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Spinal Neurons and Synapses

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Abstract

The sections in this article are:

1 I. Motoneurons
1.1 A. Alpha Motoneurons
1.2 Gamma Motoneurons
2 II. Interneurons
2.1 A. General Considerations
2.2 B. Functionally Identified Interneuron Systems
3 III. Tract Cells
3.1 General Considerations
3.2 B. Specific Systems
4 IV. Intraspinal Primary Afferents and Presynaptic Modulation
4.1 A. General Considerations
4.2 B. Intrinsic Properties of Intraspinal Afferents
4.3 C. Evidence for the Existence of Primary Afferent Depolarization (PAD)
4.4 D. Afferent Terminals Are Subjected Only to Depolarizing Input
4.5 E. Interneurons Are Involved in the Mechanism of PAD Generation
4.6 F. Possible Mechanisms of PAD Production by Interneurons
4.7 G. Changes in Synaptic Transmission Related to PAD
4.8 H. Possible Mechanisms for Presynaptic Inhibition
4.9 I. Consequences of Presynaptic Modulation of Synaptic Transmission
4.10 J. Organization of PAD
5 V. Concluding Comment
Figure 1. Figure 1.

Composite drawings of Golgi‐stained sections of cat spinal cord showing neurons and terminal arborizations of segmental afferent fibers. A: cross section showing axonal arborizations on the left and dendritic neuropile on the right. A‐C, terminations of coarse dorsal root afferents; D and E, axons from white funiculi terminating in basal dorsal horn and medial ventral horn. Neurons drawn on the right illustrate the variety in size and dendritic architecture found in segmental neurons. B: sagittal section of lumbosacral cord of the cat (plane of section indicated on inset). Roman numerals denote Rexed laminae . A, dorsal column fibers; B, interneuron of lamina VI; C and D, motoneurons with radial dendritic patterns; E, motoneuron with predominately longitudinal dendrites; F, fibers of ventral column; a, descending axonal microbundle ending in terminal arborization (a′); b, intermingling of primary afferent and ventral column terminal arborizations; c, presumed cutaneous afferent arborization in substantia gelatinosa (c′); d, local collaterals presumed to originate from an interneuron.

From Scheibel & Scheibel ; originally published by University of California Press; reprinted by permission of the Regents of the University of California. From Scheibel & Scheibel
Figure 2. Figure 2.

Cell size and electrotonic architecture in cat alpha motoneurons. Graphs on the left show the correlation of cell input resistance (upper, ordinate scaled as reciprocal of RN) and axonal conduction velocity (lower, ordinate) with total cell membrane area (abscissae, same scale for both graphs). Each point represents a different cell, marked with Procion dye after electrophysiological study. Graph on right illustrates the decrease in membrane area in one motoneuron with increasing electrotonic distance from the soma (abscissa in units of electrotonic length, λ). The ordinate shows the increment in membrane area found for each 0.1 λ increment in electronic length, summed for all dendritic branches. The decrease in membrane area per 0.1 λ increment is largely due to tapering of the dendritic branches up to about 0.8 λ from the soma and is due largely to termination of various branches beyond this point.

From data of Barrett & Crill . Data from Barrett ; see also
Figure 3. Figure 3.

Some evidence relating to action potentials in motoneuron dendrites. A‐D: antidromic action potentials in cat alpha motoneurons. A, superimposed intracellular records of antidromic spikes during passage of a 10‐nA hyperpolarizing step, which shows inflection between A and B spike components (curved arrow) and exaggeration in the second of 2 antidromic spikes (B, curved arrow; same cell and calibrations as A). Straight arrow in A denotes humplike delayed depolarization that occurred in an all‐or‐none manner in some antidromic spikes. An analogous all‐or‐none late spike component is shown in C (curved arrow), obtained by an extracellular electrode near a single antidromically invaded motoneuron conditioned by phasic synaptic input. The delayed depolarization disappeared following the second of 2 closely spaced antidromic spikes (B, straight arrow), and in another cell when antidromic spikes with a well‐developed delayed depolarization (D, curved arrow) was conditioned with inhibitory synaptic input (superimposed records of spikes with and without synaptic conditioning). E and F: all‐or‐none spikelike potentials superimposed on composite Ia EPSP's in an apparently normal alpha motoneuron with membrane potential of −60 mV. Upper traces, Photographically superimposed intracellular records; lower traces, potential at the dorsal root entry. Larger Ia input volley (F) produced spikelike responses with multiple components; note cord dorsum volley. The animal was normal, but records resemble observations in chromatolyzed motoneurons (see text). The spikelike responses (only rarely observed in normal animals) may reflect nonpropagated action potentials in parts of the dendritic tree. (Unpublished records of R. E. Burke and L. Fedina.)

A, B, and D from Nelson & Burke ; C from Nelson & Frank
Figure 4. Figure 4.

Composite and single‐fiber monosynaptic EPSP's produced by group Ia afferents in cat alpha motoneurons. A, superimposed intracellular records (lower trace; upper trace is cord dorsum potential) of composite Ia EPSP in plantaris motoneuron produced by electrical stimulation of the whole plantaris nerve (ventral roots cut). B, single‐sweep records of EPSP's produced by 2 individual Ia afferent fibers (a and b) during stretch of the plantaris muscle in the same motoneuron as in A. Time scale same in A and B, but records 10 times greater amplification in B. Note markedly different time courses of the single‐fiber EPSP's. C, computer‐averaged records of single‐fiber EPSP's produced by a single group Ia afferent in 6 different motoneurons (a‐f), all recorded on the same time base with equal amplification. The time courses vary widely, despite production by the same afferent.

A and B from Burke . From Mendell & Henneman
Figure 5. Figure 5.

Shape variations in single‐fiber Ia EPSP's. A: plot of EPSP shape indices. Rise time on the abscissa; half‐width (i.e., the duration at 1/2 amplitude) on the ordinate for presumed single‐fiber Ia EPSP's in a large sample of afferent fiber‐motoneuron combinations, •, EPSP's in extensor motoneurons; ○, EPSP's in flexor cells. The wide range in shapes and the positive correlation between rise time and half‐width are best explained by differences in spatial position of synaptic contacts established by the different afferents on postsynaptic cells (see text). B: histogram of the electrotonic distance (λ) between the motoneuron soma and the estimated site of Ia afferent contact in 236 combinations of presumed single Ia afferent and alpha motoneuron, derived from study of the EPSP shape indices as in A. Note the fall‐off in frequency of contacts closer than 0.2 λ and beyond 0.6 λ, the latter in keeping with the decrease in incremental membrane area in the more distal dendritic tree (see Fig. C).

From Jack et al.
Figure 6. Figure 6.

Evidence related to conductance changes underlying the Ia EPSP. A: linear summation of synchronous composite Ia EPSP's generated in a medial gastrocnemius (MG) motoneuron by different sets of Ia afferents; LG‐Sol, lateral gastrocnemius plus soleus nerve. Computer‐averaged intracellular records showing algebraic addition of the separate MG and LG‐Sol EPSP's (•) superimposed on the actual EPSP produced by synchronous stimulation of both nerves (Both). Such linear PSP addition, which is not uncommon, would require spatial dispersion of chemical synaptic sites (see text). B: averaged EPSP records as in A, but from a flexor digitorum longus (FDL) motoneuron in which synchronous generation of FDL and MG EPSP's (Both) produced a significantly smaller composite EPSP than the algebraic addition of the FDL and MG EPSP's (•). Such nonlinear addition, while less commonly found than the records in A, imply a conductance change mechanism underlying the Ia EPSP (see text). C: effect of depolarizing current on a Ia EPSP recorded in an alpha motoneuron. Lowermost record shows superimposed sweeps without current, and the other single traces illustrate biphasic EPSP reversal with increasing (from bottom to top) depolarizing current injected into the cell.

From Burke . From Smith et al.
Figure 7. Figure 7.

Unit EPSP components in single‐fiber Ia EPSP's. A, single sweep intracellular records from a medial gastrocnemius (MG) motoneuron during repeated electrical stimulation of a dissected filament of MG nerve. Some trials produced a small EPSP (arrows) with latency within the rise time of the composite MG EPSP (B), while other trials produced no detectable EPSP's (i.e., failures of response). C, histogram of the amplitudes of EPSP responses as in A, for about 200 trials. Number of failures is indicated by the vertical line at 0 mV. Horizontal arrows and dotted line represent the calculated amplitude distribution expected if the observed EPSP's were composed of unit components with mean amplitude about 0.2 mV, occurring with probability described by the Poisson distribution function and an assumed (best fit) variance. Vertical arrows, multiples of the estimated unit EPSP amplitude. The small EPSP's (• in A) conform to the expected size of the unit EPSP components. D, exceptionally large single‐fiber EPSP's recorded in a plantaris motoneuron during stretch of the plantaris muscle (base line slightly oblique). Inflections (arrows) suggest some asynchrony between unit components, present in about 2% of the trials. E, histogram of amplitudes of 1,000 single‐fiber EPSP's as in D. Failures occurred 120 times per 1,000 responses (horizontal line on ordinate). Theoretical distribution fitted to the observed data using a Poisson distribution function and best fit variance is indicated by the horizontal arrow (expected number of failures) and the dotted curve. Roman numerals and vertical arrows denote multiples of the expected unit component amplitude (ca. 0.7 mV). Delayed components in D (arrows) and the lowermost response in D conform to this amplitude and are assumed to represent all‐or‐none unit EPSP's.

From Kuno . From Burke
Figure 8. Figure 8.

Maximum amplitude of composite Ia EPSP's produced in medial gastrocnemius (MG) motoneurons by electrical stimulation of the MG nerve. Graph at top shows the relation between EPSP amplitude (abscissa) and motoneuron input resistance (ordinate, logarithmic scale). Each symbol denotes a different cell — ○, motoneurons innervating fast‐twitch muscle units; •, cells innervating slow‐twitch units (cf. Table ). Despite considerable scatter, there is a significant positive correlation between EPSP size and cell input resistance. Note that motoneurons of slow‐twitch units have generally greater input resistance. Histograms below the graph show the distributions of MG Ia EPSP amplitudes (abscissa on same scale as graph at top) in motoneurons identified as innervating muscle units of types FF, FR, or S (see Table ). Mean of each distribution denoted by arrows.

Data from Burke . Data from Burke et al.
Figure 9. Figure 9.

Monosynaptic vestibulospinal tract (VST) effects in cat alpha motoneurons. A, intracellular (I‐C) records of monosynaptic EPSP in a gastrocnemius‐soleus (G‐S) motoneuron produced by electrical stimulation of Deiters' nucleus (ND) or of the ipsilateral ventral cord (thoracic; iVQ). Arrival of the volley at the lumbosacral cord is signaled by deflections in the cord dorsum (CDP) and extracellular (X‐C) records. Latency between stimulus and EPSP onset for Deiters' (t2) and ventral quadrant (t1) stimulation is plotted against the conduction distance in B for 6 different G‐S motoneurons. The slopes indicate maximal conduction velocities for the responsible lateral VST axons of 90–148 m/s, and the latencies extrapolate to a segmental latency (ordinate intercept) of 0.4–0.7 ms, indicating monosynaptic connection. C, intracellular recordings from 2 back motoneurons (interspinales, IS), showing presumed monosynaptic inhibitory postsynaptic potentials (IPSP's) produced by electrical stimulation of the medial VST in the brain stem. Conduction distance in each case is given below the records. D, upper graph, latency of IPSP onset (ordinate) plotted against conduction distance (abscissa) for a group of back motoneurons; UIC, unidentified cell. Slope of the line indicates an average conduction velocity of 69.3 m/s for the responsible axons, and the ordinate intercept of 0.93 ms suggests probable monosynaptic connection. Arrows around the intercept point denote 90% confidence limits. Lower graph in D shows the latency between the positive peak of the medial VST tract potential (visible in the intracellular records and due to the fastest conducting fibers) and the IPSP onset, again plotted against conduction distance (abscissa). The positive slope suggests that fibers producing the monosynaptic IPSP's conduct more slowly than the fastest fibers activated by the electrical stimulus.

From Grillner et al. . From Wilson et al.
Figure 10. Figure 10.

Frequency potentiation in descending monosynaptic EPSP. A: computer‐averaged records of corticospinal tract (CST) EPSP's produced by single (1) and identical double (2) stimuli to motor cortex, recorded in a lumbosacral motoneuron in monkey. Subtraction of 1 from 2 yields record of enhanced second EPSP alone (. B: facilitation of second corticomotoneuronal EPSP (ordinate) as a function of interval following a conditioning EPSP in 4 different monkey motoneurons. C: same relation, obtained by averaging data from 24 motoneurons; vertical bars, 1 SE. D: intracellular records from cat gastrocnemius‐soleus motoneuron showing 2 successive monosynaptic EPSP's produced by Deiters' nucleus stimulation. No evident facilitation of second EPSP at either interval. E: amplitude of second of 2 lateral VST EPSP's (as in D) at different conditioning intervals, with no evident facilitation of the second as compared to the first.

From Muir & Porter . From Grillner et al.
Figure 11. Figure 11.

Composite and single‐fiber disynaptic group Ia IPSP's in cat alpha motoneurons. A: computer‐averaged intracellular records of single‐fiber IPSP's in 3 different motoneurons (MNs, 1–3) produced by spike activity in a single Ia inhibitory interneuron (lowermost record; Ia IN). B: composite IPSP in motoneuron 3 produced by stimulation of Ia afferents in the quadriceps nerve; Ia volley at cord dorsum in lower trace. Same time base as A but less amplification; note similar time course for single‐fiber and composite IPSP's. C: intracellular record (V) of composite Ia IPSP in cat motoneuron, together with the in‐phase component of membrane impedance (Z) measured with a bridge circuit. Arrow marks stimulus artifact; same time base as A and B. Impedance change probably reflects rather accurately the time course of IPSP conductance (see text). [From Smith et al. .] D and E: effect of intracellular injection of Cl on composite (left) and single‐fiber (right) Ia IPSP's in same motoneuron. Bottom trace in E on left shows cord dorsum record; bottom trace in E on right shows spike activity in Ia interneuron. Chloride reversal of composite IPSP (right, photographically superimposed traces) was biphasic but that of the single‐fiber IPSP (left, computer‐averaged records) was not (see text). Note different time scales for composite and single‐fiber records.

From Jankowska & Roberts . From Jankowska & Roberts
Figure 12. Figure 12.

Recurrent and disynaptic Ia IPSP's in cat motoneurons. A, recurrent IPSP in motoneuron produced by increasing (from top to bottom) stimulus intensities to L7 ventral root. Fourth record from the top represents maximal stimulation, shown again on slower time base in B. Arrows in upper 2 records of A indicate apparent component IPSP's (probably not unit PSP's), presumably produced by repetitive firing in Renshaw interneurons (cf. Fig. ). Note prolonged duration of IPSP decay. C, intracellular records (sulfate‐filled electrode) of disynaptic Ia IPSP and recurrent IPSP in a motoneuron showing reversal at same membrane potential (ca. −80 mV) during current passage. [From Coombs et al. .] D, intracellular records (upper traces; lower traces are from cord dorsum) of Ia and recurrent IPSP's in a motoneuron, recorded with KCl‐filled micropipette. Both IPSP's were initially hyperpolarizing (uppermost pair of records, no current), but the Ia IPSP reversed more readily with hyperpolarizing current and consequent injection of small amounts of Cl (increasing from top to bottom). After cessation of current, additional Cl had been injected and the Ia IPSP showed biphasic reversal while the recurrent IPSP remained hyperpolarizing (lowermost pair of records, no current; see text).

From Eccles et al. . From Burke et al.
Figure 13. Figure 13.

Gamma motoneurons. A: histogram of the least soma diameter of ventral horn neurons in the gastrocnemius‐soleus motor nucleus of the cat spinal cord, measured in 20‐μm sections from cell profiles exhibiting a nucleolus. Neurons with least soma diameters of 30‐μm or less are presumed to be gamma motoneurons. B: intracellular record (superimposed sweeps) of antidromic action potential in a gamma motoneuron (conduction velocity 30 m/s) with stimulus strength straddling threshold for the axon. Inflection between A and B spike components denoted by arrow. C: intracellular record (lower trace; upper trace from cord dorsum) from flexor digitorum longus gamma motoneuron showing absence of detectable Ia EPSP with maximum Ia volley. D: antidromic action potential showing brief early component of the afterhyperpolarization. E: record from another gamma cell showing prolonged small‐amplitude afterhyperpolarization with high amplification and slow time base.

From Van Buren & Frank . B‐E from Eccles et al.
Figure 14. Figure 14.

Effect of input interaction on transmission of disynaptic Ia IPSP to alpha motoneurons. A: Convergence of descending excitatory and recurrent inhibitory systems onto an Ia inhibitory interneuron projecting to an alpha motoneuron (the cell with intracellular electrode). B: intracellular superimposed records (upper traces; lower traces from cord dorsum) from a knee flexor motoneuron in cat. Records in C show indicated portion of traces in B (dashed lines) on faster time base. Just‐suprathreshold stimulation of quadriceps Ia afferents (Q 1.1) produced minimal disynaptic Ia IPSP. Conditioning this input by preceding stimulus to Deiters' nucleus (ND + Q) greatly enhanced the Ia IPSP in the motoneuron. Deiters' nucleus stimulation alone at 80 μA (ND 80) produced minimal synaptic effect. Preceding the paired Ia and Deiters' stimuli by a shock to the L5 and L6 ventral roots then suppressed the Ia IPSP (L5 + L6 VR → ND + Q), presumably by inhibiting firing of the Ia interneurons involved.

From Hultborn & Udo
Figure 15. Figure 15.

Records from interneurons monosynaptically excited by group Ia afferents. A: intracellular records (upper traces; lower traces from cord dorsum) from 2 lumbar interneurons (Cell 1 and Cell 2), showing monosynaptic EPSP's produced in each by increasing stimulation (given in multiples of threshold) of hamstring muscle nerves (ABSm, anterior biceps and semimembranosus; PBSt, posterior biceps and semitendinosus). Cell 1, located dorsomedial to motor nucleus (hatched area in C), had typical recurrent IPSP after stimulation of L7 ventral root (VR L7). Cell 2 was located more dorsally in intermediate nucleus (small dots in C) and had no recurrent IPSP (VR L6 + 7). Cell 1 thus was presumed to project to alpha motoneurons while projection of cell 2 was unidentified (see text). B: extracellular records (upper traces; lower traces (CDP) from cord dorsum) of presumed Ia inhibitory interneuron showing monosynaptic firing to maximum group I volley in adductor muscle nerve (Add 2.4 T), which was suppressed by prior stimulation of L6 ventral root (Cond. VR L6). Decreased group I input (Add 1.2 T) was unable to fire the cell, but prior conditioning with 4 volleys to red nucleus (Cond. RuST) provided convergent facilitation and cell fired monosynaptically (cf. Fig. A). [From Hultborn & Santini .] C: L7 segment gray matter showing location of interneurons with convergence of monosynaptic Ia excitation and recurrent inhibition (the Ia inhibitory interneurons; large open and closed circles) and Ia excited cells without recurrent inhibition (small dots). [From Hultborn et al. .]

From Hultborn et al.
Figure 16. Figure 16.

Records from Renshaw interneurons. A, Quasi‐intracellular records from Renshaw cell showing high‐frequency discharge to increasing stimulation (from top to bottom) of L7 ventral root. Maximum response (lowest record) shown on expanded time base in B. C, intracellular records from a Renshaw interneuron after spike inactivation, showing graded EPSP with increasing ventral root stimulation (from top to bottom). Graded initial fast response presumed to represent part of the EPSP (see text). Prolonged decay phase of the maximum EPSP (3rd record) is shown on slower time base in D, with greater amplification.

Records A‐D from Eccles et al. .] E‐G: spike frequency (ordinate) versus time (abscissa) in Renshaw cell responding to antidromic volleys (arrows) in 3 different muscle nerves (ipsilateral dorsal roots cut). BST, biceps and semitendinosus; MGS, medial gastrocnemius and soleus; SMAB, semimembranosus and anterior biceps. Early (nicotinic) discharge in E was followed by a pause in firing, which was in turn followed by a prolonged moderate (muscarinic) increase in discharge rate (see text). Early firing and smaller pause produced by MGS stimulation (F) shown on faster time base. Stimulation of SMAB nerve (G) produced only a decrease in Renshaw cell firing. [E‐G from Ryall
Figure 17. Figure 17.

Intracellular records from DSCT neurons. A: antidromic spike (upper trace; lower trace from cord dorsum) in L4 DSCT cell after stimulation of its axon in the ipsilateral dorsolateral quadrant in lower thoracic cord; 4‐nA hyperpolarizing current during record. B: higher gain records from same cell with and without hyperpolarizing current, showing humplike delayed depolarization (arrow) following antidromic spikes. C: intracellular records (upper traces; lower traces from cord dorsum) from DSCT cell firing to increasing (from top to bottom) group I volleys in quadriceps muscle nerve. Increasing stimulation produced increasing amplitude of postspike hump (arrows; possibly a delayed depolarization, see text), resulting in second spike in lower 2 records. D: records from the same neuron as shown in C but now during passage of transmembrane hyperpolarizing current to prevent cell firing. Note the graded, large‐amplitude composite EPSP's produced by increasing (from top to bottom) group I input. With largest input volley (lowermost record), spikes were produced on some trials, again followed by a large delayed depolarization as in C. [C and D from Kuno & Miyahara .]

From Eide et al.
Figure 18. Figure 18.

Single‐fiber group I EPSP's in DSCT neurons. A: intracellular records from DSCT cell during increasing stretch of the soleus muscle. Regularly recurring EPSP's can be attributed to single group Ia afferents. Note large amplitudes and similar shapes. B: amplitude histogram of 151 EPSP's produced in a DSCT cell by repeated firing in one group Ia afferent, as in A. Mean amplitude was 4.3 mV, and the distribution was symmetrical, without failures of occurrence (cf. Fig. ). C: relation between the amplitude (ordinate) and rise time (abscissa) in group I EPSP's as shown in A. Little correlation was evident, and all EPSP's had relatively brief rise time (<0.9 ms; cf. Fig. ).

From Eide et al.
Figure 19. Figure 19.

Occurrence of monosynaptic EPSP and disynaptic IPSP produced by same set of group Ia afferents in a spinal border cell belonging to ventral spinocerebellar tract (VSCT). A‐F: intracellular records (upper traces; lower traces from cord dorsum) during increasing electrical stimulation, noted in multiples of threshold, of quadriceps (Q) muscle nerve. The monosynaptic EPSP, apparently pure at 1.14 times threshold, was followed at higher stimulus strengths by a disynaptic IPSP also produced by the same Ia afferents. Both synaptic effects appeared to be maximal at 1.5 times threshold. Diagram on left shows the presumed set of connections accounting for this observation (see text). Mn, motoneuron. [From Lundberg .]

From Lundberg & Weight
Figure 20. Figure 20.

Some indices of primary afferent depolarization (PAD). A: cord dorsum potential (CDP) and potential change recorded along a distally cut dorsal root filament (DRP) of L6, produced by 3 volleys (at 200/s) in group I muscle afferents. B: mean antidromic excitability (•) and variance of excitability (○) in gastrocnemius Ia afferents, with electrical stimulation of the afferent arborizations in the cord. The changes with time were produced by stimulation of toe extensor (PL‐FDHL) group I afferents at various conditioning‐testing intervals. Note that time course of negative DRP in A and excitability increase in B are similar. [From Rudomin & Dutton .] C and D: transmembrane depolarization recorded within a quadriceps group Ia fiber in the dorsal horn (record I‐C), produced by 2 (C) or 4 (D) volleys in PBST (posterior biceps and tendinosus) muscle afferents (incoming volleys appear in cord dorsum trace, record CDP). There was no detectable extracellular potential immediately outside the fiber (record X‐C) with 2 volleys, but with 4 a small positive potential change was evident (D). [From Eccles et al. .]

From Burke et al.
Figure 21. Figure 21.

Some indices of primary afferent hyperpolarization (PAH). A and B: photographic (A) and computer‐averaged (B) records of positive dorsal root potential (DRP, upper traces) in L6 dorsal root filament produced by stimulation of medial gastrocnemius nerve at 20 times threshold. Cord dorsum potentials shown in lower traces. C: excitability reduction in 3 different groups of Ia afferent terminals at various intervals following a single shock to the sural nerve at twice threshold. GM, medial gastrocnemius; GL, lateral gastrocnemius; PB, posterior biceps. The ordinate scale refers to the mean area of antidromic response to intraspinal stimulation of the respective terminal arborizations. [From Rudomin et al. .] D‐F: intrafiber records (IC) from a group I flexor muscle afferent showing negative transmembrane potential changes (PAH) produced by increasing sural nerve stimulation (D‐F). Extracellular field just outside the fiber shown in lower traces (EC). [Computer‐averaged records from Mendell .]

From Burke et al.
Figure 22. Figure 22.

Depression of composite Ia EPSP by a conditioning input that produces PAD in group Ia terminals. A: intracellular records (upper traces; lower traces from cord dorsum) of large composite EPSP produced by electrical stimulation of gastrocnemius‐soleus (G‐S) group Ia afferents in a gastrocnemius motoneuron (lower traces, EPSP on faster time base). B: depression of EPSP amplitude following a conditioning train to posterior biceps and semitendinosus (PBST) group I afferents (note volley in upper set, cord dorsum trace). C: drawing from EPSP records in A and B, showing identical time courses of the unconditioned (Uncond) and conditioned (Cond) EPSP's, when scaled for equal peak amplitude. D: time course of EPSP depression (•) with various conditioning‐testing intervals. Voltage transient produced by constant current pulses injected into the cell was unaltered by the conditioning stimulus (○), suggesting absence of juxtasomatic transmembrane conductance change. Ordinate shows the EPSP and transient amplitudes as percentage of the unconditioned responses.

From Eide et al.
Figure 23. Figure 23.

Interaction of EPSP's and IPSP's generated in an electronic neuron model consisting of 9 equal input compartments (numbered circles) connected to form a uniform electrotonic cylinder [see for details]. Each input compartment represents an increment of 0.2 λ in a total cylinder with L of 1.6 λ. The model permits introduction of brief conductance transients in any compartment to mimic synaptic conductances. In A and B, excitatory conductances (driving potential +70 mV) were distributed as indicated by (+) on the diagram, following the distribution of Ia inputs observed by Jack and co‐workers in motoneurons [; cf. Fig. B]. The EPSP in compartment 1 is the unlabeled trace in A and B. Interaction of the same excitatory conductances with synchronous inhibitory conductances (driving potential −15 mV) produced the numbered traces in A and B. The spatial distribution in each case is denoted by (‐) below the model diagram. Note that inhibitory conductances occurring in distal compartments (7–9; traces A2, B4, and B5) produced alterations in the EPSP falling phase even when, as in B4 and B5, there was little change in peak amplitude. With uniform distribution of excitatory conductances, the changes in EPSP falling phase were exaggerated (not illustrated).

Unpublished experiments of E. W. Pottala and R. E. Burke
Figure 24. Figure 24.

Effect on Ia EPSP in a gastrocnemius motoneuron produced by conditioning volleys usually giving PAD in group Ia terminals. The superimposed traces in A show the mean composite Ia EPSP produced by stimulation of a branch of the medial gastrocnemius nerve without (solid line) and with (dotted line) preceding conditioning stimulation of group I afferents in a flexor muscle nerve. Unconditioned and conditioned trials were alternated for 200 repetitions; calibration pulse is 2 mV and 1 ms. The conditioning input produced no change in the mean EPSP amplitude or time course (cf. Fig. ), but the variability of conditioned EPSP's was less than that of unconditioned EPSP's, as shown in B. Note that the variance (B), calculated on a point‐by‐point basis [see ], followed the time course of the EPSP. Variance of the background activity in the cell, indicated by the height of the base line from the zero level after the trace, was unchanged by the conditioning input. The observations show that an input may significantly affect the spinal mechanism generating PAD even though no change in the computed mean EPSP can be measured (see text).

From Rudomin et al.


Figure 1.

Composite drawings of Golgi‐stained sections of cat spinal cord showing neurons and terminal arborizations of segmental afferent fibers. A: cross section showing axonal arborizations on the left and dendritic neuropile on the right. A‐C, terminations of coarse dorsal root afferents; D and E, axons from white funiculi terminating in basal dorsal horn and medial ventral horn. Neurons drawn on the right illustrate the variety in size and dendritic architecture found in segmental neurons. B: sagittal section of lumbosacral cord of the cat (plane of section indicated on inset). Roman numerals denote Rexed laminae . A, dorsal column fibers; B, interneuron of lamina VI; C and D, motoneurons with radial dendritic patterns; E, motoneuron with predominately longitudinal dendrites; F, fibers of ventral column; a, descending axonal microbundle ending in terminal arborization (a′); b, intermingling of primary afferent and ventral column terminal arborizations; c, presumed cutaneous afferent arborization in substantia gelatinosa (c′); d, local collaterals presumed to originate from an interneuron.

From Scheibel & Scheibel ; originally published by University of California Press; reprinted by permission of the Regents of the University of California. From Scheibel & Scheibel


Figure 2.

Cell size and electrotonic architecture in cat alpha motoneurons. Graphs on the left show the correlation of cell input resistance (upper, ordinate scaled as reciprocal of RN) and axonal conduction velocity (lower, ordinate) with total cell membrane area (abscissae, same scale for both graphs). Each point represents a different cell, marked with Procion dye after electrophysiological study. Graph on right illustrates the decrease in membrane area in one motoneuron with increasing electrotonic distance from the soma (abscissa in units of electrotonic length, λ). The ordinate shows the increment in membrane area found for each 0.1 λ increment in electronic length, summed for all dendritic branches. The decrease in membrane area per 0.1 λ increment is largely due to tapering of the dendritic branches up to about 0.8 λ from the soma and is due largely to termination of various branches beyond this point.

From data of Barrett & Crill . Data from Barrett ; see also


Figure 3.

Some evidence relating to action potentials in motoneuron dendrites. A‐D: antidromic action potentials in cat alpha motoneurons. A, superimposed intracellular records of antidromic spikes during passage of a 10‐nA hyperpolarizing step, which shows inflection between A and B spike components (curved arrow) and exaggeration in the second of 2 antidromic spikes (B, curved arrow; same cell and calibrations as A). Straight arrow in A denotes humplike delayed depolarization that occurred in an all‐or‐none manner in some antidromic spikes. An analogous all‐or‐none late spike component is shown in C (curved arrow), obtained by an extracellular electrode near a single antidromically invaded motoneuron conditioned by phasic synaptic input. The delayed depolarization disappeared following the second of 2 closely spaced antidromic spikes (B, straight arrow), and in another cell when antidromic spikes with a well‐developed delayed depolarization (D, curved arrow) was conditioned with inhibitory synaptic input (superimposed records of spikes with and without synaptic conditioning). E and F: all‐or‐none spikelike potentials superimposed on composite Ia EPSP's in an apparently normal alpha motoneuron with membrane potential of −60 mV. Upper traces, Photographically superimposed intracellular records; lower traces, potential at the dorsal root entry. Larger Ia input volley (F) produced spikelike responses with multiple components; note cord dorsum volley. The animal was normal, but records resemble observations in chromatolyzed motoneurons (see text). The spikelike responses (only rarely observed in normal animals) may reflect nonpropagated action potentials in parts of the dendritic tree. (Unpublished records of R. E. Burke and L. Fedina.)

A, B, and D from Nelson & Burke ; C from Nelson & Frank


Figure 4.

Composite and single‐fiber monosynaptic EPSP's produced by group Ia afferents in cat alpha motoneurons. A, superimposed intracellular records (lower trace; upper trace is cord dorsum potential) of composite Ia EPSP in plantaris motoneuron produced by electrical stimulation of the whole plantaris nerve (ventral roots cut). B, single‐sweep records of EPSP's produced by 2 individual Ia afferent fibers (a and b) during stretch of the plantaris muscle in the same motoneuron as in A. Time scale same in A and B, but records 10 times greater amplification in B. Note markedly different time courses of the single‐fiber EPSP's. C, computer‐averaged records of single‐fiber EPSP's produced by a single group Ia afferent in 6 different motoneurons (a‐f), all recorded on the same time base with equal amplification. The time courses vary widely, despite production by the same afferent.

A and B from Burke . From Mendell & Henneman


Figure 5.

Shape variations in single‐fiber Ia EPSP's. A: plot of EPSP shape indices. Rise time on the abscissa; half‐width (i.e., the duration at 1/2 amplitude) on the ordinate for presumed single‐fiber Ia EPSP's in a large sample of afferent fiber‐motoneuron combinations, •, EPSP's in extensor motoneurons; ○, EPSP's in flexor cells. The wide range in shapes and the positive correlation between rise time and half‐width are best explained by differences in spatial position of synaptic contacts established by the different afferents on postsynaptic cells (see text). B: histogram of the electrotonic distance (λ) between the motoneuron soma and the estimated site of Ia afferent contact in 236 combinations of presumed single Ia afferent and alpha motoneuron, derived from study of the EPSP shape indices as in A. Note the fall‐off in frequency of contacts closer than 0.2 λ and beyond 0.6 λ, the latter in keeping with the decrease in incremental membrane area in the more distal dendritic tree (see Fig. C).

From Jack et al.


Figure 6.

Evidence related to conductance changes underlying the Ia EPSP. A: linear summation of synchronous composite Ia EPSP's generated in a medial gastrocnemius (MG) motoneuron by different sets of Ia afferents; LG‐Sol, lateral gastrocnemius plus soleus nerve. Computer‐averaged intracellular records showing algebraic addition of the separate MG and LG‐Sol EPSP's (•) superimposed on the actual EPSP produced by synchronous stimulation of both nerves (Both). Such linear PSP addition, which is not uncommon, would require spatial dispersion of chemical synaptic sites (see text). B: averaged EPSP records as in A, but from a flexor digitorum longus (FDL) motoneuron in which synchronous generation of FDL and MG EPSP's (Both) produced a significantly smaller composite EPSP than the algebraic addition of the FDL and MG EPSP's (•). Such nonlinear addition, while less commonly found than the records in A, imply a conductance change mechanism underlying the Ia EPSP (see text). C: effect of depolarizing current on a Ia EPSP recorded in an alpha motoneuron. Lowermost record shows superimposed sweeps without current, and the other single traces illustrate biphasic EPSP reversal with increasing (from bottom to top) depolarizing current injected into the cell.

From Burke . From Smith et al.


Figure 7.

Unit EPSP components in single‐fiber Ia EPSP's. A, single sweep intracellular records from a medial gastrocnemius (MG) motoneuron during repeated electrical stimulation of a dissected filament of MG nerve. Some trials produced a small EPSP (arrows) with latency within the rise time of the composite MG EPSP (B), while other trials produced no detectable EPSP's (i.e., failures of response). C, histogram of the amplitudes of EPSP responses as in A, for about 200 trials. Number of failures is indicated by the vertical line at 0 mV. Horizontal arrows and dotted line represent the calculated amplitude distribution expected if the observed EPSP's were composed of unit components with mean amplitude about 0.2 mV, occurring with probability described by the Poisson distribution function and an assumed (best fit) variance. Vertical arrows, multiples of the estimated unit EPSP amplitude. The small EPSP's (• in A) conform to the expected size of the unit EPSP components. D, exceptionally large single‐fiber EPSP's recorded in a plantaris motoneuron during stretch of the plantaris muscle (base line slightly oblique). Inflections (arrows) suggest some asynchrony between unit components, present in about 2% of the trials. E, histogram of amplitudes of 1,000 single‐fiber EPSP's as in D. Failures occurred 120 times per 1,000 responses (horizontal line on ordinate). Theoretical distribution fitted to the observed data using a Poisson distribution function and best fit variance is indicated by the horizontal arrow (expected number of failures) and the dotted curve. Roman numerals and vertical arrows denote multiples of the expected unit component amplitude (ca. 0.7 mV). Delayed components in D (arrows) and the lowermost response in D conform to this amplitude and are assumed to represent all‐or‐none unit EPSP's.

From Kuno . From Burke


Figure 8.

Maximum amplitude of composite Ia EPSP's produced in medial gastrocnemius (MG) motoneurons by electrical stimulation of the MG nerve. Graph at top shows the relation between EPSP amplitude (abscissa) and motoneuron input resistance (ordinate, logarithmic scale). Each symbol denotes a different cell — ○, motoneurons innervating fast‐twitch muscle units; •, cells innervating slow‐twitch units (cf. Table ). Despite considerable scatter, there is a significant positive correlation between EPSP size and cell input resistance. Note that motoneurons of slow‐twitch units have generally greater input resistance. Histograms below the graph show the distributions of MG Ia EPSP amplitudes (abscissa on same scale as graph at top) in motoneurons identified as innervating muscle units of types FF, FR, or S (see Table ). Mean of each distribution denoted by arrows.

Data from Burke . Data from Burke et al.


Figure 9.

Monosynaptic vestibulospinal tract (VST) effects in cat alpha motoneurons. A, intracellular (I‐C) records of monosynaptic EPSP in a gastrocnemius‐soleus (G‐S) motoneuron produced by electrical stimulation of Deiters' nucleus (ND) or of the ipsilateral ventral cord (thoracic; iVQ). Arrival of the volley at the lumbosacral cord is signaled by deflections in the cord dorsum (CDP) and extracellular (X‐C) records. Latency between stimulus and EPSP onset for Deiters' (t2) and ventral quadrant (t1) stimulation is plotted against the conduction distance in B for 6 different G‐S motoneurons. The slopes indicate maximal conduction velocities for the responsible lateral VST axons of 90–148 m/s, and the latencies extrapolate to a segmental latency (ordinate intercept) of 0.4–0.7 ms, indicating monosynaptic connection. C, intracellular recordings from 2 back motoneurons (interspinales, IS), showing presumed monosynaptic inhibitory postsynaptic potentials (IPSP's) produced by electrical stimulation of the medial VST in the brain stem. Conduction distance in each case is given below the records. D, upper graph, latency of IPSP onset (ordinate) plotted against conduction distance (abscissa) for a group of back motoneurons; UIC, unidentified cell. Slope of the line indicates an average conduction velocity of 69.3 m/s for the responsible axons, and the ordinate intercept of 0.93 ms suggests probable monosynaptic connection. Arrows around the intercept point denote 90% confidence limits. Lower graph in D shows the latency between the positive peak of the medial VST tract potential (visible in the intracellular records and due to the fastest conducting fibers) and the IPSP onset, again plotted against conduction distance (abscissa). The positive slope suggests that fibers producing the monosynaptic IPSP's conduct more slowly than the fastest fibers activated by the electrical stimulus.

From Grillner et al. . From Wilson et al.


Figure 10.

Frequency potentiation in descending monosynaptic EPSP. A: computer‐averaged records of corticospinal tract (CST) EPSP's produced by single (1) and identical double (2) stimuli to motor cortex, recorded in a lumbosacral motoneuron in monkey. Subtraction of 1 from 2 yields record of enhanced second EPSP alone (. B: facilitation of second corticomotoneuronal EPSP (ordinate) as a function of interval following a conditioning EPSP in 4 different monkey motoneurons. C: same relation, obtained by averaging data from 24 motoneurons; vertical bars, 1 SE. D: intracellular records from cat gastrocnemius‐soleus motoneuron showing 2 successive monosynaptic EPSP's produced by Deiters' nucleus stimulation. No evident facilitation of second EPSP at either interval. E: amplitude of second of 2 lateral VST EPSP's (as in D) at different conditioning intervals, with no evident facilitation of the second as compared to the first.

From Muir & Porter . From Grillner et al.


Figure 11.

Composite and single‐fiber disynaptic group Ia IPSP's in cat alpha motoneurons. A: computer‐averaged intracellular records of single‐fiber IPSP's in 3 different motoneurons (MNs, 1–3) produced by spike activity in a single Ia inhibitory interneuron (lowermost record; Ia IN). B: composite IPSP in motoneuron 3 produced by stimulation of Ia afferents in the quadriceps nerve; Ia volley at cord dorsum in lower trace. Same time base as A but less amplification; note similar time course for single‐fiber and composite IPSP's. C: intracellular record (V) of composite Ia IPSP in cat motoneuron, together with the in‐phase component of membrane impedance (Z) measured with a bridge circuit. Arrow marks stimulus artifact; same time base as A and B. Impedance change probably reflects rather accurately the time course of IPSP conductance (see text). [From Smith et al. .] D and E: effect of intracellular injection of Cl on composite (left) and single‐fiber (right) Ia IPSP's in same motoneuron. Bottom trace in E on left shows cord dorsum record; bottom trace in E on right shows spike activity in Ia interneuron. Chloride reversal of composite IPSP (right, photographically superimposed traces) was biphasic but that of the single‐fiber IPSP (left, computer‐averaged records) was not (see text). Note different time scales for composite and single‐fiber records.

From Jankowska & Roberts . From Jankowska & Roberts


Figure 12.

Recurrent and disynaptic Ia IPSP's in cat motoneurons. A, recurrent IPSP in motoneuron produced by increasing (from top to bottom) stimulus intensities to L7 ventral root. Fourth record from the top represents maximal stimulation, shown again on slower time base in B. Arrows in upper 2 records of A indicate apparent component IPSP's (probably not unit PSP's), presumably produced by repetitive firing in Renshaw interneurons (cf. Fig. ). Note prolonged duration of IPSP decay. C, intracellular records (sulfate‐filled electrode) of disynaptic Ia IPSP and recurrent IPSP in a motoneuron showing reversal at same membrane potential (ca. −80 mV) during current passage. [From Coombs et al. .] D, intracellular records (upper traces; lower traces are from cord dorsum) of Ia and recurrent IPSP's in a motoneuron, recorded with KCl‐filled micropipette. Both IPSP's were initially hyperpolarizing (uppermost pair of records, no current), but the Ia IPSP reversed more readily with hyperpolarizing current and consequent injection of small amounts of Cl (increasing from top to bottom). After cessation of current, additional Cl had been injected and the Ia IPSP showed biphasic reversal while the recurrent IPSP remained hyperpolarizing (lowermost pair of records, no current; see text).

From Eccles et al. . From Burke et al.


Figure 13.

Gamma motoneurons. A: histogram of the least soma diameter of ventral horn neurons in the gastrocnemius‐soleus motor nucleus of the cat spinal cord, measured in 20‐μm sections from cell profiles exhibiting a nucleolus. Neurons with least soma diameters of 30‐μm or less are presumed to be gamma motoneurons. B: intracellular record (superimposed sweeps) of antidromic action potential in a gamma motoneuron (conduction velocity 30 m/s) with stimulus strength straddling threshold for the axon. Inflection between A and B spike components denoted by arrow. C: intracellular record (lower trace; upper trace from cord dorsum) from flexor digitorum longus gamma motoneuron showing absence of detectable Ia EPSP with maximum Ia volley. D: antidromic action potential showing brief early component of the afterhyperpolarization. E: record from another gamma cell showing prolonged small‐amplitude afterhyperpolarization with high amplification and slow time base.

From Van Buren & Frank . B‐E from Eccles et al.


Figure 14.

Effect of input interaction on transmission of disynaptic Ia IPSP to alpha motoneurons. A: Convergence of descending excitatory and recurrent inhibitory systems onto an Ia inhibitory interneuron projecting to an alpha motoneuron (the cell with intracellular electrode). B: intracellular superimposed records (upper traces; lower traces from cord dorsum) from a knee flexor motoneuron in cat. Records in C show indicated portion of traces in B (dashed lines) on faster time base. Just‐suprathreshold stimulation of quadriceps Ia afferents (Q 1.1) produced minimal disynaptic Ia IPSP. Conditioning this input by preceding stimulus to Deiters' nucleus (ND + Q) greatly enhanced the Ia IPSP in the motoneuron. Deiters' nucleus stimulation alone at 80 μA (ND 80) produced minimal synaptic effect. Preceding the paired Ia and Deiters' stimuli by a shock to the L5 and L6 ventral roots then suppressed the Ia IPSP (L5 + L6 VR → ND + Q), presumably by inhibiting firing of the Ia interneurons involved.

From Hultborn & Udo


Figure 15.

Records from interneurons monosynaptically excited by group Ia afferents. A: intracellular records (upper traces; lower traces from cord dorsum) from 2 lumbar interneurons (Cell 1 and Cell 2), showing monosynaptic EPSP's produced in each by increasing stimulation (given in multiples of threshold) of hamstring muscle nerves (ABSm, anterior biceps and semimembranosus; PBSt, posterior biceps and semitendinosus). Cell 1, located dorsomedial to motor nucleus (hatched area in C), had typical recurrent IPSP after stimulation of L7 ventral root (VR L7). Cell 2 was located more dorsally in intermediate nucleus (small dots in C) and had no recurrent IPSP (VR L6 + 7). Cell 1 thus was presumed to project to alpha motoneurons while projection of cell 2 was unidentified (see text). B: extracellular records (upper traces; lower traces (CDP) from cord dorsum) of presumed Ia inhibitory interneuron showing monosynaptic firing to maximum group I volley in adductor muscle nerve (Add 2.4 T), which was suppressed by prior stimulation of L6 ventral root (Cond. VR L6). Decreased group I input (Add 1.2 T) was unable to fire the cell, but prior conditioning with 4 volleys to red nucleus (Cond. RuST) provided convergent facilitation and cell fired monosynaptically (cf. Fig. A). [From Hultborn & Santini .] C: L7 segment gray matter showing location of interneurons with convergence of monosynaptic Ia excitation and recurrent inhibition (the Ia inhibitory interneurons; large open and closed circles) and Ia excited cells without recurrent inhibition (small dots). [From Hultborn et al. .]

From Hultborn et al.


Figure 16.

Records from Renshaw interneurons. A, Quasi‐intracellular records from Renshaw cell showing high‐frequency discharge to increasing stimulation (from top to bottom) of L7 ventral root. Maximum response (lowest record) shown on expanded time base in B. C, intracellular records from a Renshaw interneuron after spike inactivation, showing graded EPSP with increasing ventral root stimulation (from top to bottom). Graded initial fast response presumed to represent part of the EPSP (see text). Prolonged decay phase of the maximum EPSP (3rd record) is shown on slower time base in D, with greater amplification.

Records A‐D from Eccles et al. .] E‐G: spike frequency (ordinate) versus time (abscissa) in Renshaw cell responding to antidromic volleys (arrows) in 3 different muscle nerves (ipsilateral dorsal roots cut). BST, biceps and semitendinosus; MGS, medial gastrocnemius and soleus; SMAB, semimembranosus and anterior biceps. Early (nicotinic) discharge in E was followed by a pause in firing, which was in turn followed by a prolonged moderate (muscarinic) increase in discharge rate (see text). Early firing and smaller pause produced by MGS stimulation (F) shown on faster time base. Stimulation of SMAB nerve (G) produced only a decrease in Renshaw cell firing. [E‐G from Ryall


Figure 17.

Intracellular records from DSCT neurons. A: antidromic spike (upper trace; lower trace from cord dorsum) in L4 DSCT cell after stimulation of its axon in the ipsilateral dorsolateral quadrant in lower thoracic cord; 4‐nA hyperpolarizing current during record. B: higher gain records from same cell with and without hyperpolarizing current, showing humplike delayed depolarization (arrow) following antidromic spikes. C: intracellular records (upper traces; lower traces from cord dorsum) from DSCT cell firing to increasing (from top to bottom) group I volleys in quadriceps muscle nerve. Increasing stimulation produced increasing amplitude of postspike hump (arrows; possibly a delayed depolarization, see text), resulting in second spike in lower 2 records. D: records from the same neuron as shown in C but now during passage of transmembrane hyperpolarizing current to prevent cell firing. Note the graded, large‐amplitude composite EPSP's produced by increasing (from top to bottom) group I input. With largest input volley (lowermost record), spikes were produced on some trials, again followed by a large delayed depolarization as in C. [C and D from Kuno & Miyahara .]

From Eide et al.


Figure 18.

Single‐fiber group I EPSP's in DSCT neurons. A: intracellular records from DSCT cell during increasing stretch of the soleus muscle. Regularly recurring EPSP's can be attributed to single group Ia afferents. Note large amplitudes and similar shapes. B: amplitude histogram of 151 EPSP's produced in a DSCT cell by repeated firing in one group Ia afferent, as in A. Mean amplitude was 4.3 mV, and the distribution was symmetrical, without failures of occurrence (cf. Fig. ). C: relation between the amplitude (ordinate) and rise time (abscissa) in group I EPSP's as shown in A. Little correlation was evident, and all EPSP's had relatively brief rise time (<0.9 ms; cf. Fig. ).

From Eide et al.


Figure 19.

Occurrence of monosynaptic EPSP and disynaptic IPSP produced by same set of group Ia afferents in a spinal border cell belonging to ventral spinocerebellar tract (VSCT). A‐F: intracellular records (upper traces; lower traces from cord dorsum) during increasing electrical stimulation, noted in multiples of threshold, of quadriceps (Q) muscle nerve. The monosynaptic EPSP, apparently pure at 1.14 times threshold, was followed at higher stimulus strengths by a disynaptic IPSP also produced by the same Ia afferents. Both synaptic effects appeared to be maximal at 1.5 times threshold. Diagram on left shows the presumed set of connections accounting for this observation (see text). Mn, motoneuron. [From Lundberg .]

From Lundberg & Weight


Figure 20.

Some indices of primary afferent depolarization (PAD). A: cord dorsum potential (CDP) and potential change recorded along a distally cut dorsal root filament (DRP) of L6, produced by 3 volleys (at 200/s) in group I muscle afferents. B: mean antidromic excitability (•) and variance of excitability (○) in gastrocnemius Ia afferents, with electrical stimulation of the afferent arborizations in the cord. The changes with time were produced by stimulation of toe extensor (PL‐FDHL) group I afferents at various conditioning‐testing intervals. Note that time course of negative DRP in A and excitability increase in B are similar. [From Rudomin & Dutton .] C and D: transmembrane depolarization recorded within a quadriceps group Ia fiber in the dorsal horn (record I‐C), produced by 2 (C) or 4 (D) volleys in PBST (posterior biceps and tendinosus) muscle afferents (incoming volleys appear in cord dorsum trace, record CDP). There was no detectable extracellular potential immediately outside the fiber (record X‐C) with 2 volleys, but with 4 a small positive potential change was evident (D). [From Eccles et al. .]

From Burke et al.


Figure 21.

Some indices of primary afferent hyperpolarization (PAH). A and B: photographic (A) and computer‐averaged (B) records of positive dorsal root potential (DRP, upper traces) in L6 dorsal root filament produced by stimulation of medial gastrocnemius nerve at 20 times threshold. Cord dorsum potentials shown in lower traces. C: excitability reduction in 3 different groups of Ia afferent terminals at various intervals following a single shock to the sural nerve at twice threshold. GM, medial gastrocnemius; GL, lateral gastrocnemius; PB, posterior biceps. The ordinate scale refers to the mean area of antidromic response to intraspinal stimulation of the respective terminal arborizations. [From Rudomin et al. .] D‐F: intrafiber records (IC) from a group I flexor muscle afferent showing negative transmembrane potential changes (PAH) produced by increasing sural nerve stimulation (D‐F). Extracellular field just outside the fiber shown in lower traces (EC). [Computer‐averaged records from Mendell .]

From Burke et al.


Figure 22.

Depression of composite Ia EPSP by a conditioning input that produces PAD in group Ia terminals. A: intracellular records (upper traces; lower traces from cord dorsum) of large composite EPSP produced by electrical stimulation of gastrocnemius‐soleus (G‐S) group Ia afferents in a gastrocnemius motoneuron (lower traces, EPSP on faster time base). B: depression of EPSP amplitude following a conditioning train to posterior biceps and semitendinosus (PBST) group I afferents (note volley in upper set, cord dorsum trace). C: drawing from EPSP records in A and B, showing identical time courses of the unconditioned (Uncond) and conditioned (Cond) EPSP's, when scaled for equal peak amplitude. D: time course of EPSP depression (•) with various conditioning‐testing intervals. Voltage transient produced by constant current pulses injected into the cell was unaltered by the conditioning stimulus (○), suggesting absence of juxtasomatic transmembrane conductance change. Ordinate shows the EPSP and transient amplitudes as percentage of the unconditioned responses.

From Eide et al.


Figure 23.

Interaction of EPSP's and IPSP's generated in an electronic neuron model consisting of 9 equal input compartments (numbered circles) connected to form a uniform electrotonic cylinder [see for details]. Each input compartment represents an increment of 0.2 λ in a total cylinder with L of 1.6 λ. The model permits introduction of brief conductance transients in any compartment to mimic synaptic conductances. In A and B, excitatory conductances (driving potential +70 mV) were distributed as indicated by (+) on the diagram, following the distribution of Ia inputs observed by Jack and co‐workers in motoneurons [; cf. Fig. B]. The EPSP in compartment 1 is the unlabeled trace in A and B. Interaction of the same excitatory conductances with synchronous inhibitory conductances (driving potential −15 mV) produced the numbered traces in A and B. The spatial distribution in each case is denoted by (‐) below the model diagram. Note that inhibitory conductances occurring in distal compartments (7–9; traces A2, B4, and B5) produced alterations in the EPSP falling phase even when, as in B4 and B5, there was little change in peak amplitude. With uniform distribution of excitatory conductances, the changes in EPSP falling phase were exaggerated (not illustrated).

Unpublished experiments of E. W. Pottala and R. E. Burke


Figure 24.

Effect on Ia EPSP in a gastrocnemius motoneuron produced by conditioning volleys usually giving PAD in group Ia terminals. The superimposed traces in A show the mean composite Ia EPSP produced by stimulation of a branch of the medial gastrocnemius nerve without (solid line) and with (dotted line) preceding conditioning stimulation of group I afferents in a flexor muscle nerve. Unconditioned and conditioned trials were alternated for 200 repetitions; calibration pulse is 2 mV and 1 ms. The conditioning input produced no change in the mean EPSP amplitude or time course (cf. Fig. ), but the variability of conditioned EPSP's was less than that of unconditioned EPSP's, as shown in B. Note that the variance (B), calculated on a point‐by‐point basis [see ], followed the time course of the EPSP. Variance of the background activity in the cell, indicated by the height of the base line from the zero level after the trace, was unchanged by the conditioning input. The observations show that an input may significantly affect the spinal mechanism generating PAD even though no change in the computed mean EPSP can be measured (see text).

From Rudomin et al.
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R. E. Burke, P. Rudomin. Spinal Neurons and Synapses. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 877-944. First published in print 1977. doi: 10.1002/cphy.cp010124