Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Mechanisms of Autonomic Integration

R. A. North

10.1002/cphy.cp010402

Source: Supplement 4: Handbook of Physiology, The Nervous System, Intrinsic Regulatory Systems of the Brain

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Transmission in Autonomic Ganglia
1.1 Fast Excitatory Postsynaptic Potentials (EPSPs)
1.2 Physiological Significance of Fast EPSPs
1.3 Slow (Cholinergic) EPSPs
1.4 Late Slow (Noncholinergic) EPSPs
1.5 Physiological Significance of Slow EPSPs
1.6 Inhibitory Postsynaptic Potentials
2 Integration in Autonomic Ganglia
2.1 Cellular and Molecular Substrates
2.2 Physiological Significance of Integration
3 Concluding Remarks
Figure 1. Figure 1.

A: mammalian prevertebral ganglia. CN, colonic nerves; C‐SMG, celiac‐superior mesenteric ganglia; DR, dorsal root; DRG, dorsal root ganglion; GLSN, greater and lesser splanchnic nerves; HGN, hypogastric nerves; IMG, inferior mesenteric ganglion; IMN, intermesenteric nerve; LSC, lumbar sympathetic chain; LSN, lumbar splanchnic nerves; RC, rami communicantes; and VR, ventral root. Typical arrangements of intracellular recording electrodes (left) and stimulating electrodes (right) are also shown. B: mammalian enteric ganglia. LM, longitudinal muscle; MP, myenteric plexus; CM, circular muscle; SP, submucosal plexus; SA, submucosal arteriole; and M, mucosa. Intracellular recordings are typically made from neurons lying in myenteric and submucosal ganglia, dissected as illustrated.

A from Tsunoo et al. 232; B from Furness and Costa 65
Figure 2. Figure 2.

Spontaneous miniature excitatory postsynaptic potentials recorded from bullfrog sympathetic ganglion cell bathed in 10 mM K+ solution.

From Kuba and Koketsu 142
Figure 3. Figure 3.

Mimicry of spontaneous miniature excitatory postsynaptic potential (EPSP) by iontophoretic application of acetylcholine (ACh) in frog atrial ganglion cell. Note similar time course and amplitude of spontaneous miniature EPSP and of ACh‐evoked response (records are from 2 different cells). As a rule, times to peak of miniature EPSPs were 5–8 ms, and fastest ACh potentials had range of 7–10 ms.

From Dennis et al. 47
Figure 4. Figure 4.

Intracellular recordings from myenteric neuron. A: fast EPSPs in response to 1 stimulus applied 100 μm away from cell soma. Downward deflection is stimulus artifact. Stimulus strengths: 1, 9 V; 2, 10 V (local response appears but does not reach threshold for full soma membrane spike); and 3, 11 V (full spike evoked). B: EPSPs declined in amplitude when evoked at frequencies >0.1 Hz. Each point with vertical bar (SE) indicates mean of data from 5 to 23 different cells. Frequency of stimuli indicated beside each curve. Values at 40 Hz are means from 3 cells. Amplitude of first EPSP ranged from 8 to 24 mV. Spontaneous variation of EPSP amplitude was observed at 0.017 Hz and may have occurred at higher frequencies.

From Nishi and North 192
Figure 5. Figure 5.

Reversal of fast EPSP in bullfrog sympathetic ganglion. Synaptic potentials were evoked at various levels of membrane potential (indicated in mV). Resting membrane potential was −70 mV; other potentials were obtained by application of current through recording electrode. Spike potentials were evoked by synaptic potential at membrane potentials between −22 and −70 mV. Vertical bar, 50 mV; time frequency, 1 kHz.

From Nishi and Koketsu 189
Figure 6. Figure 6.

Reversal potentials for synaptic transmission and iontophoretically applied ACh in frog atrial ganglion cells. A: reversal of synaptic potential alone (dotted lines, zero potential), which occurred at −12 mV. B: responses from another cell to both iontophoretically applied ACh and synaptic stimulation, recorded on same sweeps. Reversal occurred at −2 mV.

From Dennis et al. 47
Figure 7. Figure 7.

ACh‐induced fluctuations of membrane current and excitatory postsynaptic current (EPSC) recorded from same neuron. Digitalized records of current fluctuations before (A) and during (B) iontophoretic application of ACh (ACh‐induced steady current = 3.8 nA). C: spectral density of ACh‐induced current fluctuations is shown as function of frequency. Spectrum was obtained by subtracting averaged spectrum of 4 records similar to A from averaged spectrum of 4 records similar to B. Line through data points represents sum of 2 Lorentz functions, with cut‐off frequencies f1 and f2 corresponding to mean channel lifetimes for fast‐operating channels (τf) and for slow‐operating channels τs). S(f), spectral density at frequency f; S(0), asymptotic spectral density at frequency zero; S1(0)/S2(0) = 0.3. D: EPSC evoked by 1 preganglionic stimulus decays exponentially. E: semilogarithmic plot of EPSC amplitude against time; value of EPSC decay time constant τd) is close to τs. I(t) end‐plate current at time t; and I(0), end‐plate current at time zero.

From Skok et al. 224
Figure 8. Figure 8.

Organization of bullfrog lumbar paravertebral chain ganglia and fast EPSPs. A: camera lucida drawing of preparation used in experiments. It contains 7th‐10th sympathetic ganglia (G7‐G10) and 7th‐10th spinal nerves. Spinal end of 7th and 8th spinal nerves, chain above G7, and sciatic nerve were each fitted with suction electrodes, thus permitting orthodromic and antidromic stimulation of neurons in G9 and G10. B: anatomical separation of synaptic inputs to B and C neurons, a‐c, Intracellular responses of C cell to stimulation of 7th and 8th spinal nerves (a), chain above G7 (b), and sciatic nerve (c). d‐f, Intracellular responses of B cell to stimulation of chain above G7 (d), 7th and 8th spinal nerves (e), and sciatic nerve (f). Note different latencies of B and C responses. Contribution of fast nicotinic EPSPs can be seen by comparing orthodromic and antidromic responses.

From Dodd and Horn 48
Figure 9. Figure 9.

Intracellular recordings from 3 different neurons (1–3) in rabbit superior cervical ganglion in vivo. Note spontaneous subthreshold fast EPSPs. Inspiration occurred during time indicated by bar. Lower traces in 1 are intracellular recordings at 2 different speeds. Calibration, 50 mV; time marks (dots) are 500 ms apart.

Adapted from Skok 223
Figure 10. Figure 10.

Intracellular recordings from 2 cat ciliary ganglion cells in vivo (A and B). Eye was illuminated during periods indicated by bar. This reflexly induced an increase in frequency of fast EPSPs and action potentials.

From Skok 223
Figure 11. Figure 11.

Nicotinic and muscarinic depolarizations in same myenteric plexus cell. A: depolarization evoked by nerve stimulation. Single‐pulse stimulus (arrow) evoked fast EPSP followed by much larger and longer‐lasting slow EPSP. B: depolarization evoked by ACh iontophoresis (▴ 20 nA for 1 ms). 1, Hyoscine (1 μM) completely abolished slow depolarization but did not affect rapid depolarization. After washing out hyoscine, hexamethonium (200 nM) was used to abolish rapid depolarization. 2, At resting potential (−55 mV) ACh iontophoresis caused both rapid and slow depolarization. Rapid (nicotinic) depolarization increased with membrane hyperpolarization. Slow (muscarinic) depolarization decreased and reversed polarity with membrane hyperpolarization. Note increase in input resistance accompanying muscarinic effect of ACh.

From North and Tokimasa 202
Figure 12. Figure 12.

Ionic currents underlying slow EPSP in bullfrog sympathetic ganglia, hypothesized largely from voltage recordings by Kuba and Koketsu 142. Ordinates, membrane currents. Inward currents were taken as negative and outward currents as positive. Abscissas, membrane potential. Dashed lines, K+ currents (IK) caused by inactivation of K+ conductance (GK). Equilibrium potential for K+ (EK) was assumed to be −80 mV, since EK of many cells was close to this value under these experimental conditions. Dotted lines, sum of Na+ and Ca2+ currents (INa, + ICa) caused by activation of their ion conductances. Reversal level of this current was assumed to be +50 mV. Solid lines, synaptic currents for slow EPSP. In Type 1 cells, K+ inactivation is almost balanced by Na+ and K+ activation; in Type 3 cells, K+ inactivation predominates and synaptic current reverses; and in Type 2 cells, an intermediate condition exists. Type 2 cells would not show any voltage sensitivity of EPSC from −50 to −100 mV.

From Kuba and Koketsu 142
Figure 13. Figure 13.

Clamp currents recorded from bullfrog sympathetic neuron. A: 30‐mV hyperpolarizing voltage command from holding potential (VH) of −30 mV; B: 30‐mV depolarizing voltage command from holding potential of −60 mV. Top traces (A and B), voltage; bottom traces, current (outward current upwards). Slow inward relaxation after instantaneous current steps reflects deactivation, and outward relaxation reflects reactivation of potassium M‐current.

From Adams et al. 3
Figure 14. Figure 14.

Synaptic inhibition of M‐current in voltage‐clamped bullfrog ganglion cell. Effect of repetitive preganglionic stimulation (arrow) on relaxations of steady current and M‐current in a neuron voltage clamped at −35 mV (2‐electrode clamp). Nerve stimulation reduced steady outward current flowing at −35 mV but caused no change in current flowing at −65 mV. Chart speed was slowed 100‐fold during stimulus train and recovery.

From Adams and Brown 2
Figure 15. Figure 15.

Reversal of muscarinic slow EPSP. Intracellular recording from myenteric neuron. Slow EPSP was evoked by single‐pulse stimulus (arrow) to presynaptic fibers entering myenteric ganglion. Responses were recorded at membrane potentials indicated beside each trace. Initial rapid upward deflection is fast EPSP. Action potentials evoked by fast EPSP (at −28 and −50 mV) are truncated.

K. Morita and R. A. North, unpublished observations
Figure 16. Figure 16.

Reversal of slow muscarinic ACh potential in myenteric neuron. A: response to iontophoresis of ACh (10 nA/100 ms) recorded at membrane potential shown beside each trace. Electrotonic potentials were removed from all but 2 traces. Hexamethonium (200 μM) was present throughout. B: amplitude of ACh potential as function of membrane potential. Reversal of muscarinic ACh potential occurs near −90 mV.

From Morita et al. 182
Figure 17. Figure 17.

Fast nicotinic and slow muscarinic responses in single myenteric neuron. Iontophoresis of ACh (▴, 20 nA/1 ms) evoked nicotinic depolarization followed by muscarinic depolarization. Top trace, control; bottom trace, after adding hexamethonium (200 μM) to perfusing solution. Hexamethonium blocked nicotinic response and slightly increased amplitude of initial component of muscarinic depolarization. Electrotonic potentials are evoked by slightly larger current in bottom trace; hexamethonium itself did not change input resistance or membrane potential. Slight increase in amplitude of initial part of muscarinic response in presence of hexamethonium is due to removal of an afterhyperpolarization that results from Ca2+ entry during the nicotinic depolarization.

From Tokimasa et al. 228
Figure 18. Figure 18.

Four types of synaptic responses in neurons of bullfrog 10th sympathetic ganglion measured with intracellular electrodes. A: single preganglionic stimulus produces fast subthreshold EPSP (left); stronger stimulus excites 2nd axon, producing larger EPSP and impulse. B: Slow inhibitory postsynaptic potential (IPSP) in a C neuron (lasting 2 s) on stimulation of central portion of 7th and 8th spinal nerves with 13 pulses at 20 Hz. Fast EPSPs were blocked with dihydro‐β‐erythroidine. C: slow cholinergic EPSP (lasting 30 s) results from 4 pulses at 50 Hz applied to synaptic chain above 7th sympathetic ganglion. Initial rapid deflections are 4 large nerve impulses (cropped). D: late slow EPSP (peptidergic) lasts −300 s on stimulation of central portions of 7th and 8th spinal nerves (50 pulses at 10 Hz). Nicotinic blocking drugs were used in B.

From Jan et al. 101
Figure 19. Figure 19.

Intracellular recording from guinea pig myenteric plexus neuron. Optimum stimulus frequency needed to evoke late slow EPSP is ∼20 Hz. Late slow EPSPs were evoked by 2 pulses (500‐μs duration) applied to presynaptic fibers entering ganglion. Neither 1 pulse, nor 2 pulses separated by 2 ms, elicited a response. Interval between pulses was then increased (indicated in ms). Late slow EPSP was largest at interval of 30–100 ms (33–10 Hz), and then declined. Pulse separations of 1, 2, and 5 s elicited responses similar to 500 ms; pulse separation of 10 ms did not elicit a response (not shown).

J. C. Bornstein and R. A. North, unpublished observations
Figure 20. Figure 20.

Different types of late slow EPSCs recorded from 2 voltage‐clamped bullfrog sympathetic neurons. Responses were elicited by train of supramaximal preganglionic stimuli at 10 Hz for 5 s (arrows). Top traces in A and B are voltage recordings showing command pulses (lasting 1 s) of 15 mV (A) and 30 mV (B) repeated at 0.3 Hz. Middle and bottom traces are current recordings at indicated holding potentials. First type of response (A) is accompanied by fall in conductance (reduced current excursion for fixed‐voltage command) and decreases with hyperpolarization. Second type of response (B) is accompanied by rise in conductance and increases with membrane hyperpolarization. Note difference in time course.

From Katayama and Nishi 119
Figure 21. Figure 21.

Nerve‐evoked peptidergic late slow EPSCs and muscarinic slow EPSPs in 3 bullfrog sympathetic neurons. Left traces, nonreversing response; center traces, reversing response. Cells were voltage clamped at membrane potential indicated beside each current recording, and 7th and 8th spinal nerves (carrying peptidergic fibers) were stimulated at 20 Hz for 5 s (arrows). Resting membrane potentials of both of these cells were ca. −50 mV, with 2 mM K+ in bathing solution. Right traces, muscarinic slow EPSCs following 6 pulses at 50 Hz applied to sympathetic chain. Clamped‐membrane potential is indicated beside each trace. Resting membrane potential of cell was −35 mV. Dihydro‐β‐erythroidine and prostigmine were present in bathing solution, with 6 mM K+ also present. Note reversal of early, but not late, part of response.

From Kuffler and Sejnowski 146
Figure 22. Figure 22.

Substance P (SP) immunoreactivity in guinea pig inferior mesenteric ganglion. A: pattern of varicose and nonvaricose fibers is revealed by monoclonal antibody in inferior mesenteric ganglion of normal guinea pig, perfused and processed together with tissue in B. B: inferior mesenteric ganglion of capsaicin‐treated guinea pig, showing total loss of specific SP immunofluoresence, apart from small residual trace (*). C: SP immunofluorescence in inferior mesenteric ganglion of normal guinea pig, perfused and processed together with tissue in D. D: almost total disappearance of SP immunofluorescence in guinea pig inferior mesenteric ganglion 4 days after lumbar nerves were severed. E: persistence of varicose and nonvaricose SP immunoreactive (SPI) fibers in inferior mesenteric ganglion of guinea pig in which spinal cord had been removed (below Th7) 4 days previously. F: trails of varicosities immunoreactively labeled by SP/peroxidase‐antiperoxidase method in 50‐μm slice of celiac superior mesenteric ganglion, photographed before osmication and embedding for electron microscopy. G: electron micrograph showing dense deposits revealing SPI material over nerve terminal (*) synapsing with dendrite (D) of sympathetic postganglionic neuron. This type of nerve terminal (commonly seen in guinea pig inferior mesenteric ganglion) contains a large cluster of small clear synaptic vesicles, which are massed in presynaptic zone; it also contains a lesser number of large dense‐core vesicles, lying chiefly at periphery of cluster of small vesicles (away from presynaptic membrane), together with group of mitochondria. SP immunoreactivity within nerve terminal is localized over cores of large dense‐core vesicles and is also associated with cytoplasmic (external) surfaces of small vesicles; both features have been reported for SPI‐nerve terminals in substantia gelatinosa of spinal cord. N, nucleus of satellite cell; S, satellite cell cytoplasm; ct, connective tissue space. Scale: bars, 1 μm for A‐F and 0.5 μm for G. H: organization of sensory SPI‐peripheral nerve fibers at lumbar spinal levels. Example is sensory neuron of lumbar origin innervating colon by way of lumbar splanchnic nerve and colonic branch of inferior mesenteric ganglion (IMG). DH, dorsal horn; VH, ventral horn; sg, substantia gelatinosa; DRG, dorsal root ganglion; LSG, lumbar sympathetic ganglion of paravertebral chain; LSN, lumbar splanchnic nerve; imn, intermesenteric nerve; CN, colonic nerve fascicle; and HNN, hypogastric nerves.

From Matthews and Cuello 171
Figure 23. Figure 23.

A: intracellular recording from a myenteric neuron. Substance P was applied by electrophoresis (40 nA, 5 s) to soma membrane (▴). High‐concentration K+ solution (bar) depolarized membrane and greatly reduced amplitude of substance P potential. Membrane potential was shifted back to control level (arrow down) by hyperpolarizing current. Substance P potential was now reversed. These changes were reversible when hyperpolarizing current was terminated (arrow up) and when perfusion with normal Krebs solution was restarted. B: relationship between substance P reversal potential and extracellular [K+]. Reversal potentials are mean values (with SE indicated) for number of cells shown in parentheses. Slope of dashed line (fitted by eye) is 54 mV/10‐fold change in [K+].

From Katayama et al. 120
Figure 24. Figure 24.

Responses of AH‐myenteric plexus neuron to repetitive presynaptic nerve stimulation. A: nerve stimulation (10 Hz/3 s) is indicated by arrow and bar. Response was biphasic. Hyoscine (1 μM) abolished initial component of slow synaptic potential (combination of slow EPSP and late slow EPSP), whereas tetrodotoxin (TTX, 100 nM) abolished entire synaptic potential. B: example from another AH neuron. Hyoscine (1 μM) depressed only initial part of slow potential. Total duration of slow EPSP is not shown but was ∼3 min. C: amplitude of muscarinic component of response in B obtained by subtracting amplitude when hyoscine was present from amplitude when it was not.

From North and Tokimasa 202
Figure 25. Figure 25.

Schematic representation of synaptic potentials that can be recorded in bullfrog lumbar 9th or 10th sympathetic ganglion B and C cells (see also Fig. 18). Fast EPSPs can be recorded from B cells by stimulating presynaptic B‐fibers and from C cells by stimulating presynaptic C‐fibers. Slow EPSPs can be recorded from B cells by stimulating presynaptic B‐fibers. Late slow EPSPs can be recorded from B and C cells, but only by stimulating presynaptic C‐fibers. Transmitter, luteinizing hormone‐releasing hormone (LHRH), is assumed to diffuse to B cells. Slow IPSPs can be recorded in C cells when presynaptic C‐fibers are stimulated. 6–8, Spinal nerves.
Figure 26. Figure 26.

Intracellular recording from bullfrog sympathetic ganglion C cell. Reversal of action‐potential afterpotential, slow IPSP and muscarinic ACh response in curarized neuron. Amount of polarizing current is indicated for each trace. Tops of antidromic action potentials were cropped. Synaptic and ACh responses have same reversal potential. Arrows indicate half‐decay points of muscarinic responses. Decay times increased as cell was hyperpolarized from rest (ca. −50 mV). T = 22°C.

From Dodd and Horn 49
Figure 27. Figure 27.

Intracellular recording from ganglion cell in mudpuppy cardiac ganglion. Reversal potentials of inhibitory responses resulting from nerve stimulation (30 Hz for 700 ms) and iontophoretic application of ACh (20 nA for 10 ms) and bethanechol (170 nA for 20 ms). Membrane potential was monitored and varied by current passed through an electrode. Bathing solution contained 5 × 10−8 M dihydro‐β‐erythroidine to attenuate excitatory responses. As cell was hyperpolarized, magnitude of fast excitatory responses increased, while inhibitory responses decreased and reversed polarity between −90 and −100 mV for all modes of stimulation. Stimulus is indicated by bar or dot. Excitatory responses to nerve stimulation partially obscured inhibitory responses. Responses to all 3 types of stimulation have same reversal potential.

From Hartzell et al. 82
Figure 28. Figure 28.

Enkephalin causes presynaptic inhibition by blocking action‐potential propagation. Left: control shows fast EPSP recorded intracellularly from myenteric neuron in guinea pig small intestine. Single stimulus evoked 20‐mV multifiber EPSP (trace is average of 4 with similar amplitudes). Enkephalin was applied from pipette (tip diam 5 μm) containing 1 μM Met5‐enkephalin. Pipette tip was moved to various positions on surface of myenteric plexus (right), and enkephalin was ejected by a 300‐ms pressure pulse. At positions 1 and 3 enkephalin had no effect. At 2, enkephalin reduced EPSP amplitude; this effect recovered within 2–3 min.

E. Cherubini and R. A. North, unpublished observations
Figure 29. Figure 29.

Interaction between muscarinic and peptidergic late slow EPSCs. Bullfrog sympathetic neuron was voltage clamped at its resting potential (−58 mV), and cholinergic input was stimulated 10 times at 50 Hz, with stimulation repeated every 2 min. Fast nicotinic responses are cropped (arrow). Amount of muscarinic current was reduced after train of 100 stimuli at 20 Hz was applied to 7th and 8th spinal nerves and recovered with decline of peptidergic current.

From Kuffler and Sejnowski 146
Figure 30. Figure 30.

Nerve‐released transmitter of late slow EPSP (probably substance P) depresses muscarinic ACh response in a myenteric neuron. Top: trace 1, control response to ACh iontophoresis (10 nA/1 ms). Center trace, response to 1 stimulus applied to presynaptic nerves (ns). This evokes typical muscarinic slow EPSP. Right trace, beginning of late slow EPSP evoked by repetitive stimulation of presynaptic nerves (10 Hz, 3 s; bar). Bottom: responses to ACh evoked after onset of nerve stimulation. Traces 2 and 3, applications of ACh during noncholinergic slow EPSP evoked 11 s (2) and 38 s (3) after nerve stimulation. Response to ACh is abolished or depressed. Depolarization of membrane to same level would increase amplitude of ACh response. Trace 4, full recovery of ACh response 93 s after repetitive nerve stimulation, when late slow EPSP had declined.

From Tokimasa and North 230
Figure 31. Figure 31.

IPSP inhibits repetitive firing of bullfrog sympathetic neurons. This intracellular recording was taken from a C cell during period of repetitive firing induced by late slow EPSP. Tubocurarine (100 μM) was used to block nicotinic synapses. Train of presynaptic stimuli was applied to neurons (dotted line) and an IPSP was produced. As IPSP developed, repetitive firing was inhibited. As IPSP subsided, membrane potential began to oscillate and repetitive firing recommenced.

From Horn and Dodd 96
Figure 32. Figure 32.

Effect of inhibitory nerve stimulation on time course of EPSP recorded at reversal potential for IPSP. A: control records of electrotonic potential and fast EPSP. B: records of electrotonic potential and fast EPSP when membrane was shunted by stimulating inhibitory nerves. Bottom traces, EPSPs recorded at faster sweep speed and higher amplification. Arrow, stimulation of inhibitory nerves. No potential change occurred, because membrane was held at IPSP reversal potential. C: time courses of EPSPs, before (○) and during (•) inhibitory conductance change. Solid lines, time courses of EPSPs computed with assumptions that control cell resistance was 180 MΩ and fell to 80 MΩ during IPSP and that cell capacitance was 94 pF throughout. Dashed line, time course of synaptic current required to simulate both EPSPs.

From Edwards et al. 59
Figure 33. Figure 33.

Slow IPSP does not inhibit nicotinic excitation of bullfrog sympathetic neurons. In normal Ringer solution, train of 10 presynaptic stimuli produces 12 suprathreshold nicotinic fast EPSPs followed by slow IPSP. Tops of action potentials produced by EPSPs were cropped. When cell was bathed in curare (100 μM) and same train applied, nicotinic EPSPs were almost completely blocked, leaving stimulus artifacts superimposed on intact muscarinic IPSP. It is clear then that slow IPSP starts as early as 4th stimulus artifact and is almost fully developed by 10th. Comparison of traces demonstrates that IPSP, even as it approaches its maximum amplitude, does not inhibit nicotinic EPSPs from initiating action potentials.

From Horn and Dodd 96
Figure 34. Figure 34.

Most parsimonious arrangement of neurons in myenteric plexus that mediate peristaltic reflex. lm, Longitudinal muscle; cm, circular muscle. A: graded reflex (preparatory phase) and desending inhibition. Low level of radial distension excites afferent neurons 2. Position and nature of sensory receptors 1 are unknown; they may lie in cell body, neuronal process within myenteric ganglion, or process reaching circular muscle or submucosal layers. Transmitter released by afferent neurons is not ACh (graded reflex is not blocked by hexamethonium) but may be same substance that mediates slow EPSP (substance P ?). This slowly excites cholinergic neurons 3, which project anally. These neurons, either directly or through other interneurons (not shown), excite neurons 5 that inhibit the circular muscle layer (descending inhibition). ACh released from varicosities 4 of cholinergic neurons can also reach longitudinal muscle (graded reflex). B: peristaltic reflex proper, descending excitation. Further distension of lumen excites other afferent neurons 6, which may or may not be identical to afferent neurons 2 on descending inhibitory pathway. Latency of interneuron 7 in descending excitatory pathway to reaching threshold may depend on slow EPSP and decreases as distension increases. Inter‐neuron projects anally and releases ACh onto neurons 8 that are motor to muscle layers. Neurons (5 and 8) receive nicotinic synaptic input and must be S cells. Afferent neurons (2 and 6) do not receive nicotinic synaptic input and may be AH cells. Some evidence suggests that cholinergic neurons and perhaps interneurons may also be AH cells.

From North 198


Figure 1.

A: mammalian prevertebral ganglia. CN, colonic nerves; C‐SMG, celiac‐superior mesenteric ganglia; DR, dorsal root; DRG, dorsal root ganglion; GLSN, greater and lesser splanchnic nerves; HGN, hypogastric nerves; IMG, inferior mesenteric ganglion; IMN, intermesenteric nerve; LSC, lumbar sympathetic chain; LSN, lumbar splanchnic nerves; RC, rami communicantes; and VR, ventral root. Typical arrangements of intracellular recording electrodes (left) and stimulating electrodes (right) are also shown. B: mammalian enteric ganglia. LM, longitudinal muscle; MP, myenteric plexus; CM, circular muscle; SP, submucosal plexus; SA, submucosal arteriole; and M, mucosa. Intracellular recordings are typically made from neurons lying in myenteric and submucosal ganglia, dissected as illustrated.

A from Tsunoo et al. 232; B from Furness and Costa 65


Figure 2.

Spontaneous miniature excitatory postsynaptic potentials recorded from bullfrog sympathetic ganglion cell bathed in 10 mM K+ solution.

From Kuba and Koketsu 142


Figure 3.

Mimicry of spontaneous miniature excitatory postsynaptic potential (EPSP) by iontophoretic application of acetylcholine (ACh) in frog atrial ganglion cell. Note similar time course and amplitude of spontaneous miniature EPSP and of ACh‐evoked response (records are from 2 different cells). As a rule, times to peak of miniature EPSPs were 5–8 ms, and fastest ACh potentials had range of 7–10 ms.

From Dennis et al. 47


Figure 4.

Intracellular recordings from myenteric neuron. A: fast EPSPs in response to 1 stimulus applied 100 μm away from cell soma. Downward deflection is stimulus artifact. Stimulus strengths: 1, 9 V; 2, 10 V (local response appears but does not reach threshold for full soma membrane spike); and 3, 11 V (full spike evoked). B: EPSPs declined in amplitude when evoked at frequencies >0.1 Hz. Each point with vertical bar (SE) indicates mean of data from 5 to 23 different cells. Frequency of stimuli indicated beside each curve. Values at 40 Hz are means from 3 cells. Amplitude of first EPSP ranged from 8 to 24 mV. Spontaneous variation of EPSP amplitude was observed at 0.017 Hz and may have occurred at higher frequencies.

From Nishi and North 192


Figure 5.

Reversal of fast EPSP in bullfrog sympathetic ganglion. Synaptic potentials were evoked at various levels of membrane potential (indicated in mV). Resting membrane potential was −70 mV; other potentials were obtained by application of current through recording electrode. Spike potentials were evoked by synaptic potential at membrane potentials between −22 and −70 mV. Vertical bar, 50 mV; time frequency, 1 kHz.

From Nishi and Koketsu 189


Figure 6.

Reversal potentials for synaptic transmission and iontophoretically applied ACh in frog atrial ganglion cells. A: reversal of synaptic potential alone (dotted lines, zero potential), which occurred at −12 mV. B: responses from another cell to both iontophoretically applied ACh and synaptic stimulation, recorded on same sweeps. Reversal occurred at −2 mV.

From Dennis et al. 47


Figure 7.

ACh‐induced fluctuations of membrane current and excitatory postsynaptic current (EPSC) recorded from same neuron. Digitalized records of current fluctuations before (A) and during (B) iontophoretic application of ACh (ACh‐induced steady current = 3.8 nA). C: spectral density of ACh‐induced current fluctuations is shown as function of frequency. Spectrum was obtained by subtracting averaged spectrum of 4 records similar to A from averaged spectrum of 4 records similar to B. Line through data points represents sum of 2 Lorentz functions, with cut‐off frequencies f1 and f2 corresponding to mean channel lifetimes for fast‐operating channels (τf) and for slow‐operating channels τs). S(f), spectral density at frequency f; S(0), asymptotic spectral density at frequency zero; S1(0)/S2(0) = 0.3. D: EPSC evoked by 1 preganglionic stimulus decays exponentially. E: semilogarithmic plot of EPSC amplitude against time; value of EPSC decay time constant τd) is close to τs. I(t) end‐plate current at time t; and I(0), end‐plate current at time zero.

From Skok et al. 224


Figure 8.

Organization of bullfrog lumbar paravertebral chain ganglia and fast EPSPs. A: camera lucida drawing of preparation used in experiments. It contains 7th‐10th sympathetic ganglia (G7‐G10) and 7th‐10th spinal nerves. Spinal end of 7th and 8th spinal nerves, chain above G7, and sciatic nerve were each fitted with suction electrodes, thus permitting orthodromic and antidromic stimulation of neurons in G9 and G10. B: anatomical separation of synaptic inputs to B and C neurons, a‐c, Intracellular responses of C cell to stimulation of 7th and 8th spinal nerves (a), chain above G7 (b), and sciatic nerve (c). d‐f, Intracellular responses of B cell to stimulation of chain above G7 (d), 7th and 8th spinal nerves (e), and sciatic nerve (f). Note different latencies of B and C responses. Contribution of fast nicotinic EPSPs can be seen by comparing orthodromic and antidromic responses.

From Dodd and Horn 48


Figure 9.

Intracellular recordings from 3 different neurons (1–3) in rabbit superior cervical ganglion in vivo. Note spontaneous subthreshold fast EPSPs. Inspiration occurred during time indicated by bar. Lower traces in 1 are intracellular recordings at 2 different speeds. Calibration, 50 mV; time marks (dots) are 500 ms apart.

Adapted from Skok 223


Figure 10.

Intracellular recordings from 2 cat ciliary ganglion cells in vivo (A and B). Eye was illuminated during periods indicated by bar. This reflexly induced an increase in frequency of fast EPSPs and action potentials.

From Skok 223


Figure 11.

Nicotinic and muscarinic depolarizations in same myenteric plexus cell. A: depolarization evoked by nerve stimulation. Single‐pulse stimulus (arrow) evoked fast EPSP followed by much larger and longer‐lasting slow EPSP. B: depolarization evoked by ACh iontophoresis (▴ 20 nA for 1 ms). 1, Hyoscine (1 μM) completely abolished slow depolarization but did not affect rapid depolarization. After washing out hyoscine, hexamethonium (200 nM) was used to abolish rapid depolarization. 2, At resting potential (−55 mV) ACh iontophoresis caused both rapid and slow depolarization. Rapid (nicotinic) depolarization increased with membrane hyperpolarization. Slow (muscarinic) depolarization decreased and reversed polarity with membrane hyperpolarization. Note increase in input resistance accompanying muscarinic effect of ACh.

From North and Tokimasa 202


Figure 12.

Ionic currents underlying slow EPSP in bullfrog sympathetic ganglia, hypothesized largely from voltage recordings by Kuba and Koketsu 142. Ordinates, membrane currents. Inward currents were taken as negative and outward currents as positive. Abscissas, membrane potential. Dashed lines, K+ currents (IK) caused by inactivation of K+ conductance (GK). Equilibrium potential for K+ (EK) was assumed to be −80 mV, since EK of many cells was close to this value under these experimental conditions. Dotted lines, sum of Na+ and Ca2+ currents (INa, + ICa) caused by activation of their ion conductances. Reversal level of this current was assumed to be +50 mV. Solid lines, synaptic currents for slow EPSP. In Type 1 cells, K+ inactivation is almost balanced by Na+ and K+ activation; in Type 3 cells, K+ inactivation predominates and synaptic current reverses; and in Type 2 cells, an intermediate condition exists. Type 2 cells would not show any voltage sensitivity of EPSC from −50 to −100 mV.

From Kuba and Koketsu 142


Figure 13.

Clamp currents recorded from bullfrog sympathetic neuron. A: 30‐mV hyperpolarizing voltage command from holding potential (VH) of −30 mV; B: 30‐mV depolarizing voltage command from holding potential of −60 mV. Top traces (A and B), voltage; bottom traces, current (outward current upwards). Slow inward relaxation after instantaneous current steps reflects deactivation, and outward relaxation reflects reactivation of potassium M‐current.

From Adams et al. 3


Figure 14.

Synaptic inhibition of M‐current in voltage‐clamped bullfrog ganglion cell. Effect of repetitive preganglionic stimulation (arrow) on relaxations of steady current and M‐current in a neuron voltage clamped at −35 mV (2‐electrode clamp). Nerve stimulation reduced steady outward current flowing at −35 mV but caused no change in current flowing at −65 mV. Chart speed was slowed 100‐fold during stimulus train and recovery.

From Adams and Brown 2


Figure 15.

Reversal of muscarinic slow EPSP. Intracellular recording from myenteric neuron. Slow EPSP was evoked by single‐pulse stimulus (arrow) to presynaptic fibers entering myenteric ganglion. Responses were recorded at membrane potentials indicated beside each trace. Initial rapid upward deflection is fast EPSP. Action potentials evoked by fast EPSP (at −28 and −50 mV) are truncated.

K. Morita and R. A. North, unpublished observations


Figure 16.

Reversal of slow muscarinic ACh potential in myenteric neuron. A: response to iontophoresis of ACh (10 nA/100 ms) recorded at membrane potential shown beside each trace. Electrotonic potentials were removed from all but 2 traces. Hexamethonium (200 μM) was present throughout. B: amplitude of ACh potential as function of membrane potential. Reversal of muscarinic ACh potential occurs near −90 mV.

From Morita et al. 182


Figure 17.

Fast nicotinic and slow muscarinic responses in single myenteric neuron. Iontophoresis of ACh (▴, 20 nA/1 ms) evoked nicotinic depolarization followed by muscarinic depolarization. Top trace, control; bottom trace, after adding hexamethonium (200 μM) to perfusing solution. Hexamethonium blocked nicotinic response and slightly increased amplitude of initial component of muscarinic depolarization. Electrotonic potentials are evoked by slightly larger current in bottom trace; hexamethonium itself did not change input resistance or membrane potential. Slight increase in amplitude of initial part of muscarinic response in presence of hexamethonium is due to removal of an afterhyperpolarization that results from Ca2+ entry during the nicotinic depolarization.

From Tokimasa et al. 228


Figure 18.

Four types of synaptic responses in neurons of bullfrog 10th sympathetic ganglion measured with intracellular electrodes. A: single preganglionic stimulus produces fast subthreshold EPSP (left); stronger stimulus excites 2nd axon, producing larger EPSP and impulse. B: Slow inhibitory postsynaptic potential (IPSP) in a C neuron (lasting 2 s) on stimulation of central portion of 7th and 8th spinal nerves with 13 pulses at 20 Hz. Fast EPSPs were blocked with dihydro‐β‐erythroidine. C: slow cholinergic EPSP (lasting 30 s) results from 4 pulses at 50 Hz applied to synaptic chain above 7th sympathetic ganglion. Initial rapid deflections are 4 large nerve impulses (cropped). D: late slow EPSP (peptidergic) lasts −300 s on stimulation of central portions of 7th and 8th spinal nerves (50 pulses at 10 Hz). Nicotinic blocking drugs were used in B.

From Jan et al. 101


Figure 19.

Intracellular recording from guinea pig myenteric plexus neuron. Optimum stimulus frequency needed to evoke late slow EPSP is ∼20 Hz. Late slow EPSPs were evoked by 2 pulses (500‐μs duration) applied to presynaptic fibers entering ganglion. Neither 1 pulse, nor 2 pulses separated by 2 ms, elicited a response. Interval between pulses was then increased (indicated in ms). Late slow EPSP was largest at interval of 30–100 ms (33–10 Hz), and then declined. Pulse separations of 1, 2, and 5 s elicited responses similar to 500 ms; pulse separation of 10 ms did not elicit a response (not shown).

J. C. Bornstein and R. A. North, unpublished observations


Figure 20.

Different types of late slow EPSCs recorded from 2 voltage‐clamped bullfrog sympathetic neurons. Responses were elicited by train of supramaximal preganglionic stimuli at 10 Hz for 5 s (arrows). Top traces in A and B are voltage recordings showing command pulses (lasting 1 s) of 15 mV (A) and 30 mV (B) repeated at 0.3 Hz. Middle and bottom traces are current recordings at indicated holding potentials. First type of response (A) is accompanied by fall in conductance (reduced current excursion for fixed‐voltage command) and decreases with hyperpolarization. Second type of response (B) is accompanied by rise in conductance and increases with membrane hyperpolarization. Note difference in time course.

From Katayama and Nishi 119


Figure 21.

Nerve‐evoked peptidergic late slow EPSCs and muscarinic slow EPSPs in 3 bullfrog sympathetic neurons. Left traces, nonreversing response; center traces, reversing response. Cells were voltage clamped at membrane potential indicated beside each current recording, and 7th and 8th spinal nerves (carrying peptidergic fibers) were stimulated at 20 Hz for 5 s (arrows). Resting membrane potentials of both of these cells were ca. −50 mV, with 2 mM K+ in bathing solution. Right traces, muscarinic slow EPSCs following 6 pulses at 50 Hz applied to sympathetic chain. Clamped‐membrane potential is indicated beside each trace. Resting membrane potential of cell was −35 mV. Dihydro‐β‐erythroidine and prostigmine were present in bathing solution, with 6 mM K+ also present. Note reversal of early, but not late, part of response.

From Kuffler and Sejnowski 146


Figure 22.

Substance P (SP) immunoreactivity in guinea pig inferior mesenteric ganglion. A: pattern of varicose and nonvaricose fibers is revealed by monoclonal antibody in inferior mesenteric ganglion of normal guinea pig, perfused and processed together with tissue in B. B: inferior mesenteric ganglion of capsaicin‐treated guinea pig, showing total loss of specific SP immunofluoresence, apart from small residual trace (*). C: SP immunofluorescence in inferior mesenteric ganglion of normal guinea pig, perfused and processed together with tissue in D. D: almost total disappearance of SP immunofluorescence in guinea pig inferior mesenteric ganglion 4 days after lumbar nerves were severed. E: persistence of varicose and nonvaricose SP immunoreactive (SPI) fibers in inferior mesenteric ganglion of guinea pig in which spinal cord had been removed (below Th7) 4 days previously. F: trails of varicosities immunoreactively labeled by SP/peroxidase‐antiperoxidase method in 50‐μm slice of celiac superior mesenteric ganglion, photographed before osmication and embedding for electron microscopy. G: electron micrograph showing dense deposits revealing SPI material over nerve terminal (*) synapsing with dendrite (D) of sympathetic postganglionic neuron. This type of nerve terminal (commonly seen in guinea pig inferior mesenteric ganglion) contains a large cluster of small clear synaptic vesicles, which are massed in presynaptic zone; it also contains a lesser number of large dense‐core vesicles, lying chiefly at periphery of cluster of small vesicles (away from presynaptic membrane), together with group of mitochondria. SP immunoreactivity within nerve terminal is localized over cores of large dense‐core vesicles and is also associated with cytoplasmic (external) surfaces of small vesicles; both features have been reported for SPI‐nerve terminals in substantia gelatinosa of spinal cord. N, nucleus of satellite cell; S, satellite cell cytoplasm; ct, connective tissue space. Scale: bars, 1 μm for A‐F and 0.5 μm for G. H: organization of sensory SPI‐peripheral nerve fibers at lumbar spinal levels. Example is sensory neuron of lumbar origin innervating colon by way of lumbar splanchnic nerve and colonic branch of inferior mesenteric ganglion (IMG). DH, dorsal horn; VH, ventral horn; sg, substantia gelatinosa; DRG, dorsal root ganglion; LSG, lumbar sympathetic ganglion of paravertebral chain; LSN, lumbar splanchnic nerve; imn, intermesenteric nerve; CN, colonic nerve fascicle; and HNN, hypogastric nerves.

From Matthews and Cuello 171


Figure 23.

A: intracellular recording from a myenteric neuron. Substance P was applied by electrophoresis (40 nA, 5 s) to soma membrane (▴). High‐concentration K+ solution (bar) depolarized membrane and greatly reduced amplitude of substance P potential. Membrane potential was shifted back to control level (arrow down) by hyperpolarizing current. Substance P potential was now reversed. These changes were reversible when hyperpolarizing current was terminated (arrow up) and when perfusion with normal Krebs solution was restarted. B: relationship between substance P reversal potential and extracellular [K+]. Reversal potentials are mean values (with SE indicated) for number of cells shown in parentheses. Slope of dashed line (fitted by eye) is 54 mV/10‐fold change in [K+].

From Katayama et al. 120


Figure 24.

Responses of AH‐myenteric plexus neuron to repetitive presynaptic nerve stimulation. A: nerve stimulation (10 Hz/3 s) is indicated by arrow and bar. Response was biphasic. Hyoscine (1 μM) abolished initial component of slow synaptic potential (combination of slow EPSP and late slow EPSP), whereas tetrodotoxin (TTX, 100 nM) abolished entire synaptic potential. B: example from another AH neuron. Hyoscine (1 μM) depressed only initial part of slow potential. Total duration of slow EPSP is not shown but was ∼3 min. C: amplitude of muscarinic component of response in B obtained by subtracting amplitude when hyoscine was present from amplitude when it was not.

From North and Tokimasa 202


Figure 25.

Schematic representation of synaptic potentials that can be recorded in bullfrog lumbar 9th or 10th sympathetic ganglion B and C cells (see also Fig. 18). Fast EPSPs can be recorded from B cells by stimulating presynaptic B‐fibers and from C cells by stimulating presynaptic C‐fibers. Slow EPSPs can be recorded from B cells by stimulating presynaptic B‐fibers. Late slow EPSPs can be recorded from B and C cells, but only by stimulating presynaptic C‐fibers. Transmitter, luteinizing hormone‐releasing hormone (LHRH), is assumed to diffuse to B cells. Slow IPSPs can be recorded in C cells when presynaptic C‐fibers are stimulated. 6–8, Spinal nerves.



Figure 26.

Intracellular recording from bullfrog sympathetic ganglion C cell. Reversal of action‐potential afterpotential, slow IPSP and muscarinic ACh response in curarized neuron. Amount of polarizing current is indicated for each trace. Tops of antidromic action potentials were cropped. Synaptic and ACh responses have same reversal potential. Arrows indicate half‐decay points of muscarinic responses. Decay times increased as cell was hyperpolarized from rest (ca. −50 mV). T = 22°C.

From Dodd and Horn 49


Figure 27.

Intracellular recording from ganglion cell in mudpuppy cardiac ganglion. Reversal potentials of inhibitory responses resulting from nerve stimulation (30 Hz for 700 ms) and iontophoretic application of ACh (20 nA for 10 ms) and bethanechol (170 nA for 20 ms). Membrane potential was monitored and varied by current passed through an electrode. Bathing solution contained 5 × 10−8 M dihydro‐β‐erythroidine to attenuate excitatory responses. As cell was hyperpolarized, magnitude of fast excitatory responses increased, while inhibitory responses decreased and reversed polarity between −90 and −100 mV for all modes of stimulation. Stimulus is indicated by bar or dot. Excitatory responses to nerve stimulation partially obscured inhibitory responses. Responses to all 3 types of stimulation have same reversal potential.

From Hartzell et al. 82


Figure 28.

Enkephalin causes presynaptic inhibition by blocking action‐potential propagation. Left: control shows fast EPSP recorded intracellularly from myenteric neuron in guinea pig small intestine. Single stimulus evoked 20‐mV multifiber EPSP (trace is average of 4 with similar amplitudes). Enkephalin was applied from pipette (tip diam 5 μm) containing 1 μM Met5‐enkephalin. Pipette tip was moved to various positions on surface of myenteric plexus (right), and enkephalin was ejected by a 300‐ms pressure pulse. At positions 1 and 3 enkephalin had no effect. At 2, enkephalin reduced EPSP amplitude; this effect recovered within 2–3 min.

E. Cherubini and R. A. North, unpublished observations


Figure 29.

Interaction between muscarinic and peptidergic late slow EPSCs. Bullfrog sympathetic neuron was voltage clamped at its resting potential (−58 mV), and cholinergic input was stimulated 10 times at 50 Hz, with stimulation repeated every 2 min. Fast nicotinic responses are cropped (arrow). Amount of muscarinic current was reduced after train of 100 stimuli at 20 Hz was applied to 7th and 8th spinal nerves and recovered with decline of peptidergic current.

From Kuffler and Sejnowski 146


Figure 30.

Nerve‐released transmitter of late slow EPSP (probably substance P) depresses muscarinic ACh response in a myenteric neuron. Top: trace 1, control response to ACh iontophoresis (10 nA/1 ms). Center trace, response to 1 stimulus applied to presynaptic nerves (ns). This evokes typical muscarinic slow EPSP. Right trace, beginning of late slow EPSP evoked by repetitive stimulation of presynaptic nerves (10 Hz, 3 s; bar). Bottom: responses to ACh evoked after onset of nerve stimulation. Traces 2 and 3, applications of ACh during noncholinergic slow EPSP evoked 11 s (2) and 38 s (3) after nerve stimulation. Response to ACh is abolished or depressed. Depolarization of membrane to same level would increase amplitude of ACh response. Trace 4, full recovery of ACh response 93 s after repetitive nerve stimulation, when late slow EPSP had declined.

From Tokimasa and North 230


Figure 31.

IPSP inhibits repetitive firing of bullfrog sympathetic neurons. This intracellular recording was taken from a C cell during period of repetitive firing induced by late slow EPSP. Tubocurarine (100 μM) was used to block nicotinic synapses. Train of presynaptic stimuli was applied to neurons (dotted line) and an IPSP was produced. As IPSP developed, repetitive firing was inhibited. As IPSP subsided, membrane potential began to oscillate and repetitive firing recommenced.

From Horn and Dodd 96


Figure 32.

Effect of inhibitory nerve stimulation on time course of EPSP recorded at reversal potential for IPSP. A: control records of electrotonic potential and fast EPSP. B: records of electrotonic potential and fast EPSP when membrane was shunted by stimulating inhibitory nerves. Bottom traces, EPSPs recorded at faster sweep speed and higher amplification. Arrow, stimulation of inhibitory nerves. No potential change occurred, because membrane was held at IPSP reversal potential. C: time courses of EPSPs, before (○) and during (•) inhibitory conductance change. Solid lines, time courses of EPSPs computed with assumptions that control cell resistance was 180 MΩ and fell to 80 MΩ during IPSP and that cell capacitance was 94 pF throughout. Dashed line, time course of synaptic current required to simulate both EPSPs.

From Edwards et al. 59


Figure 33.

Slow IPSP does not inhibit nicotinic excitation of bullfrog sympathetic neurons. In normal Ringer solution, train of 10 presynaptic stimuli produces 12 suprathreshold nicotinic fast EPSPs followed by slow IPSP. Tops of action potentials produced by EPSPs were cropped. When cell was bathed in curare (100 μM) and same train applied, nicotinic EPSPs were almost completely blocked, leaving stimulus artifacts superimposed on intact muscarinic IPSP. It is clear then that slow IPSP starts as early as 4th stimulus artifact and is almost fully developed by 10th. Comparison of traces demonstrates that IPSP, even as it approaches its maximum amplitude, does not inhibit nicotinic EPSPs from initiating action potentials.

From Horn and Dodd 96


Figure 34.

Most parsimonious arrangement of neurons in myenteric plexus that mediate peristaltic reflex. lm, Longitudinal muscle; cm, circular muscle. A: graded reflex (preparatory phase) and desending inhibition. Low level of radial distension excites afferent neurons 2. Position and nature of sensory receptors 1 are unknown; they may lie in cell body, neuronal process within myenteric ganglion, or process reaching circular muscle or submucosal layers. Transmitter released by afferent neurons is not ACh (graded reflex is not blocked by hexamethonium) but may be same substance that mediates slow EPSP (substance P ?). This slowly excites cholinergic neurons 3, which project anally. These neurons, either directly or through other interneurons (not shown), excite neurons 5 that inhibit the circular muscle layer (descending inhibition). ACh released from varicosities 4 of cholinergic neurons can also reach longitudinal muscle (graded reflex). B: peristaltic reflex proper, descending excitation. Further distension of lumen excites other afferent neurons 6, which may or may not be identical to afferent neurons 2 on descending inhibitory pathway. Latency of interneuron 7 in descending excitatory pathway to reaching threshold may depend on slow EPSP and decreases as distension increases. Inter‐neuron projects anally and releases ACh onto neurons 8 that are motor to muscle layers. Neurons (5 and 8) receive nicotinic synaptic input and must be S cells. Afferent neurons (2 and 6) do not receive nicotinic synaptic input and may be AH cells. Some evidence suggests that cholinergic neurons and perhaps interneurons may also be AH cells.

From North 198
References
 1. Adams, P. R., and D. A. Brown. Actions of γ‐aminobutyric acid on sympathetic ganglion cells. J. Physiol. London 250: 85–120, 1975.
 2. Adams, P. R., and D. A. Brown. Synaptic inhibition of the M‐current: slow excitatory post‐synaptic potential mechanism in bullfrog sympathetic neurones. J. Physiol. London 332: 263–272, 1982.
 3. Adams, P. R., D. A. Brown, and A. Constanti. M‐currents and other potassium currents in bullfrog sympathetic neurones. J. Physiol. London 330: 537–572, 1982.
 4. Adams, P. R., D. A. Brown, and A. Constanti. Pharmacological inhibition of the M‐current. J. Physiol. London 332: 223–262, 1982.
 5. Adams, P. R., D. A. Brown, and S. W. Jones. Substance P inhibits the M‐current in bullfrog sympathetic neurones. Br. J. Pharmacol. 79: 330–333, 1983.
 6. Adams, P. R., A. Constanti, D. A. Brown, and R. B. Clark. Intracellular Ca2+ activates a fast voltage‐sensitive K+ current in vertebrate sympathetic neurones. Nature London 296: 746–749, 1982.
 7. Akasu, T. Voltage‐clamp analysis of muscarinic effects on action potentials in sympathetic ganglion cells of bullfrogs (Abstract). Neurosci. Lett. 6, Suppl.: 559, 1981.
 8. Akasu, T., and K. Koketsu. Modulation of voltage‐dependent currents by muscarinic receptor in sympathetic neurones of bullfrog. Neurosci. Lett. 29: 41–45, 1982.
 9. Ascher, P., W. A. Large, and H. P. Rang. Studies on the mechanism of action of acetylcholine antagonists on rat parasympathetic ganglion cells. J. Physiol. London 295: 139–170, 1979.
 10. Ashe, J. H., and B. Libet. Modulation of slow postsynaptic potentials by dopamine, in rabbit sympathetic ganglion. Brain Res. 217: 93–106, 1981.
 11. Ashe, J. H., and B. Libet. Orthodromic production of non‐cholinergic slow depolarising response in the superior cervical ganglion of the rabbit. J. Physiol. London 320: 333–346, 1981.
 12. Ashe, J. H., and B. Libet. Pharmacological properties and monoaminergic mediation of the slow IPSP, in mammalian sympathetic ganglion. Brain Res. 242: 345–349, 1982.
 13. Barthó, L., P. Holzer, J. Donnerer, and F. Lembeck. Evidence for the involvement of substance P in the atropine‐resistant peristalsis of the guinea‐pig ileum. Neurosci. Lett. 32: 69–74, 1982.
 14. Bayliss, W. M., and E. H. Starling. The movements and innervation of the small intestine. J. Physiol. London 24: 99–143, 1899.
 15. Bennett, M. R. Autonomic Neuromuscular Transmission. Cambridge, UK: Cambridge Univ. Press, 1972.
 16. Bennett, M. R., G. Burnstock, and M. E. Holman. Transmission from intramural inhibitory nerves to the smooth muscle of the guinea‐pig taenia coli. J. Physiol. London 182: 541–558, 1966.
 17. Bennett, M. R., T. Florin, and A. G. Pettigrew. The effect of calcium ions on the binomial statistic parameters that control acetylcholine release at preganglionic nerve terminals. J. Physiol. London 257: 597–620, 1976.
 18. Blackman, J. G. Dependence on membrane potential of the blocking action of hexamethonium at a sympathetic ganglionic synapse. Proc. Univ. Otago Med. Sch. 48: 4–5, 1970.
 19. Blackman, J. G., P. J. Crowcroft, C. E. Devine, M. E. Holman, and K. Yonemura. Transmission from preganglionic fibres in the hypogastric nerve to peripheral ganglia of male guinea pigs. J. Physiol. London 201: 723–743, 1969.
 20. Blackman, J. G., and R. D. Purves. Intracellular recordings from ganglia of the thoracic sympathetic chain of the guineapig. J. Physiol. London 203: 173–198, 1969.
 21. Booth, A. M., and W. C. DeGroat. A study of facilitation in vesical parasympathetic ganglia of the cat using intracellular recording techniques. Brain Res. 169: 388–392, 1979.
 22. Bornstein, J. C. Spontaneous multiquantal release at synapse in guinea‐pig hypogastric ganglia: evidence that release can occur in bursts. J. Physiol. London 282: 375–398, 1978.
 23. Bornstein, J. C., R. A. North, M. Costa, and J. B. Furness. Excitatory synaptic potentials due to activation of neurons with short projections in the myenteric plexus. Neuroscience 11: 723–732, 1984.
 24. Brown, D. A., and P. R. Adams. Muscarinic suppression of a novel voltage‐sensitive K+ current in a vertebrate neurone. Nature London 283: 673–676, 1980.
 25. Brown, D. A., P. R. Adams, and A. Constanti. Voltage‐sensitive K‐currents in sympathetic neurons and their modulation by neurotransmitters. J. Auton. Nerv. Syst. 6: 23–35, 1982.
 26. Brown, D. A., and M. P. Caulfield. Hyperpolarizing α2‐adrenoceptors in rat sympathetic ganglia. Br. J. Pharmacol. 65: 435–445, 1979.
 27. Brown, D. A., A. E. Constanti, and S. Marsh. Angiotensin mimics the action of muscarinic agonists on rat sympathetic neurones. Brain Res. 193: 614–619, 1980.
 28. Burnstock, G. Purinergic nerves. Pharmacol. Rev. 24: 509–581, 1972.
 29. Burnstock, G. Interactions of cholinergic, adrenergic, purinergic and peptidergic neurons in the gut. In: Integrative Functions of the Autonomic Nervous System, edited by C. McC. Brooks, K. Koizumi, and A. Sato. Amsterdam: Elsevier, 1979, p. 145–158.
 30. Burnstock, G. Neurotransmitters and trophic factors in the autonomic nervous system. J. Physiol. London 313: 1–55, 1981.
 31. Busis, N. A., F. F. Weight, and P. A. Smith. Synaptic potentials in sympathetic ganglia: are they mediated by cyclic nucleotides? Science 200: 1079–1081, 1978.
 32. Cherubini, E., and R. A. North. γ‐Aminobutyric acid actions on neurones of guinea‐pig myenteric plexus. Br. J. Pharmacol. 82: 93–100, 1984.
 33. Cherubini, E., and R. A. North. Inhibition of calcium spikes and transmitter release by γ‐aminobutyric acid in the guineapig myenteric plexus. Br. J. Pharmacol. 82: 101–106, 1984.
 34. Christ, D. D., and S. Nishi. Effects of adrenaline on nerve terminals in the superior cervical ganglion of the rabbit. Br. J. Pharmacol. 41: 331–448, 1971.
 35. Cole, A. E., and P. Shinnick‐Gallagher. Alpha‐adrenoceptor and dopamine receptor antagonists do not block the slow inhibitory postsynaptic potential in sympathetic ganglia. Brain Res. 187: 226–230, 1980.
 36. Cole, A. E., and P. Shinnick‐Gallagher. Comparison of the receptors mediating the catecholamine hyperpolarization and slow inhibitory postsynaptic potential in sympathetic ganglia. J. Pharmacol. Exp. Ther. 217: 440–444, 1981.
 37. Collier, B. Biochemistry and physiology of cholinergic transmission. In: Handbook of Physiology. The Nervous System. Cellular Biology of Neurons, edited by E. R. Kandel. Bethesda, MD: Am. Physiol. Soc., 1977, sect. 1, vol. I, pt. 1, chapt. 13, p. 463–492.
 38. Colquhoun, D. The link between drug binding and response: theories and observations. In: The Receptors: A Comprehensive Treatise, edited by R. D. O'Brien. New York: Plenum, 1979, p. 93–142.
 39. Constanti, A., and D. A. Brown. M‐currents in voltage‐clamped mammalian sympathetic neurones. Neurosci. Lett. 24: 289–294, 1981.
 40. Costa, M., A. C. Cuello, J. B. Furness, and R. Franco. Distribution of enteric neurons showing immunoreactivity for substance P in the guinea‐pig ileum. Neuroscience 5: 323–331, 1980.
 41. Costa, M., and J. B. Furness. The peristaltic reflex: an analysis of the nerve pathways and their pharmacology. Naunyn‐Schmeideberg's Arch. Pharmacol. 294: 47–60, 1976.
 42. Costa, M., and J. B. Furness. Nervous control of intestinal motility. In: Handbook of Experimental Pharmacology. Mediators and Drugs in Gastrointestinal Motility. Morphological Basis and Neurophysiological Control, edited by G. Bertaccini. Berlin: Springer‐Verlag, 1982, vol. 59, pt. 1, p. 279–461.
 43. Crowcroft, P. J., M. E. Holman, and J. H. Szurszewski. Excitatory input from the distal colon to the inferior mesenteric ganglion in the guinea pig. J. Physiol London 219: 443–461, 1971.
 44. Crowcroft, P. J., and J. H. Szurszewski. A study of the inferior mesenteric and pelvic ganglia of guinea‐pigs with intracellular electrodes. J. Physiol. London 219: 421–441, 1971.
 45. Cunnane, T. J., and L. Starjne. Secretion of transmitter from individual varicosities of guinea‐pig and mouse vas deferens: all‐or‐none and extremely intermittent. Neuroscience 7: 2565–2576, 1982.
 46. DelCastillo, J., and B. Katz. Quantal components of the endplate potential J. Physiol. London 124: 560–573, 1954.
 47. Dennis, M. J., A. J. Harris, and S. W. Kuffler. Synaptic transmission and its duplication by focally applied acetylcholine in parasympathetic neurones in the heart of the frog. Proc. R. Soc. London Ser. B 177: 509–539, 1971.
 48. Dodd, J., and J. P. Horn. A reclassification of B and C neurones in the ninth and tenth paravertebral sympathetic ganglia of the bullfrog. J. Physiol. London 334: 255–269, 1983.
 49. Dodd, J., and J. P. Horn. Muscarinic inhibition of sympathetic C neurones in the bullfrog. J. Physiol. London 334: 271–291, 1983.
 50. Dun, N. J., and Z. G. Jiang. Non‐cholinergic excitatory transmission in inferior mesenteric ganglia of the guinea‐pig: possible mediation by substance P. J. Physiol. London 325: 145–159, 1981.
 51. Dun, N. J., and A. G. Karczmar. The presynaptic site of action of norepinephrine in the superior cervical ganglion of the guinea pig. J. Pharmacol. Exp. Ther. 200: 328–335, 1977.
 52. Dun, N. J., and A. G. Karczmar. Evidence for a presynaptic inhibitory action of 5‐hydroxytryptamine in a mammalian sympathetic ganglion. J. Pharmacol. Exp. Ther. 217: 714–718, 1981.
 53. Dun, N. J., and S. Minota. Effects of substance P on neurones of the inferior mesenteric ganglia of the guinea‐pig. J. Physiol. London 321: 259–271, 1981.
 54. Dun, N. J., and S. Nishi. Effects of dopamine on the superior cervical ganglion of the rabbit. J. Physiol. London 239: 155–164, 1974.
 55. Dunant, Y., and M. Dolivo. Relations entre les potentiels synaptiques lents et l'excitabilité du ganglion sympathetique chez le rat. J. Physiol. Paris 59: 281–294, 1967.
 56. Eccles, J. C. The Physiology of Synapses. Berlin: Springer‐Verlag, 1964.
 57. Eccles, R. M. Intracellular potentials recorded from a mammalian sympathetic ganglion. J. Physiol. London 130: 572–584, 1955.
 58. Eccles, R. M., and B. Libet. Origin and blockade of the synaptic responses of curarized sympathetic ganglia. J. Physiol. London 157: 484–503, 1961.
 59. Edwards, F. R., G. D. S. Hirst, and E. M. Silinsky. Interaction between inhibitory and excitatory synaptic potentials at a peripheral neurone. J. Physiol. London 259: 647–663, 1976.
 60. Edwards, F. R., S. J. Redman, and B. Walmsley. Nonquantal fluctuations and transmission failures in charge transfers at Ia synapses on spinal motoneurones. J. Physiol. London 259: 689–704, 1976.
 61. Erulkar, S. D., and J. K. Woodward. Intracellular recording from mammalian superior cervical ganglion in situ. J. Physiol. London 199: 189–204, 1968.
 62. Fahrenkrug, J., U. Haglund, M. Jodal, O. Lundgren, L. Olbe, and O. B. Schaffalitzky de Muckadell. Nervous release of vasoactive intestinal polypeptide in the gastrointestinal tract of cats: possible physiological implications. J. Physiol. London 284: 291–305, 1978.
 63. Franco, R., M. Costa, and J. B. Furness. Evidence for the release of endogenous substance P from intestinal nerves. Naunyn‐Schmeideberg's Arch. Pharmacol. 306: 195–201, 1979.
 64. Furchgott, R. F. The classification of adrenoceptors (adrenergic receptors). An evaluation from the standpoint of receptor theory. In: Handbook of Experimental Pharmacology. Catecholamines, edited by H. Blaschko and E. Muscholl. Berlin: Springer‐Verlag, 1972, vol. 33, p. 283–335.
 65. Furness, J. B., and M. Costa. Types of nerves in the enteric nervous system. Neuroscience 5: 1–20, 1980.
 66. Furness, J. B., and M. Costa. Identification of gastrointestinal neurotransmitters. In: Handbook of Experimental Pharmacology. Mediators and Drugs in Gastrointestinal Motility. Morphological Basis and Neurophysiological Control, edited by G. Bertaccini. Berlin: Springer‐Verlag, 1982, vol. 59, pt. 1, p. 383–462.
 67. Furshpan, E. J., D. D. Potter, and S. J. Landis. On the transmitter repertoire of sympathetic neurons in culture. Harvey Lect. 76: 149–191, 1982.
 68. Gabella, G. Structure of the Autonomic Nervous System. London: Chapman & Hall, 1976.
 69. Gallagher, J. P., W. H. Griffith, and P. Shinnick‐Gallagher. Cholinergic transmission in cat parasympathetic ganglia. J. Physiol. London 332: 473–486, 1982.
 70. Gallagher, J. P., and P. Shinnick‐Gallagher. Cyclic nucleotides injected intracellulary into rat superior cervical ganglion cells. Science 198: 851–852, 1977.
 71. Gallagher, J. P., P. Shinnick‐Gallagher, A. E. Cole, W. H. Griffith III, and B. J. Williams. Current hypotheses for the slow inhibitory postsynaptic potential in sympathetic ganglia. Federation Proc. 39: 3009–3015, 1980.
 72. Galvan, M., and P. R. Adams. Control of calcium current in rat sympathetic neurons by norepinephrine. Brain Res. 244: 135–144, 1982.
 73. Galvan, M., P. Grafe, and G. ten Bruggencate. Presynaptic actions of 4‐aminopyridine and γ‐aminobutyric acid on rat sympathetic ganglia in vitro. Naunyn‐Schmiedeberg's Arch. Pharmacol. 314: 141–147, 1980.
 74. Gershon, M. D. The enteric nervous system. Annu. Rev. Neurosci. 4: 227–272, 1981.
 75. Ginsborg, B. L. On the presynaptic acetylcholine receptors in sympathetic ganglia of the frog. J. Physiol. London 216: 237–246, 1971.
 76. Grafe, P., C. J. Mayer, and J. D. Wood. Synaptic modulation of calcium‐dependent potassium conductance in myenteric neurones in the guinea‐pig. J. Physiol. London 305: 235–248, 1980.
 77. Greengard, P., and J. W. Kebabian. Role of cyclic AMP in synaptic transmission in the mammalian peripheral nervous system. Federation Proc. 33: 1059–1067, 1974.
 78. Griffith, W. H., III, J. P. Gallagher, and P. Shinnick‐Gallagher. An intracellular investigation of cat vesical pelvic ganglia. J. Neurophysiol. 43: 343–354, 1980.
 79. Hammer, R., C. P. Berrie, N. J. M. Birdsall, A. S. V. Burgen, and E. C. Hulme. Pirenzipine distinguishes between different subclasses of muscarinic receptors. Nature London 283: 90–92, 1980.
 80. Harris, A. J., S. W. Kuffler, and M. J. Dennis. Differential chemosensitivity of synaptic and extrasynaptic areas on the neuronal surface membrane in parasympathetic neurones of the frog, tested by microapplication of acetylcholine. Proc. R. Soc. London Ser. B 177: 541–553, 1971.
 81. Hartzell, H. C. Mechanisms of slow postsynaptic potentials. Nature London 291: 539–544, 1981.
 82. Hartzell, H. C., S. W. Kuffler, R. Stickgold, and D. Yoshikami. Synaptic excitation and inhibition resulting from direct action of acetylcholine on two types of chemoreceptors on individual amphibian parasympathetic neurones. J. Physiol. London 271: 817–846, 1977.
 83. Hashiguchi, H., H. Kobayashi, T. Tosaka, and B. Libet. Two muscarinic depolarizing mechanisms in mammalian sympathetic neurons. Brain Res. 242: 378–382, 1982.
 84. Henderson, C. G., and A. Ungar. Effect of cholinergic antagonists on sympathetic ganglionic transmission of vasomotor reflexes from the carotid baroreceptors and chemoreceptors of the dog. J. Physiol. London 277: 379–385, 1978.
 85. Henon, B. K., and D. A. McAfee. The ionic basis of adenosine receptor actions on postganglionic neurones in the rat. J. Physiol. London 336: 607–620, 1983.
 86. Hirst, G. D. S., M. E. Holman, and I. Spence. Two types of neurones in the myenteric plexus of duodenum in the guinea pig. J. Physiol. London 236: 303–326, 1974.
 87. Hirst, G. D. S., and H. C. McKirdy. A nervous mechanism for descending inhibition in guinea‐pig small intestine. J. Physiol. London 238: 129–143, 1974.
 88. Hirst, G. D. S., and H. C. McKirdy. Presynaptic inhibition at a mammalian peripheral synapse? Nature London 250: 430–431, 1974.
 89. Hirst, G. D. S., and H. C. McKirdy. Synaptic potentials recorded from some neurones of the submucous plexus of the guinea‐pig small intestine. J. Physiol. London 249: 369–385, 1975.
 90. Hirst, G. D. S., and I. Spence. Calcium action potentials in mammalian peripheral neurones. Nature London New Biol. 243: 54–56, 1973.
 91. Hodgkin, A. L. The conduction of the nervous impulse. In: The Sherrington Lectures VII. Liverpool, UK: Liverpool Univ. Press, 1967.
 92. Hökfelt, T., O. Johansson, A. Ljungdahl, J. M. Lundberg, and M. Schultzberg. Peptidergic neurones. Nature London 284: 515–521, 1980.
 93. Holman, M. E., and G. D. S. Hirst. Junctional transmission in smooth muscle and the autonomic nervous system. In: Handbook of Physiology. The Nervous System. Cellular Biology of Neurons, edited by E. R. Kandel. Bethesda, MD: Am. Physiol. Soc., 1977, sect. 1, vol. I, pt. 1, chapt 12, p. 417–461.
 94. Holman, M. E., T. C. Muir, J. H. Szurszewski, and K. Yonemura. Effect of iontophoretic application of cholinergic agonists and their antagonists to guinea‐pig pelvic ganglia. Br. J. Pharmacol. 41: 26–40, 1971.
 95. Horn, J. P., and J. Dodd. Monosynaptic muscarinic activation of K+ conductance underlies the slow inhibitory postsynaptic potential in sympathetic ganglia. Nature London 292: 625–627, 1981.
 96. Horn, J. P., and J. Dodd. Inhibitory cholinergic synapses in autonomic ganglia. Trends Neurosci. 6: 180–184, 1983.
 97. Horn, J. P., and D. A. McAfee. Alpha‐adrenergic inhibition of calcium‐dependent potentials in rat sympathetic neurones. J. Physiol. London 301: 191–204, 1980.
 98. Ivanov, A. Y., and V. I. Skok. Slow inhibitory postsynaptic potentials and hyperpolarization evoked by noradrenaline in the neurones of mammalian sympathetic ganglion. J. Auton. Nerv. Syst. 1: 255–263, 1980.
 99. Jan, L. Y., and Y. N. Jan. Peptidergic transmission in sympathetic ganglia of the frog. J. Physiol. London 327: 219–246, 1982.
 100. Jan, L. Y., Y. N. Jan, and M. S. Brownfield. Peptidergic transmitters in synaptic boutons of sympathetic ganglia. Nature London 288: 380–382, 1980.
 101. Jan, Y. N., L. Y. Jan, and S. W. Kuffler. A peptide as a possible transmitter in sympathetic ganglia of the frog. Proc. Natl. Acad. Sci. USA 76: 1501–1505, 1979.
 102. Jan, Y. N., L. Y. Jan, and S. W. Kuffler. Further evidence for peptidergic transmission in sympathetic ganglia. Proc. Natl. Acad. Sci. USA 77: 5008–5012, 1980.
 103. Jänig, W. Reciprocal reaction patterns of sympathetic subsystems with respect to various afferent inputs. In: Integrative Functions of the Autonomic Nervous System, edited by C. McC. Brooks. Amsterdam: Elsevier, 1979, p. 263–274.
 104. Jänig, W., and H. Blumberg. Enhancement of resting activity in postganglionic vasoconstrictor neurones following short‐lasting repetitive activation of preganglionic axons. Pfluegers Arch. 396: 89–94, 1983.
 105. Jänig, W., R. Krauspe, and G. Wiedersatz. Transmission of impulses from pre‐ to postganglionic vasoconstrictor and sudomotor neurons. J. Auton. Nerv. Syst. 6: 95–106, 1982.
 106. Jänig, W., R. Krauspe, and G. Wiedersatz. Reflex activation of postganglionic vasoconstrictor neurones supplying skeletal muscle by stimulation of arterial chemoreceptors via non‐nicotinic synaptic mechanisms in sympathetic ganglia. Pfluegers Arch. 396: 95–100, 1983.
 107. Jänig, W., and P. Szulczyk. The organization of lumbar preganglionic neurons. J. Auton. Nerv. Syst. 3: 177–191, 1981.
 108. Jessen, K. R., R. Mirsky, M. E. Dennison, and G. Burnstock. GABA may be a neurotransmitter in the vertebrate peripheral nervous system. Nature London 281: 71–74, 1979.
 109. Jiang, Z. G., and N. J. Dun. Multiple conductance change associated with the slow excitatory potential in mammalian sympathetic neurons. Brain Res. 229: 203–208, 1981.
 110. Jiang, Z. G., N. J. Dun, and A. G. Karczmar. Substance P: a putative sensory transmitter in mammalian autonomic ganglia. Science 20: 739–741, 1982.
 111. Jiang, Z. G., M. A. Simmons, and N. J. Dun. Enkephalinergic modulation of non‐cholinergic transmission in mammalian prevertebral ganglia. Brain Res. 235: 185–191, 1982.
 112. Johnson, D. A., and G. Pilar. The release of acetylcholine from postganglionic cell bodies in response to depolarisation. J. Physiol. London 299: 605–620, 1980.
 113. Johnson, D. A., and D. Purves. Post‐natal reduction of neural unit size in the rabbit ciliary ganglion. J. Physiol. London 318: 143–159, 1981.
 114. Johnson, S. M., Y. Katayama, K. Morita, and R. A. North. Mediators of slow synaptic potentials in the myenteric plexus of the guinea‐pig ileum. J. Physiol. London 320: 175–186, 1981.
 115. Johnson, S. M., Y. Katayama, and R. A. North. Slow synaptic potentials in neurones of the myenteric plexus. J. Physiol. London 301: 505–516, 1980.
 116. Johnson, S. M., Y. Katayama, and R. A. North. Multiple actions of 5‐hydroxytryptamine on myenteric neurones of the guinea‐pig ileum. J. Physiol. London 304: 459–470, 1980.
 117. Kandel, E. R. Calcium and the control of synaptic strength by learning. Nature London 293: 697–700, 1981.
 118. Katayama, Y., and S. Nishi. The ionic mechanism of the late slow e.p.s.p. in amphibian sympathetic ganglion cells (Abstract). Proc. Int. Union Physiol. Sci. 13: 371, 1977.
 119. Katayama, Y., and S. Nishi. Voltage‐clamp analysis of peptidergic slow depolarizations in bullfrog sympathetic ganglion cells. J. Physiol. London 333: 305–314, 1982.
 120. Katayama, Y., R. A. North, and J. T. Williams. The action of substance P on neurones of the myenteric plexus of the guinea‐pig small intestine. Proc. R. Soc. London Ser. B 206: 191–208, 1979.
 121. Kato, K., and K. Kuba. Inhibition of transmitter release in bullfrog sympathetic ganglia induced by γ‐aminobutyric acid. J. Physiol. London 298: 271–284, 1980.
 122. Katz, B., and R. Miledi. The statistical nature of the acetylcholine potential and its molecular components. J. Physiol. London 224: 665–699, 1972.
 123. Kobayashi, H., and B. Libet. Generation of slow postsynaptic potentials without increase in ionic conductance. Proc. Natl. Acad. Sci. USA 60: 1304–1311, 1968.
 124. Kobayashi, H., and B. Libet. Actions of noradrenaline and acetylcholine on sympathetic ganglion cells. J. Physiol. London 208: 353–372, 1970.
 125. Kobayashi, H., and B. Libet. Is inactivation of potassium conductance involved in slow postsynaptic excitation of sympathetic ganglion cells? Effects of nicotine. Life Sci. 14: 1871–1883, 1974.
 126. Koelle, G. B. A proposed dual neurohumoral role of acetylcholine: its functions at the pre‐ and postsynaptic sites. Nature London 190: 208–211, 1961.
 127. Koketsu, K., T. Akasu, and M. Miyagawa. Identification of gK systems activated by [Ca2+]. Brain Res. 243: 369–372, 1982.
 128. Koketsu, K., and S. Nishi. Acetylcholine depolarization of bullfrog sympathetic preganglionic nerve terminals. Life Sci. 6: 1169–1177, 1967.
 129. Koketsu, K., and S. Nishi. Characteristics of the slow inhibitory postsynaptic potential of bullfrog ganglion cells. Life Sci. 6: 1827–1836, 1967.
 130. Koketsu, K., and S. Nishi. Cholinergic receptors at sympathetic preganglionic nerve terminals J. Physiol. London 196: 293–310, 1968.
 131. Koketsu, K., and M. Yamada. Presynaptic muscarinic receptors inhibiting active acetylcholine release in the bullfrog sympathetic ganglion. Br. J. Pharmacol. 77: 75–82, 1982.
 132. Konishi, S., M. Otsuka, K. Folkers, and S. Rosell. A substance P antagonist blocks non‐cholinergic slow excitatory postsynaptic potential in guinea‐pig sympathetic ganglia. Acta Physiol. Scand. 117: 157–160, 1983.
 133. Konishi, S., A. Tsunoo, and M. Otsuka. Enkephalins pre‐synaptically inhibit cholinergic transmission in sympathetic ganglia. Nature London 282: 515–516, 1979.
 134. Konishi, S., A. Tsunoo, and M. Otsuka. Substance P and noncholinergic excitatory synaptic transmission in guinea pig sympathetic ganglia. Proc. Jpn. Acad. B 55: 525–530, 1979.
 135. Konishi, S., A. Tsunoo, and M. Otsuka. Enkephalin as a transmitter for presynaptic inhibition in sympathetic ganglia. Nature London 294: 80–82, 1981.
 136. Kreulen, D. L., and J. H. Szurszewski. Nerve pathways in celiac plexus of the guinea pig. Am. J. Physiol. 237 (Endocrinol. Metab. 6): E90–E97, 1979.
 137. Kreulen, D. L., and J. H. Szurszewski. Reflex pathways in the abdominal prevertebral ganglia: evidence for a colocolonic inhibitory reflex. J. Physiol. London 295: 21–32, 1979.
 138. Krnjevic, K. Effects of substance P on central neurons in cats. In: Substance P, edited by U. S. von Euler and B. Pernow. New York: Raven, 1977, p. 217–230. (Nobel Symp. Ser., no. 37.)
 139. Kuba, K. Release of calcium ions linked to the activation of potassium conductance in a caffeine‐treated sympathetic neurone. J. Physiol. London 298: 251–269, 1980.
 140. Kuba, K., and K. Koketsu. Ionic mechanism of slow excitatory postsynaptic potential in bullfrog sympathetic ganglion cells. Brain Res. 81: 338–342, 1974.
 141. Kuba, K., and K. Koketsu. Analysis of slow excitatory postsynaptic potential in bullfrog sympathetic ganglion cells. Jpn. J. Physiol. 26: 647–664, 1976.
 142. Kuba, K., and K. Koketsu. Synaptic events in sympathetic ganglia. Prog. Neurobiol. 11: 77–169, 1978.
 143. Kuba, K., and S. Nishi. Membrane current associated with the fast EPSP of sympathetic neurons (Abstract). Physiologist 14: 176, 1971.
 144. Kuba, K., and S. Nishi. Characteristics of fast excitatory postsynaptic current in bullfrog sympathetic ganglion cells. Pfluegers Arch. 378: 205–212, 1979.
 145. Kuffler, S. W. Slow synaptic responses in autonomic ganglia and the pursuit of a peptidergic transmitter. J. Exp. Biol. 89: 257–286, 1980.
 146. Kuffler, S. W., and T. J. Sejnowski. Peptidergic and muscarinic excitation at amphibian sympathetic synapses. J. Physiol. London 341: 257–278, 1983.
 147. Kuffler, S. W., and D. Yoshikami. The number of transmitter molecules in a quantum: an estimate from iontophoretic application of acetylcholine at the neuromuscular synapse. J. Physiol. London 251: 465–482, 1975.
 148. Langer, S. Z. Presynaptic adrenoceptors and regulation of release. In: The Release of Catecholamines From Adrenergic Neurons, edited by D. M. Paton. New York: Pergamon, 1979, p. 59–85.
 149. Langley, J. N. The Autonomic Nervous System. Cambridge, UK: Heffer, 1921, pt. 1.
 150. Leander, S., R. Håkanson, S. Rosell, K. Folkers, F. Sundler, and K. Tornqvist. A specific substance P antagonist blocks smooth muscle contractions induced by non‐cholinergic, non‐adrenergic nerve stimulation. Nature London 294: 467–469, 1981.
 151. Lees, G. M., and D. I. Wallis. Hyperpolarization of rabbit superior cervical ganglion cells due to activity of an electrogenic sodium pump. Br. J. Pharmacol. 50: 79–93, 1974.
 152. Libet, B. Slow synaptic responses and excitatory changes in sympathetic ganglia. J. Physiol. London 174: 1–25, 1964.
 153. Libet, B. Long latent periods and further analysis of slow synaptic responses in sympathetic ganglia. J. Neurophysiol. 30: 494–514, 1967.
 154. Libet, B. Slow postsynaptic actions in ganglionic function. In: Integrative Functions of the Autonomic Nervous System, edited by C. McC. Brooks, K. Koizumi, and A. Sato. Amsterdam: Elsevier, 1979, p. 197–222.
 155. Libet, B. Longlasting modulation of slow excitatory postsynaptic potential (sEPSP) by catecholamines. Adv. Physiol. Sci. 4: 305–309, 1981.
 156. Libet, B., S. Chichibu, and T. Tosaka. Slow synaptic responses and excitability in sympathetic ganglia of the bullfrog. J. Neurophysiol. 31: 383–395, 1968.
 157. Libet, B., and H. Kobayashi. Adrenergic mediation of slów inhibitory postsynaptic potential in sympathetic ganglia of the frog. J. Neurophysiol. 37: 805–814, 1974.
 158. Lichtman, J. W. The reorganization of synaptic connexions in the rat submandibular ganglion during postnatal development. J. Physiol. London 273: 155–177, 1977.
 159. Lichtman, J. W. On the predominantly single innervation of submandibular ganglion cells in the rat. J. Physiol. London 302: 121–130, 1980.
 160. Lichtman, J. W., D. Purves, and J. W. Yip. On the purpose of selective innervation of guinea‐pig superior cervical ganglion cells. J. Physiol. London 292: 69–84, 1979.
 161. Livett, B. G., V. Kozousek, F. Mizobe, and D. M. Dean. Substance P inhibits nicotinic activation of chromaffin cells. Nature London 278: 256–257, 1979.
 162. Llewellyn‐Smith, I. J., J. B. Furness, and M. Costa. Ultrastructural localization of substance P‐like immunoreactivity in the myenteric ganglia of the guinea‐pig ileum. Neurosci. Lett. 8, Suppl.: S65, 1982.
 163. Llewellyn‐Smith, I. J., A. J. Wilson, J. B. Furness, M. Costa, and R. A. Rush. Ultrastructural identification of noradrenergic axons and their distribution within the enteric plexuses of the guinea‐pig small intestine. J. Neurocytol. 10: 331–352, 1981.
 164. Lundberg, J. M., A. Anggård, J. Fahrenkrug, T. Hökfelt, and V. Mutt. Vasoactive intestinal polypeptide in cholinergic neurons of exocrine glands: functional significance of coexisting transmitters for vasodilation and secretion. Proc. Natl. Acad. Sci. USA 77: 1651–1655, 1980.
 165. Lundberg, J. M., B. Hedlung, and T. Bartfai. Vasoactive intestinal polypeptide enhances muscarinic ligand binding in cat submandibular salivary gland. Nature London 295: 147–149, 1982.
 166. MacDermott, A. B., E. A. Connor, V. E. Dionne, and R. L. Parsons. Voltage clamp study of fast excitatory synaptic currents in bullfrog sympathetic ganglion cells. J. Gen. Physiol. 75: 39–60, 1980.
 167. MacDermott, A. B., and F. F. Weight. Action potential repolarization may involve a transient, Ca2+‐sensitive outward current in a vertebrate neurone. Nature London 300: 185–188, 1982.
 168. Marshall, L. M. Synaptic localization of α‐bungarotoxin binding which blocks nicotinic transmission at frog sympathetic neurons. Proc. Natl. Acad. Sci. USA 78: 1948–1952, 1981.
 169. Martin, A. R., and G. Pilar. Dual mode of synaptic transmission in the avian ciliary ganglion. J. Physiol. London 168: 443–463, 1963.
 170. Martin, A. R., and G. Pilar. Quantal components of the synaptic potential in the ciliary ganglion of the chick. J. Physiol. London 175: 1–16, 1964.
 171. Matthews, M. R., and A. C. Cuello. Substance P‐immunoreactive peripheral branches of sensory neurons innervate guinea pig sympathetic neurons. Proc. Natl. Acad. Sci. USA 79: 1668–1672, 1982.
 172. McCort, S. M., J. W. Nash, and F. F. Weight. Voltage clamp analysis of slow muscarinic excitation in sympathetic neurons of bullfrog. Soc. Neurosci. Abstr. 8: 501, 1982.
 173. McLachlan, E. M. An analysis of the release of acetylcholine during repetitive stimulation. J. Physiol. London 245: 447–466, 1975.
 174. McLachlan, E. M. The statistics of transmitter release at chemical synapses. In: Neurophysiology III, edited by R. Porter. Baltimore, MD: University Park, 1978, vol. 17, p. 49–117. (Int. Rev. Physiol. Ser.)
 175. McMahan, U. J., and S. W. Kuffler. Visual identification of synaptic boutons on living ganglion cells and of varicosities in postganglionic axons in the heart of the frog. Proc. R. Soc. London Ser. B 177: 485–508, 1971.
 176. McMahan, U. J., and D. Purves. Visual identification of two kinds of nerve cells and their synaptic contacts in a living autonomic ganglion of the mudpuppy (Necturus maculosus). J. Physiol. London 254: 405–425, 1976.
 177. Minota, S., N. J. Dun, and A. G. Karczmar. Substance P‐induced depolarization in sympathetic neurons: not simple K‐inactivation. Brain Res. 216: 224–228, 1981.
 178. Morita, K., and R. A. North. Clonidine activates membrane potassium conductance in myenteric neurones. Br. J. Pharmacol. 74: 419–428, 1981.
 179. Morita, K., and R. A. North. Opiates and enkephalin reduce the excitability of neuronal processes. Neuroscience 6: 1943–1951, 1981.
 180. Morita, K., and R. A. North. Opiate activation of potassium conductance in myenteric neurons: inhibition by calcium ion. Brain Res. 242: 145–150, 1982.
 181. Morita, K., R. A. North, and T. Tokimasa. The calcium‐activated potassium conductance in guinea‐pig myenteric neurones. J. Physiol. London 329: 341–354, 1982.
 182. Morita, K., R. A. North, and T. Tokimasa. Muscarinic agonists inactivate potassium conductance of guinea‐pig myenteric neurones. J. Physiol. London 333: 125–139, 1982.
 183. Morita, K., R. A. North, and T. Tokimasa. Muscarinic presynaptic inhibition of synaptic transmission in myenteric plexus of guinea‐pig ileum. J. Physiol. London 333: 141–149, 1982.
 184. Neild, T. O. Slowly‐developing depolarization of neurones in the guinea‐pig inferior mesenteric ganglion following repetitive stimulation of the preganglionic nerves. Brain Res. 140: 231–239, 1978.
 185. Nemeth, P. R., W. R. Ewart, and J. D. Wood. Actions of substance P analogs (D‐Pro2, D‐Phe7, D‐Trp9)‐substance P and (D‐Pro2, D‐Trp7,9) substance P in myenteric ganglia of guineapig small intestine. Soc. Neurosci. Abstr. 8: 285, 1982.
 186. Nishi, S. Cholinergic and adrenergic receptors at sympathetic preganglionic nerve terminals. Federation Proc. 29: 1957–1965, 1970.
 187. Nishi, S. Ganglionic transmission. In: The Peripheral Nervous System, edited by J. I. Hubbard. New York: Plenum, 1974, p. 225–256.
 188. Nishi, S., and Y. Katayama. The noncholinergic excitatory transmission in sympathetic ganglia. Adv. Physiol. Sci. 4: 323–327, 1981.
 189. Nishi, S., and K. Koketsu. Electrical properties and activities of single sympathetic neurons in frogs. J. Cell. Comp. Physiol. 55: 15–30, 1960.
 190. Nishi, S., and K. Koketsu. Early and late afterdischarges of amphibian sympathetic ganglion cells. J. Neurophysiol. 31: 109–121, 1968.
 191. Nishi, S., and R. A. North. Presynaptic action of noradrenaline in the myenteric plexus (Abstract). J. Physiol. London 231: 29P–30P, 1973.
 192. Nishi, S., and R. A. North. Intracellular recording from the myenteric plexus of the guinea‐pig ileum. J. Physiol. London 231: 471–491, 1973.
 193. Nishi, S., H. Soeda, and K. Koketsu. Studies on sympathetic B and C neurons and patterns of preganglionic innervation. J. Cell. Comp. Physiol. 66: 19–32, 1965.
 194. Nishi, S., H. Soeda, and K. Koketsu. Release of acetylcholine from sympathetic preganglionic nerve terminals. J. Neurophysiol. 30: 114–134, 1967.
 195. Nishi, S., H. Soeda, and K. Koketsu. Influence of membrane potential on the fast acetylcholine potential of sympathetic ganglion cells. Life Sci. 8: 499–505, 1969.
 196. Nja, A., and D. Purves. Specific innervation of guinea‐pig superior cervical ganglion cells by preganglionic fibres arising from different levels of the spinal cord. J. Physiol. London 264: 565–583, 1977.
 197. North, R. A. The calcium‐dependent slow after‐hyperpolarization in myenteric plexus neurones with tetrodotoxin‐resistant action potentials. Br. J. Pharmacol. 49: 709–711, 1973.
 198. North, R. A. Electrophysiology of the enteric nervous system. Neuroscience 7: 315–325, 1982.
 199. North, R. A., G. Henderson, Y. Katayama, and S. M. Johnson. Electrophysiological evidence for presynaptic inhibition of acetylcholine release by 5‐hydroxytryptamine in the enteric nervous system. Neuroscience 5: 581–586, 1980.
 200. North, R. A., Y. Katayama, and J. T. Williams. On the mechanism and site of action of enkephalin on single myenteric neurons. Brain Res. 165: 67–77, 1979.
 201. North, R. A., and S. Nishi. Properties of ganglion cells of the myenteric plexus of the guinea‐pig ileum determined by intracellular recording. In: Proceedings of the IVth International Symposium on Gastrointestinal Motility, edited by E. E. Daniel. Vancouver, Canada: Mitchell, 1974, p. 667–676.
 202. North, R. A., and A. Surprenant. Inhibitory synaptic potentials resulting from α2‐adrenoceptor activation in guineapig submucous plexus neurones. J. Physiol. London 358: 17–32, 1985.
 203. North, R. A., and T. Tokimasa. Muscarinic synaptic potentials in guinea‐pig myenteric plexus neurones. J. Physiol. London 333: 151–156, 1982.
 204. North, R. A., and T. Tokimasa. Depression of calcium‐dependent potassium conductance in guinea‐pig myenteric neurones by muscarinic agonists. J. Physiol. London 342: 253–266, 1983.
 205. North, R. A., and T. Tokimasa. The time course of muscarinic depolarization of myenteric neurones. Br. J. Pharmacol. 82: 85–92, 1984.
 206. Ostberg, A. J. C., G. Raisman, P. M. Field, L. L. Iversen, and R. E. Zigmond. A quantitative comparison of the formation of synapses in the rat superior cervical ganglion by its own and by foreign nerve fibers. Brain Res. 107: 445–470, 1976.
 207. Paton, W. D. M., and E. J. Zaimis. The pharmacological actions of polymethylene bistrimethylammonium salts. Br. J. Pharmacol. Chemother. 4: 381–400, 1949.
 208. Perri, V., O. Sacchi, and C. Casella. Electrical properties and synaptic connections of the sympathetic neurons in the rat and guinea‐pig superior cervical ganglion. Pfluegers Arch. 314: 40–54, 1970.
 209. Petersen, O. H. Electrophysiology of mammalian gland cells. Physiol. Rev. 56: 535–577, 1976.
 210. Petersen, O. H. The Electrophysiology of Gland Cells. London: Academic, 1980.
 211. Petersen, O. H. Electrophysiology of exocrine gland cells. In: Physiology of the Gastrointestinal Tract, edited by L. R. Johnson. New York: Raven, 1981, p. 749–772.
 212. Potter, D. D., S. C. Landis, and E. J. Furshpan. Dual function during development of rat sympathetic neurones in culture. J. Exp. Biol. 89: 57–71, 1980.
 213. Purves, D., and D. J. Wigston. Neural units in the superior cervical ganglion of the guinea‐pig. J. Physiol. London 334: 169–178, 1983.
 214. Rang, H. P. The characteristics of synaptic currents and responses to acetylcholine of rat submandibular ganglion cells. J. Physiol. London 311: 23–55, 1981.
 215. Rang, H. P. The action of ganglionic blocking drugs on the synaptic responses of rat submandibular ganglion cells. Br. J. Pharmacol 75: 151–168, 1982.
 216. Robson, L. E., and H. W. Kosterlitz. Specific protection of the binding sites of D‐Ala2‐D‐Leu5‐enkephalin (δ‐receptors) and dihydromorphine (μ‐receptors). Proc. R. Soc. London Ser. B 205: 425–432, 1979.
 217. Roper, S. An electrophysiological study of chemical and electrical synapses on neurones in the parasympathetic cardiac ganglion of the mudpuppy, Necturus maculosus: evidence for intrinsic ganglionic innervation J. Physiol. London 254: 427–454, 1976.
 218. Sacchi, O., and V. Perri. Quantal release of acetylcholine from the nerve endings of the guinea‐pig superior cervical ganglion. Pfluegers Arch. 329: 207–219, 1971.
 219. Schulman, J. A., and F. F. Weight. Synaptic transmission: long‐lasting potentiation by a postsynaptic mechanism. Science 194: 1437–1439, 1976.
 220. Selyanko, A. A., V. A. Derkach, and V. I. Skok. Fast excitatory postsynaptic currents in voltage‐clamped mammalian sympathetic ganglion neurones. J. Auton. Nerv. Syst. 1: 127–137, 1979.
 221. Siegelbaum, S. A., J. S. Camardo, and E. R. Kandel. Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurones. Nature London 299: 413–417, 1982.
 222. Siggins, G. R. Regulation of cellular excitability by cyclic nucleotides. In: Handbook of Experimental Pharmacology. Biochemistry of Cyclic Nucleotides, edited by J. A. Nathanson and J. W. Kebabian. Berlin: Springer‐Verlag, 1982, vol. 58, pt. 1, p. 305–316.
 223. Siggins, G. R., D. Gruol, A. Padjen, and D. Forman. Purine and pyrimidine mononucleotides depolarize neurones of explanted amphibian sympathetic ganglia. Nature London 270: 263–265, 1977.
 224. Skok, V. I. Physiology of Autonomic Ganglia. Tokyo: Igaku Shoin, 1973.
 225. Skok, V. I., A. A. Selyanko, and V. A. Derkach. Two modes of activity of nicotinic acetylcholine receptor channels in sympathetic neurons. Brain Res. 238: 480–483, 1982.
 226. Szurszewski, J. H. Physiology of mammalian prevertebral ganglia. Annu. Rev. Physiol. 43: 53–68, 1981.
 227. Takeuchi, A., and N. Takeuchi. On the permeability of end‐plate membrane during the action of transmitter. J. Physiol. London 154: 52–67, 1960.
 228. Tokimasa, T. Muscarinic agonists depress calcium dependent gK in bullfrog sympathetic neurones. J. Auton. Nerv. Syst. 10: 107–116, 1984.
 229. Tokimasa, T., E. Cherubini, and R. A. North. Nicotinic depolarization activates calcium dependent gK in myenteric neurones. Brain Res. 263: 57–62, 1983.
 230. Tokimasa, T., K. Morita, and R. A. North. Opiates and clonidine prolong calcium‐dependent after‐hyperpolarizations. Nature London 294: 162–163, 1981.
 231. Tokimasa, T., and R. A. North. Many transmitters, few channels: interactions between substance P and muscarinic action of acetylcholine on the membrane of enteric neurones. In: Coexistence of Neuroactive Substances, edited by S. L. Palay and V. Chan‐Palay. New York: Wiley, 1984, p. 217–224.
 232. Tosaka, T., S. Chichibu, and B. Libet. Intracellular analysis of slow inhibitory and excitatory postsynaptic potentials in sympathetic ganglia of the frog. J. Neurophysiol. 31: 396–409, 1968.
 233. Tsunoo, A., S. Konishi, and M. Otsuka. Substance P as an excitatory transmitter of primary afferent neurons in guineapig sympathetic ganglia. Neuroscience 7: 2025–2037, 1982.
 234. Vanhoutte, P. M., and M. N. Levy. Cholinergic inhibition of adrenergic neurotransmission in the cardiovascular system. In: Integrative Functions of the Autonomic Nervous System, edited by C. McC. Brooks, K. Koizumi, and A. Sato. Amsterdam: Elsevier, 1979, p. 159–176.
 235. Volle, R. L. Modification by drugs of synaptic mechanisms in autonomic ganglia. Pharmacol. Rev. 18: 839–869, 1966.
 236. Wallis, D. I., and R. A. North. Synaptic input to cells of the rabbit superior cervical ganglion. Pfluegers Arch. 374: 145–152, 1978.
 237. Weight, F. F. Synaptic mechanisms in amphibian sympathetic ganglia. In: Autonomic Ganglia, edited by L.‐G. Elfvin. New York: Wiley, 1983, p. 309–344.
 238. Weight, F. F., and A. Padjen. Slow synaptic inhibition: evidence for inactivation of sodium conductance in sympathetic ganglion cells. Brain Res. 55: 219–224, 1973.
 239. Weight, F. F., and A. Padjen. Acetylcholine and slow synaptic inhibition in frog sympathetic ganglion cells. Brain Res. 55: 225–228, 1973.
 240. Weight, F. F., and J. Votava. Slow synaptic excitation in sympathetic ganglion cells: evidence for synaptic inactivation of potassium conductance. Science 170: 775–758, 1970.
 241. Williams, J. T., Y. Katayama, and R. A. North. The actions of neurotensin on single myenteric neurones. Eur. J. Pharmacol. 59: 181–186, 1979.
 242. Winslow, J. P. Exposition Anatomique du Corps Humain. Paris: Deprez, 1732.
 243. Wood, J. D., and C. J. Mayer. Intracellular study of tonic‐type enteric neurons in guinea pig small intestine. J. Neurophysiol. 42: 569–581, 1979.
 244. Wood, J. D., and C. J. Mayer. Serotonergic activation of tonic‐type enteric neurons in guinea pig small bowel. J. Neurophysiol. 42: 582–593, 1979.
 245. Yoshimura, M., H. Higashi, and S. Nishi. Multiple innervation of amphibian sympathetic ganglion cells. Kurume Med. J. 26: 381–385, 1979.
 246. Zengel, J. E., K. L. Magleby, J. P. Horn, D. A. McAfee, and P. J. Yarowsky. Facilitation, augmentation, and potentiation of synaptic transmission at the superior cervical ganglion of the rabbit. J. Gen. Physiol. 76: 213–231, 1980.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Mechanisms of Autonomic Integration
 

How to Cite

R. A. North. Mechanisms of Autonomic Integration. Compr Physiol 2011, Supplement 4: Handbook of Physiology, The Nervous System, Intrinsic Regulatory Systems of the Brain: 115-153. First published in print 1986. doi: 10.1002/cphy.cp010402