., R. S. Johansson, C. K. Thomas, and B. Bigland‐Ritchie. Measurement of contractile and electrical properties of single human thenar motor units in response to intraneural motor‐axon stimulation. J. Neurophysiol. 64: 1331–1338, 1990.
 360. White, S. R., and S. J. Fung. Serotonin depolarizes cat spinal motoneurons in situ and decreases motoneuron after‐hyperolarizing potentials. Brain Res. 502: 205–213, 1989.
 361. Windhorst, U., T. M. Hamm, and D. G. Stuart. On the function of muscle and reflex partitioning. Brain Behav. Sci. 12: 629–681, 1989.
 362. Wuerker, R. B., A. M. McPhedran, and E. Henneman. Properties of motor units in a heterogeneous pale muscle (m. gastrocnemius) in the cat. J. Neurophysiol. 28: 85–99, 1965.
 363. Yoshii, K., L. E. Moore, and B. N. Christensen. Transfer impedances between different regions of branched excitable cells. J. Neurophysiol. 59: 706–716, 1988.
 364. Zajac, F. E., and J. S. Faden. Relationship among recruitment order, axonal conduction velocity, and muscle‐unit properties of type‐identified motor units in cat plantaris muscle. J. Neurophysiol. 53: 1303–1322, 1985.
 365. Zajac, F. E., and J. S. Young. Discharge properties of hind‐limb motoneurons in decerebrate cats during locomotion induced by mesencephalic stimulation. J. Neurophysiol. 43: 1221–1235, 1980.
 366. Zengel, J. E., S. A. Reid, G. W. Sypert, and J. B. Munson. Membrane electrical properties and prediction of motor‐unit type of medial gastrocnemius motoneurons in the cat. J. Neurophysiol. 53: 1323–1344, 1985.
 367. Zhang, L., and K. Krnjevi'c. Effects of 4‐aminopyridine on the action potential and the after‐hyperpolarization of cat spinal motoneurons. Can. J. Physiol. Pharmacol. 64: 1402–1406, 1986.
 368. Zhang, L., and K. Krnjevi'c. Effects of intracellular injections of phorbol ester and protein kinase C on cat spinal motoneurons in vivo. Neurosci. Lett. 77: 287–292, 1987.
 369. Zhang, L., and K. Krnjevi'c. Intracellular injection of Ca2+ chelator does not affect spike repolarization of cat spinal motoneurons. Brain Res. 462: 174–180, 1988.
 370. Ziskind‐Conhaim, L. NMDA receptors mediate poly‐ and monosynaptic potentials in motoneurons of rat embryos. J. Neurosci. 10: 125–135, 1990.
 371. Zwaagstra, B., and D. Kernell. The duration of after‐hyperpolarization in hindlimb alpha motoneurones of different sizes in the cat. Neurosci. Lett. 19: 303–307, 1980.

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Marc D. Binder, C. J. Heckman, Randall K. Powers. The Physiological Control of Motoneuron Activity. Compr Physiol 2011, Supplement 29: Handbook of Physiology, Exercise: Regulation and Integration of Multiple Systems: 3-53. First published in print 1996. doi: 10.1002/cphy.cp120101