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Physiology of prevertebral ganglia in mammals with special reference to inferior mesenteric ganglion

J. H. Szurszewski, B. F. King

10.1002/cphy.cp060115

Source: Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation

Originally published: 1989

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Neuroanatomy of Prevertebral Ganglia
1.1 General Descriptions
1.2 Components of Prevertebral Ganglia
2 Innervation of Prevertebral Ganglia
2.1 Spinal Preganglionic Neurons to Prevertebral Ganglion Cells
2.2 Visceral Afferent Fibers to Prevertebral Ganglion Cells
3 Electrophysiology of Prevertebral Ganglion Cells
3.1 Resting Membrane Potential
3.2 Neuromodulation of Resting Membrane Potential
3.3 Other Modulations of Resting Membrane Potential
3.4 Firing Patterns of Sympathetic Neurons
3.5 Modification of Firing Patterns
3.6 Afterspike Hyperpolarizations of Sympathetic Neurons
4 Synaptic Transmission in Prevertebral Ganglia
4.1 Fast Synaptic Transmission
4.2 Slow Synaptic Transmission
5 Neurotransmitters in Prevertebral Ganglia
5.1 Substance P
5.2 Enkephalins and Endorphin
5.3 Vasoactive Intestinal Polypeptide
5.4 Cholecystokinin
5.5 Dynorphin
5.6 Bombesin
5.7 Calcitonin Gene‐Related Peptide
5.8 Neurotensin
5.9 Serotonin
5.10 Vasopressin
5.11 Somatostatin and Neuropeptide Y
6 Summary
Figure 1. Figure 1.

Celiac superior and inferior mesenteric ganglia and associated structures in male guinea pig. Orad is at left and ventral is up.

From Kreulen and Szurszewski 325
Figure 2. Figure 2.

Pelvic‐hypogastric plexus. Principal ganglion cells are scattered throughout region where hypogastric and pelvic nerves intersect. HG.N., hypogastric nerve; S.V., seminal vesicles; V.D., vas deferens; P, prostate gland; C, coagulating gland; B, urinary bladder; pelv. N., pelvic nerves; L, lumbar root; and S, sacral nerve.
Figure 3. Figure 3.

Responses of principal ganglion cell of inferior mesenteric ganglion of guinea pig to increasing depolarizing current pulses applied through intracellular microelectrode. Note that successive increases in strength of depolarizing current pulse increased frequency of action potentials. In each panel, upper trace is membrane potential, bottom trace is current monitor.

From Crowcroft and Szurszewski 110
Figure 4. Figure 4.

Responses of presumed small intensely fluorescing (SIF) cells to depolarizing (A) and hyperpolarizing (B) current pulses applied through intracellular microelectrode and to orthodromic nerve stimulation (C‐F). Responses in A and B obtained from a presumed SIF cell located in a pelvic‐hypogastric ganglion of guinea pig. Note that depolarizing current >1 nA was needed to initiate action potentials. Top trace, membrane potential; bottom trace, current monitor. C, synaptic responses due to stimulation of left pelvic nerve 52 mm from recording site; it consists of three superimposed traces. D, recordings obtained from another presumed SIF cell in inferior mesenteric ganglion of guinea pig. Responses due to repetitive stimulation of intermesenteric nerve (20 Hz for 1 s). Responses are subthreshold EPSPs recorded at high gain. E, F, recordings obtained from two presumed SIF cells in inferior mesenteric ganglia of two guinea pigs. Response in E due to suprathreshold stimulation of intermesenteric nerve (40 Hz for 0.2 s) and response in F due to repetitive stimulation of lumbar colonic nerve (40 Hz for 0.2 s). Note that after single action potential (E) or burst of action potentials (F), membrane potential returned to base line without passing through after spike hyperpolarization. Resting membrane potential of these four cells ranged from −86 to −80 mV. Calibrations for recordings: C, 60 mV and 60 ms; D, 15 mV and 3 s; E, 60 mV and 30 ms; F, 80 mV and 0.86 s.

Recordings from J. H. Szurszewski and P. J. Crowcroft
Figure 5. Figure 5.

Response of satellite cell of inferior mesenteric ganglion of guinea pig to depolarizing current pulses applied through intracellular microelectrode (A) and to suprathreshold repetitive stimulation of lumbar colonic nerve (B). Note that this cell type is inexcitable to both forms of stimulation. Depolarization of membrane during repetitive nerve stimulation has been attributed to accumulation of K+ in extracellular spaces.

Recording from J. H. Szurszewski and P. J. Crowcroft
Figure 6. Figure 6.

Electron micrographs of two principal ganglion cells of pelvic‐hypogastric ganglion of guinea pig. Top panel, principal ganglion cell (GC), 25 μm diam, is surrounded by satellite cell containing large nucleus. Bottom panel, higher‐power electron micrograph of region of principal ganglion cell with tuftlike ganglion cell processes (GCP) and varicosities of axons.

Electron micrographs from J. H. Szurszewski and A. Ostberg
Figure 7. Figure 7.

High‐power electron micrograph of synapse of preganglionic axon with ganglion cell process of pelvic‐hypogastric ganglion of guinea pig. Varicosity of preganglionic axon contains agranular vesicles (AGV) and large granular vesicles (LGV).

Electron micrograph from J. H. Szurszewski, A. Ostberg, and P. J. Crowcroft
Figure 8. Figure 8.

Electron micrograph of small intensely fluorescing (SIF) cell of inferior mesenteric ganglion of guinea pig. Note numerous vesicles (1,000–1,600 Å diam), each containing large densely staining granule (400–900 Å diam). SIF cell enveloped by satellite cell (SC) with numerous mitochondria and large nucleus (N). This SIF cell is type I and is surrounded by portions of four other SIF cells.

Electron micrograph from J. H. Szurszewski, A. Ostberg, and P. J. Crowcroft
Figure 9. Figure 9.

Location of main nuclei of sympathetic preganglionic neurons of spinal cord of dog. IMLp, nucleus intermediolateralis pars principalis; IMLf, nucleus intermediolateralis pars funicularis; IML, nucleus intermediolateralis; IC, nucleus intercalatus spinalis; ICPe, nucleus intercalatus pars paraependymalis.

From Petras and Faden 483
Figure 10. Figure 10.

Location of four principal groups of sympathetic preganglionic neurons of lumbar segment of spinal cord of guinea pig. IMLp, nucleus intermediolateralis pars principalis; IMLf, nucleus intermediolateralis pars funicularis; IC, nucleus intercalatus spinalis; ICPe, nucleus intercalatus pars paraependymalis.
Figure 11. Figure 11.

Frequency histogram of conduction velocities of preganglionic fibers in different trunks attached to nerve inferior mesenteric ganglion of guinea pig.

Data from J. H. Szurszewski and P. J. Crowcroft
Figure 12. Figure 12.

Ongoing rhythmic discharge of action potentials recorded intracellularly from four neurons of four preparations of cat inferior mesenteric ganglia. In each record, note slow depolarization in membrane potential preceding each action potential. Frequency of action potentials: A, 0.6 Hz; B, 2.3 Hz; C, 3.2 Hz; D, 12.9 Hz.

From Julé and Szurszewski 281
Figure 13. Figure 13.

Relationship between endogenously active spinal sympathetic preganglionic neurons and endogenously active neurons located in inferior mesenteric ganglion of cat. CM, enteric cholinergic motoneuron; SN, sympathetic neuron; ˜, spontaneously active neuron.
Figure 14. Figure 14.

Excitatory synaptic activity in principal ganglion cell in inferior mesenteric ganglion of guinea pig before and after cutting lumbar colonic nerves that connected ganglion to segment of distal colon. After cutting lumbar colonic nerves, all synaptic input was abolished. Dot indicates moment of cutting nerve.

From Crowcroft et al. 109
Figure 15. Figure 15.

Effect of increasing colonic intraluminal pressure on excitatory synaptic input to principal ganglion cell in guinea pig inferior mesenteric ganglion. Intraluminal pressure was measured at both proximal (P) and distal (D) ends of colonic segment. In each panel, bottom trace is intracellularly recorded electrical activity from same cell during three different levels of maintained pressure: 2, 6, and 8 cmH2O. Each increase in basal pressure caused increase in incidence of excitatory synaptic input that was maintained as long as increase in pressure was maintained (longest duration, 1 h).

From Weems and Szurszewski 586. Copyright 1977. Reprinted with permission by the American Gastroenterological Association
Figure 16. Figure 16.

Effect of spontaneous increase in colonic intraluminal pressure on excitatory synaptic input to principal ganglion cell in guinea pig inferior mesenteric ganglion. Upper trace, intraluminal pressure measured from orad end of colonic segment. Lower trace, intracellularly recorded electrical activity. Note that spontaneous increase in basal intraluminal pressure caused increase in excitatory synaptic input and depolarization of cell membrane potential. Dashed line in lower trace represents apparent membrane potential before spontaneous change in pressure.

From Weems and Szurszewski 587
Figure 17. Figure 17.

Effect of superfusing colon only with tubocurarine on excitatory synaptic input to principal ganglion cell in guinea pig inferior mesenteric ganglion. Two‐compartment organ bath allowed for addition of antagonist to colon only. A, synaptic input when colonic segment was bathed in normal Krebs solution. B, synaptic input 5 min after adding tubocurarine to solution bathing colonic segment. C, effect of distending colonic segment with air when tubocurarine was still present in solution bathing segment of colon. Note that distension caused immediate increase in excitatory synaptic input during blockade of nicotinic receptors in colon wall. This suggests that population of mechanosensitive fibers project to inferior mesenteric ganglion without intervening nicotinic synapse. All recordings from same cell. Recording in C continuous with recording in B

From Szurszewski and Weems 550
Figure 18. Figure 18.

Neural connections between inferior mesenteric ganglion and colon of guinea pigs. Darkened enteric ganglionic cells represent peripheral, cholinergic afferent mechanosensory pathway. SN, sympathetic neuron; CM, enteric cholinergic motoneuron; MP, myenteric plexus.
Figure 19. Figure 19.

Examples of excitatory synaptic input to two different principal ganglion cells in right celiac ganglion (A and B) and to principal ganglion cell in superior mesenteric ganglion (C).

From Kreulen and Szurszewski 325
Figure 20. Figure 20.

Intracellular recording from principal ganglion cell in guinea pig superior mesenteric ganglion receiving excitatory synaptic input from attached segment of colon. In A, distension of colon caused immediate increase in synaptic input. In B, most of fibers running in lumbar colonic nerve were cut during maintained distension. Note sharp decrease in synaptic input. In C, all but one fiber running in lumbar colonic nerve were cut.

From Kreulen and Szurszewski 325
Figure 21. Figure 21.

Peripheral pathways mediating colocolonic inhibitory reflex. SN, sympathetic neuron; CM, enteric cholinergic motorneuron; MP, myenteric plexus. Darkened enteric ganglion cells represent afferent, cholinergic mechanosensory pathway. All unmarked synapses are excitatory.
Figure 22. Figure 22.

Peripheral pathways mediating gastroduodenal inhibitory reflex. SN, sympathetic neuron; CM, enteric cholinergic motoneuron; MP, myenteric plexus. Darkened enteric ganglion cell in gastric antrum represents cholinergic, mechanosensory pathway.
Figure 23. Figure 23.

Response of two principal ganglion cells to long‐lasting depolarization currents of different strength applied through intracellular microelectrode. A‐D, firing patterns of neuron on left exemplify responses of phasic firing neuron; E‐H, firing patterns on right exemplify responses of tonic firing neuron. Note that adapted firing frequency of various tonic discharges is maintained constant throughout period of depolarization. Note also that afterspike hyperpolarization in phasic firing cell is shorter than afterspike hyperpolarization in tonic firing cell.

From Weems and Szurszewski 587
Figure 24. Figure 24.

Frequency‐current relationship of three principal ganglion cells of inferior mesenteric ganglion of guinea pig. Adapted firing rate of spikes is plotted as function of strength of depolarizing currents applied through intracellular microelectrode. Each cell had afterspike hyperpolarization (ASH) of different duration. Durations of ASH for these three cells were 74 ms (•), 210 ms (○), and 310 ms (×). Note that neuron with longest duration ASH had lower frequency of firing at firing threshold than did neuron with shortest duration ASH. Also slope of frequency‐current relation was least for neuron with longest duration ASH.

From Weems and Szurszewski 587
Figure 25. Figure 25.

Antidromic and synaptic responses of principal ganglion cell in guinea pig inferior mesenteric ganglion evoked after stimulation of lumbar colonic nerves (A, C) and right hypogastric nerve (B). In top trace of A, two action potentials were produced by stimulation of lumbar colonic nerve. Hyperpolarization of cell due to injection of hyperpolarizing current through recording microelectrode (bottom trace of A) revealed subthreshold fast‐rise response followed by subthreshold synaptic response. Note that fast‐rise response decayed with time course similar to decay of electrotonic potential. Occurrence of fast‐rise response indicates that first action potential in top trace was antidromic. B, subthreshold, fast‐rise response recorded from another principal ganglion cell to stimulation of right hypogastric nerve. Dot marks location of stimulus artifact. C, sequence of responses of another cell to increase in strength of stimulation of lumbar colonic nerve; antidromic response was subthreshold (top trace), but synaptic responses superimposed upon it (middle and bottom traces) elicited action potentials. Dots mark location of stimulus artifact. A, B, C, uncorrected velocities of propagation of nerve fibers giving rise to antidromic responses were 0.9, 0.5, and 0.9 m/s, respectively, indicating conduction along C‐fibers.

Recordings from J. H. Szurszewski, B. F. King, and P. J. Crowcroft
Figure 26. Figure 26.

Intracellular recordings from principal ganglion cell in pelvic‐hypogastric ganglion of guinea pig, showing responses to orthodromic nerve stimulation before (A), during (B, C, D), and after (E, F) iontophoretic application of dihydro‐β‐erythroidine (DHβE). B, C, D were taken 10, 20, and 30 s, respectively, after onset of iontophoretic application of DHβE. E, F taken 4 min and 15 min, respectively, after stopping application of DHβE. Each record is three superimposed responses to single stimuli of hypogastric nerve (60 V, 0.5 ms, 0.7 Hz). Thin white line in each panel indicates level of resting membrane potential at start of experiment.

From Holman et al. 243
Figure 27. Figure 27.

Time course of fast excitatory postsynaptic potentials (EPSPs) in irregularly discharging neuron evoked by subthreshold stimulation of lumbar colonic nerve (LCN) and of fast EPSPs due to input from intrinsic, regularly discharging neuron in orad lobe of cat inferior mesenteric ganglion. A and B are continuous records.

From Julé and Szurszewski 281
Figure 28. Figure 28.

Responses of principal ganglion cell in guinea pig inferior mesenteric ganglion to increasing strength of stimulation of ascending mesenteric (intermesenteric) nerve (A‐J) and right hypogastric nerve (X‐Z). Each record consists of six successive responses to nerve stimulation of same current strength. Numbers at right of each trace indicate strength of stimulation in volts. Arrows in each trace indicate additional synaptic responses due to recruitment by higher stimulus strength of additional preganglionic fibers.

From Crowcroft and Szurszewski 110
Figure 29. Figure 29.

Responses of principal ganglion cell in guinea pig pelvichypogastric ganglion to increasing strength of stimulation of right hypogastric nerve (A) and right pelvic nerve (B). Responses at top of A and B were due to stimulus strength that was just threshold. Responses at bottom of A and B were due to maximum strength stimulus applied to each nerve. Threshold response to stimulation of both nerves was an action potential. Note that after second action potential in second trace of A, membrane potential remained depolarized for 54 ms before onset of afterhyperpolarization. Amount of transmitter released to trigger second action potential must have been considerably greater than that normally seen in inferior mesenteric ganglion. Such strong synaptic input is characteristic feature of synaptic inputs to pelvic‐hypogastric ganglia. Note also that third action potential in third trace of A is smaller in amplitude and has higher threshold, providing additional support for supposition that sustained depolarization after second action potential was due to continued transmitter action.

From Crowcroft and Szurszewski 110
Figure 30. Figure 30.

B‐E, response of principal ganglion cell in guinea pig inferior mesenteric ganglion to repetitive stimulation of intermesenteric nerve in normal Krebs solution and during exposure to dihydro‐β‐erythroidine (DHβE) (5 × 10−6 g/ml). A, note sequence of afterpotentials after repetitive stimulation (8 Hz, 1 s). Aftertrain hyperpolarization is immediately followed by slow depolarization that was 4 mV in amplitude and 3.3 s in duration. B, 2 min after nicotinic blockade, stimulation of intermesenteric nerve (8 Hz, 1 s) caused long‐lasting depolarization. C, D, effect of stimulation (30 Hz, 2 s) is shown at low and high amplification 2 and 4 min, respectively, after adding DHβE. E, 5 min after adding DHβE, slow depolarization after repetitive stimulation (30 Hz, 0.5 s) was prolonged and reached threshold for firing action potentials. Note that initiation of action potentials during slow depolarization is not normally seen in normal Krebs solution. In B‐E, single action preceding nerve stimulation was initiated by intracellular injection of suprathreshold depolarization to confirm cell's ability to generate action potential in face of nicotinic‐receptor blockade. Thin white line in C‐E indicates period of nerve stimulation. Although not shown, slow depolarization was blocked after addition of atropine (10−6 g/ml). Voltage calibration: A, B, D, 25 mV; C, E, 100 mV.

Data from J. H. Szurszewski and P. J. Crowcroft
Figure 31. Figure 31.

Response of principal ganglion cell in guinea pig celiac ganglion to repetitive stimulation of inferior celiac nerves (ICN) without (A) and with (B) an attached segment of colon. Note that following repetitive stimulation, there were two phases of afterpotentials: an aftertrain hyperpolarization that was immediately followed by a slow depolarization 8 mV in amplitude and lasted 22 s. B, note that in presence of ongoing excitatory synaptic input from colonic mechanoreceptors, some of fast excitatory postsynaptic potentials (EPSPs) reached threshold for firing action potential during slow depolarization. Recordings were made from two different cells in two different preparations of right celiac ganglion. Dashed line indicates level of membrane potential before nerve stimulation. Although not shown, slow depolarization was resistant to nicotinic and muscarinic receptor antagonists.

Recording from J. H. Szurszewski and D. L. Kreulen
Figure 32. Figure 32.

Response of principal ganglion cell in guinea pig inferior mesenteric ganglion to single and repetitive stimulation of lumbar colonic nerve. In A and B, top trace is intracellularly recorded potential without depolarizing current pulses, middle trace is with depolarizing current pulses, and bottom trace is current monitor. In C, bottom two traces are continuous with middle two traces. Before nerve stimulation, intracellularly injected depolarizing current pulses applied through microelectrode were subthreshold for initiation of action potential. Lumbar colonic nerve stimulated with single stimulus in A and stimulated repetitively in B (10 Hz, 1 s) and C (30 Hz, 1 s). Note that amplitude and duration of slow depolarization after afterspike hyperpolarization and aftertrain hyperpolarization were dependent on frequency of nerve stimulation. Note also that depolarizing current pulses that were subthreshold for initiation of action potential evoked action potential during slow depolarization. Increase in excitability and slow depolarization were associated with increase in membrane resistance. Numbers below C indicate minutes after repetitive nerve stimulation. (Note break in tracing in C.)

From Crowcroft and Szurszewski 110
Figure 33. Figure 33.

Effect of administration of capsaicin in vitro on noncholinergic slow excitatory postsynaptic potentials (EPSPs) in principal ganglion cell in guinea pig inferior mesenteric ganglion. In A, B, C, upper trace is response to supramaximal stimulation of both hypogastric nerves (20 Hz, 4 s, open triangles), and lower trace is response to distension of segment of distal colon (20 cmH2O for 65 s, between arrows). Note that in B, 10 min after adding capsaicin, the electrically evoked EPSP was abolished and distension‐induced slow depolarization was attenuated to 2.2 mV, compared with A, 11.2 mV in normal Krebs solution. C, responses obtained 10 min after washing out capsaicin.

From Kreulen and Peters 323
Figure 34. Figure 34.

Substance P pathway between lumbar spinal cord, inferior mesenteric ganglion, and distal colon of guinea pig. Note that of two substance P pathways shown, only central pathway is proposed as participating in substance P‐dependent transmission in inferior mesenteric ganglion. Substance P terminals located between circular and longitudinal muscle layers, as described by Aldskogius et al. 8, are presumed to function as mechanoreceptors and nociceptors. SP, substance P pathway; SN, sympathetic neuron; MP, myenteric plexus; B.V., blood vessel; CM, enteric cholinergic motoneuron. Darkened enteric ganglion cells represent peripheral, cholinergic afferent mechanosensory pathway. All unmarked synapses are excitatory.
Figure 35. Figure 35.

Effect of leucine‐enkephalin (Leu‐Enk) on cholinergic synaptic transmission in principal ganglion cell in inferior mesenteric ganglion of guinea pig. A, C, response to electrical stimulation of intermesenteric nerve in normal Krebs solution before (A) and after (C) washout of leucine‐enkephalin. B, recording made with leucine‐enkephalin present in bathing solution. Each panel consists of three superimposed successive responses to nerve stimulation.

From Shu et al. 527
Figure 36. Figure 36.

Effect of leucine‐enkephalin on afferent, colonic mechanosensory synaptic input to principal ganglion cell in guinea pig inferior mesenteric ganglion. In A, B, C, top trace is colonic intraluminal pressure and bottom trace is intracellular recorded electrical activity. In A, activity in normal Krebs solution; in B, 6 min after leucine‐enkephalin was added to solution perfusing only inferior mesenteric ganglion; in C, 3–5 min after washout of leucine‐enkephalin. Note that in presence of leucine‐enkephalin, there was significant reduction in total synaptic input from colon and there was increase in basal intraluminal pressure.

From Shu et al. 527
Figure 37. Figure 37.

Enkephalin pathway between spinal cord and inferior mesenteric ganglion of guinea pig. Note that terminals containing enkephalin‐like material end presynaptically on substance P collaterals and on terminals of cholinergic afferent mechanosensory fibers. For simplicity, enkephalin endings on other cholinergic preganglionic fibers have been left out. SP, substance P pathway, IMLf, nucleus intermediolateralis pars funcularis; IMLp, nucleus intermediolateralis pars principalis; ENK, enkephalin pathway; SN, sympathetic neuron; MP, myenteric plexus; B.V. blood vessel; CM, enteric cholinergic motoneuron. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.
Figure 38. Figure 38.

Effect of vasoactive intestinal peptide (VIP) antiserum of noncholinergic slow excitatory postsynaptic potential (EPSP) recorded from principal ganglion cell in guinea pig inferior mesenteric ganglion. Hexamethonium (2 × 10−4 M) and atropine (2 × 10−6 M) were present throughout to block nicotinic and muscarinic receptors, respectively. A, repetitive stimulation of lumbar colonic nerve (20 Hz, 4 s) evoked noncholinergic slow EPSP 4 mV in amplitude. B, nonimmune‐rabbit serum applied by pressure ejection for 2 min. Stimulation of lumbar colonic nerves evoked noncholinergic slow EPSP 4.5 mV in amplitude. C, amplitude of noncholinergic slow EPSP was reduced to 2 mV during pressure ejection of rabbit VIP antiserum. All recordings made from same cell.

From Love and Szurszewski 391
Figure 39. Figure 39.

Effect of vasoactive intestinal peptide (VIP) antiserum on slow depolarization evoked by distension of segment of distal colon of guinea pig. Intracellular recording obtained from principal ganglion cell in inferior mesenteric ganglion. Throughout experiment, hexamethonium (2 × 10−4 M) and atropine (2 × 10−6 M) were present in Krebs solution, bathing only inferior mesenteric ganglion. In A, B, C, upper trace is intracellular recording; bottom trace is intraluminal colonic pressure. In A, increase in pressure in segment of colon to 15 cmH2O caused 4 mV depolarization of neuron in ganglion. In B, pressure ejection of rabbit VIP antiserum onto neuron greatly reduced amplitude of distension‐induced membrane depolarization. Two minutes after ending application of VIP antiserum and after washout of antiserum, distension of colon evoked noncholinergic slow depolarization 5 mV in amplitude. All recordings made from same neuron.

From Love and Szurszewski 391
Figure 40. Figure 40.

Vasoactive intestinal polypeptide (VIP) pathway between prevertebral ganglia (celiac and superior and inferior mesenteric ganglion) and colon of guinea pig. Note that it is being suggested that mechanosensory fibers containing VIP‐like material end on NA/— and NA/SOM prevertebral neurons. The NA/— neurons in turn innervate motor apparatus of gut, whereas NA/SOM neurons innervate DYN/VIP neurons thought to regulate mucosal function 106,198,404. NA/NPY, noradrenergic neuron with neuropeptide Y immunoreactivity; NA/—, noradrenergic neuron that has not been demonstrated to contain a neuropeptide; NA/SOM, noradrenergic neuron with somatostatin immunoreactivity; MP, myenteric plexus; CM, enteric cholinergic motor neuron; DYN/VIP, enteric neuron in the submucous plexus containing dynorphin and VIP immunoreactivity. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.
Figure 41. Figure 41.

Response of principal ganglion cell in guinea pig inferior mesenteric ganglion to repetitive nerve stimulation before (A) and after (C) desensitization to nonsulfated cholecystokinin‐8 (CCK‐8). Nonsulfated CCK‐8 was applied by pressure ejection in B. Before desensitization to nonsulfated CCK‐8, noncholinergic slow excitatory postsynaptic potential (EPSP) was 6 mV in amplitude and lasted 63 s (A). After desensitization (C), EPSP was 2 mV and 19 s in duration.

From Schumann and Kreulen 519. Copyright 1986, with permission of the American Society for Pharmacology and Experimental Therapeutics
Figure 42. Figure 42.

Peripheral CCK pathway. SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motor neuron; CCK, cholecystokinin. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.
Figure 43. Figure 43.

Peripheral dynorphin and bombesin pathways. SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motor neuron; Bom, bombesin; DYN, dynorphin. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway.
Figure 44. Figure 44.

Calcitonin gene‐related peptides (CGRP) pathway and other related pathways. Note that CGRP is colocalized in substance P (SP) pathway. In contrast, peripheral substance P pathway does not contain CGRP‐like immunoreactivity. Enkephalin (ENK) pathway is shown to inhibit release of CGRP and substance P from collaterals present in inferior mesenteric ganglion. IMLf, nucleus intermediolaterals pars funicularis; IMLp, nucleus intermediolateralis pars principalis; SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motoneuron; B.V., blood vessel. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.
Figure 45. Figure 45.

Neurotensin pathway and other related pathways. Note that central neurotensin pathway acts presynaptically in inferior mesenteric ganglion to cause release of substance P (SP) and calcitonin gene‐related peptide (CGRP) and also postsynaptically on sympathetic neuron to cause direct excitation. IMLp, nucleus intermediolateralis pars principalis; NT, neurotensin; SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motoneuron; B.V., blood vessel. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.
Figure 46. Figure 46.

Pathways for acetylcholine and noradrenergic neurons running between distal colon, inferior mesenteric ganglion, and lumbar spinal cord of guinea pig. Note that for completeness, mechanosensory cholinergic neuron is shown projecting to inferior mesenteric ganglion without cholinergic input from other enteric neurons. All open‐symbol synapses are excitatory. SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motoneuron; L, lumbar spinal cord; IMLp, nucleus intermediolateralis pars principalis; IMLf, nucleus intermediolateralis pars funicularis; IC, nucleus intercalatus spinalis; ICP2, nucleus intercalatus spinalis pars paraependymalis.
Figure 47. Figure 47.

Peptidergic pathways between distal colon, inferior mesenteric ganglion, and lumbar spinal cord of guinea pig. Note specific locations for neurotensin (NT) and enkephalin (ENK) neurons. Cholinergic, mechanosensory afferent pathway (darkened neurons) is included because one site of action for enkephalin pathway is to inhibit release of acetylcholine from terminals of this pathway. Note also that peptidergic mechanosensory pathways utilizing vasoactive intestinal polypeptide (VIP), cholecystokinin (CCK), bombesin (BOM), and dynorphin (DYN) as neurotransmitters are shown as occurring within same neuron and also in subpopulation of mechanosensory neurons distinct from cholinergic mechanosensory pathway. MP, myenteric plexus; SP, substance P; CGRP, calcitonin gene‐related peptide; NA, norepinephrine neuron; SOM, somatostatin; ACh, acetylcholine; B.V., blood vessel.


Figure 1.

Celiac superior and inferior mesenteric ganglia and associated structures in male guinea pig. Orad is at left and ventral is up.

From Kreulen and Szurszewski 325


Figure 2.

Pelvic‐hypogastric plexus. Principal ganglion cells are scattered throughout region where hypogastric and pelvic nerves intersect. HG.N., hypogastric nerve; S.V., seminal vesicles; V.D., vas deferens; P, prostate gland; C, coagulating gland; B, urinary bladder; pelv. N., pelvic nerves; L, lumbar root; and S, sacral nerve.



Figure 3.

Responses of principal ganglion cell of inferior mesenteric ganglion of guinea pig to increasing depolarizing current pulses applied through intracellular microelectrode. Note that successive increases in strength of depolarizing current pulse increased frequency of action potentials. In each panel, upper trace is membrane potential, bottom trace is current monitor.

From Crowcroft and Szurszewski 110


Figure 4.

Responses of presumed small intensely fluorescing (SIF) cells to depolarizing (A) and hyperpolarizing (B) current pulses applied through intracellular microelectrode and to orthodromic nerve stimulation (C‐F). Responses in A and B obtained from a presumed SIF cell located in a pelvic‐hypogastric ganglion of guinea pig. Note that depolarizing current >1 nA was needed to initiate action potentials. Top trace, membrane potential; bottom trace, current monitor. C, synaptic responses due to stimulation of left pelvic nerve 52 mm from recording site; it consists of three superimposed traces. D, recordings obtained from another presumed SIF cell in inferior mesenteric ganglion of guinea pig. Responses due to repetitive stimulation of intermesenteric nerve (20 Hz for 1 s). Responses are subthreshold EPSPs recorded at high gain. E, F, recordings obtained from two presumed SIF cells in inferior mesenteric ganglia of two guinea pigs. Response in E due to suprathreshold stimulation of intermesenteric nerve (40 Hz for 0.2 s) and response in F due to repetitive stimulation of lumbar colonic nerve (40 Hz for 0.2 s). Note that after single action potential (E) or burst of action potentials (F), membrane potential returned to base line without passing through after spike hyperpolarization. Resting membrane potential of these four cells ranged from −86 to −80 mV. Calibrations for recordings: C, 60 mV and 60 ms; D, 15 mV and 3 s; E, 60 mV and 30 ms; F, 80 mV and 0.86 s.

Recordings from J. H. Szurszewski and P. J. Crowcroft


Figure 5.

Response of satellite cell of inferior mesenteric ganglion of guinea pig to depolarizing current pulses applied through intracellular microelectrode (A) and to suprathreshold repetitive stimulation of lumbar colonic nerve (B). Note that this cell type is inexcitable to both forms of stimulation. Depolarization of membrane during repetitive nerve stimulation has been attributed to accumulation of K+ in extracellular spaces.

Recording from J. H. Szurszewski and P. J. Crowcroft


Figure 6.

Electron micrographs of two principal ganglion cells of pelvic‐hypogastric ganglion of guinea pig. Top panel, principal ganglion cell (GC), 25 μm diam, is surrounded by satellite cell containing large nucleus. Bottom panel, higher‐power electron micrograph of region of principal ganglion cell with tuftlike ganglion cell processes (GCP) and varicosities of axons.

Electron micrographs from J. H. Szurszewski and A. Ostberg


Figure 7.

High‐power electron micrograph of synapse of preganglionic axon with ganglion cell process of pelvic‐hypogastric ganglion of guinea pig. Varicosity of preganglionic axon contains agranular vesicles (AGV) and large granular vesicles (LGV).

Electron micrograph from J. H. Szurszewski, A. Ostberg, and P. J. Crowcroft


Figure 8.

Electron micrograph of small intensely fluorescing (SIF) cell of inferior mesenteric ganglion of guinea pig. Note numerous vesicles (1,000–1,600 Å diam), each containing large densely staining granule (400–900 Å diam). SIF cell enveloped by satellite cell (SC) with numerous mitochondria and large nucleus (N). This SIF cell is type I and is surrounded by portions of four other SIF cells.

Electron micrograph from J. H. Szurszewski, A. Ostberg, and P. J. Crowcroft


Figure 9.

Location of main nuclei of sympathetic preganglionic neurons of spinal cord of dog. IMLp, nucleus intermediolateralis pars principalis; IMLf, nucleus intermediolateralis pars funicularis; IML, nucleus intermediolateralis; IC, nucleus intercalatus spinalis; ICPe, nucleus intercalatus pars paraependymalis.

From Petras and Faden 483


Figure 10.

Location of four principal groups of sympathetic preganglionic neurons of lumbar segment of spinal cord of guinea pig. IMLp, nucleus intermediolateralis pars principalis; IMLf, nucleus intermediolateralis pars funicularis; IC, nucleus intercalatus spinalis; ICPe, nucleus intercalatus pars paraependymalis.



Figure 11.

Frequency histogram of conduction velocities of preganglionic fibers in different trunks attached to nerve inferior mesenteric ganglion of guinea pig.

Data from J. H. Szurszewski and P. J. Crowcroft


Figure 12.

Ongoing rhythmic discharge of action potentials recorded intracellularly from four neurons of four preparations of cat inferior mesenteric ganglia. In each record, note slow depolarization in membrane potential preceding each action potential. Frequency of action potentials: A, 0.6 Hz; B, 2.3 Hz; C, 3.2 Hz; D, 12.9 Hz.

From Julé and Szurszewski 281


Figure 13.

Relationship between endogenously active spinal sympathetic preganglionic neurons and endogenously active neurons located in inferior mesenteric ganglion of cat. CM, enteric cholinergic motoneuron; SN, sympathetic neuron; ˜, spontaneously active neuron.



Figure 14.

Excitatory synaptic activity in principal ganglion cell in inferior mesenteric ganglion of guinea pig before and after cutting lumbar colonic nerves that connected ganglion to segment of distal colon. After cutting lumbar colonic nerves, all synaptic input was abolished. Dot indicates moment of cutting nerve.

From Crowcroft et al. 109


Figure 15.

Effect of increasing colonic intraluminal pressure on excitatory synaptic input to principal ganglion cell in guinea pig inferior mesenteric ganglion. Intraluminal pressure was measured at both proximal (P) and distal (D) ends of colonic segment. In each panel, bottom trace is intracellularly recorded electrical activity from same cell during three different levels of maintained pressure: 2, 6, and 8 cmH2O. Each increase in basal pressure caused increase in incidence of excitatory synaptic input that was maintained as long as increase in pressure was maintained (longest duration, 1 h).

From Weems and Szurszewski 586. Copyright 1977. Reprinted with permission by the American Gastroenterological Association


Figure 16.

Effect of spontaneous increase in colonic intraluminal pressure on excitatory synaptic input to principal ganglion cell in guinea pig inferior mesenteric ganglion. Upper trace, intraluminal pressure measured from orad end of colonic segment. Lower trace, intracellularly recorded electrical activity. Note that spontaneous increase in basal intraluminal pressure caused increase in excitatory synaptic input and depolarization of cell membrane potential. Dashed line in lower trace represents apparent membrane potential before spontaneous change in pressure.

From Weems and Szurszewski 587


Figure 17.

Effect of superfusing colon only with tubocurarine on excitatory synaptic input to principal ganglion cell in guinea pig inferior mesenteric ganglion. Two‐compartment organ bath allowed for addition of antagonist to colon only. A, synaptic input when colonic segment was bathed in normal Krebs solution. B, synaptic input 5 min after adding tubocurarine to solution bathing colonic segment. C, effect of distending colonic segment with air when tubocurarine was still present in solution bathing segment of colon. Note that distension caused immediate increase in excitatory synaptic input during blockade of nicotinic receptors in colon wall. This suggests that population of mechanosensitive fibers project to inferior mesenteric ganglion without intervening nicotinic synapse. All recordings from same cell. Recording in C continuous with recording in B

From Szurszewski and Weems 550


Figure 18.

Neural connections between inferior mesenteric ganglion and colon of guinea pigs. Darkened enteric ganglionic cells represent peripheral, cholinergic afferent mechanosensory pathway. SN, sympathetic neuron; CM, enteric cholinergic motoneuron; MP, myenteric plexus.



Figure 19.

Examples of excitatory synaptic input to two different principal ganglion cells in right celiac ganglion (A and B) and to principal ganglion cell in superior mesenteric ganglion (C).

From Kreulen and Szurszewski 325


Figure 20.

Intracellular recording from principal ganglion cell in guinea pig superior mesenteric ganglion receiving excitatory synaptic input from attached segment of colon. In A, distension of colon caused immediate increase in synaptic input. In B, most of fibers running in lumbar colonic nerve were cut during maintained distension. Note sharp decrease in synaptic input. In C, all but one fiber running in lumbar colonic nerve were cut.

From Kreulen and Szurszewski 325


Figure 21.

Peripheral pathways mediating colocolonic inhibitory reflex. SN, sympathetic neuron; CM, enteric cholinergic motorneuron; MP, myenteric plexus. Darkened enteric ganglion cells represent afferent, cholinergic mechanosensory pathway. All unmarked synapses are excitatory.



Figure 22.

Peripheral pathways mediating gastroduodenal inhibitory reflex. SN, sympathetic neuron; CM, enteric cholinergic motoneuron; MP, myenteric plexus. Darkened enteric ganglion cell in gastric antrum represents cholinergic, mechanosensory pathway.



Figure 23.

Response of two principal ganglion cells to long‐lasting depolarization currents of different strength applied through intracellular microelectrode. A‐D, firing patterns of neuron on left exemplify responses of phasic firing neuron; E‐H, firing patterns on right exemplify responses of tonic firing neuron. Note that adapted firing frequency of various tonic discharges is maintained constant throughout period of depolarization. Note also that afterspike hyperpolarization in phasic firing cell is shorter than afterspike hyperpolarization in tonic firing cell.

From Weems and Szurszewski 587


Figure 24.

Frequency‐current relationship of three principal ganglion cells of inferior mesenteric ganglion of guinea pig. Adapted firing rate of spikes is plotted as function of strength of depolarizing currents applied through intracellular microelectrode. Each cell had afterspike hyperpolarization (ASH) of different duration. Durations of ASH for these three cells were 74 ms (•), 210 ms (○), and 310 ms (×). Note that neuron with longest duration ASH had lower frequency of firing at firing threshold than did neuron with shortest duration ASH. Also slope of frequency‐current relation was least for neuron with longest duration ASH.

From Weems and Szurszewski 587


Figure 25.

Antidromic and synaptic responses of principal ganglion cell in guinea pig inferior mesenteric ganglion evoked after stimulation of lumbar colonic nerves (A, C) and right hypogastric nerve (B). In top trace of A, two action potentials were produced by stimulation of lumbar colonic nerve. Hyperpolarization of cell due to injection of hyperpolarizing current through recording microelectrode (bottom trace of A) revealed subthreshold fast‐rise response followed by subthreshold synaptic response. Note that fast‐rise response decayed with time course similar to decay of electrotonic potential. Occurrence of fast‐rise response indicates that first action potential in top trace was antidromic. B, subthreshold, fast‐rise response recorded from another principal ganglion cell to stimulation of right hypogastric nerve. Dot marks location of stimulus artifact. C, sequence of responses of another cell to increase in strength of stimulation of lumbar colonic nerve; antidromic response was subthreshold (top trace), but synaptic responses superimposed upon it (middle and bottom traces) elicited action potentials. Dots mark location of stimulus artifact. A, B, C, uncorrected velocities of propagation of nerve fibers giving rise to antidromic responses were 0.9, 0.5, and 0.9 m/s, respectively, indicating conduction along C‐fibers.

Recordings from J. H. Szurszewski, B. F. King, and P. J. Crowcroft


Figure 26.

Intracellular recordings from principal ganglion cell in pelvic‐hypogastric ganglion of guinea pig, showing responses to orthodromic nerve stimulation before (A), during (B, C, D), and after (E, F) iontophoretic application of dihydro‐β‐erythroidine (DHβE). B, C, D were taken 10, 20, and 30 s, respectively, after onset of iontophoretic application of DHβE. E, F taken 4 min and 15 min, respectively, after stopping application of DHβE. Each record is three superimposed responses to single stimuli of hypogastric nerve (60 V, 0.5 ms, 0.7 Hz). Thin white line in each panel indicates level of resting membrane potential at start of experiment.

From Holman et al. 243


Figure 27.

Time course of fast excitatory postsynaptic potentials (EPSPs) in irregularly discharging neuron evoked by subthreshold stimulation of lumbar colonic nerve (LCN) and of fast EPSPs due to input from intrinsic, regularly discharging neuron in orad lobe of cat inferior mesenteric ganglion. A and B are continuous records.

From Julé and Szurszewski 281


Figure 28.

Responses of principal ganglion cell in guinea pig inferior mesenteric ganglion to increasing strength of stimulation of ascending mesenteric (intermesenteric) nerve (A‐J) and right hypogastric nerve (X‐Z). Each record consists of six successive responses to nerve stimulation of same current strength. Numbers at right of each trace indicate strength of stimulation in volts. Arrows in each trace indicate additional synaptic responses due to recruitment by higher stimulus strength of additional preganglionic fibers.

From Crowcroft and Szurszewski 110


Figure 29.

Responses of principal ganglion cell in guinea pig pelvichypogastric ganglion to increasing strength of stimulation of right hypogastric nerve (A) and right pelvic nerve (B). Responses at top of A and B were due to stimulus strength that was just threshold. Responses at bottom of A and B were due to maximum strength stimulus applied to each nerve. Threshold response to stimulation of both nerves was an action potential. Note that after second action potential in second trace of A, membrane potential remained depolarized for 54 ms before onset of afterhyperpolarization. Amount of transmitter released to trigger second action potential must have been considerably greater than that normally seen in inferior mesenteric ganglion. Such strong synaptic input is characteristic feature of synaptic inputs to pelvic‐hypogastric ganglia. Note also that third action potential in third trace of A is smaller in amplitude and has higher threshold, providing additional support for supposition that sustained depolarization after second action potential was due to continued transmitter action.

From Crowcroft and Szurszewski 110


Figure 30.

B‐E, response of principal ganglion cell in guinea pig inferior mesenteric ganglion to repetitive stimulation of intermesenteric nerve in normal Krebs solution and during exposure to dihydro‐β‐erythroidine (DHβE) (5 × 10−6 g/ml). A, note sequence of afterpotentials after repetitive stimulation (8 Hz, 1 s). Aftertrain hyperpolarization is immediately followed by slow depolarization that was 4 mV in amplitude and 3.3 s in duration. B, 2 min after nicotinic blockade, stimulation of intermesenteric nerve (8 Hz, 1 s) caused long‐lasting depolarization. C, D, effect of stimulation (30 Hz, 2 s) is shown at low and high amplification 2 and 4 min, respectively, after adding DHβE. E, 5 min after adding DHβE, slow depolarization after repetitive stimulation (30 Hz, 0.5 s) was prolonged and reached threshold for firing action potentials. Note that initiation of action potentials during slow depolarization is not normally seen in normal Krebs solution. In B‐E, single action preceding nerve stimulation was initiated by intracellular injection of suprathreshold depolarization to confirm cell's ability to generate action potential in face of nicotinic‐receptor blockade. Thin white line in C‐E indicates period of nerve stimulation. Although not shown, slow depolarization was blocked after addition of atropine (10−6 g/ml). Voltage calibration: A, B, D, 25 mV; C, E, 100 mV.

Data from J. H. Szurszewski and P. J. Crowcroft


Figure 31.

Response of principal ganglion cell in guinea pig celiac ganglion to repetitive stimulation of inferior celiac nerves (ICN) without (A) and with (B) an attached segment of colon. Note that following repetitive stimulation, there were two phases of afterpotentials: an aftertrain hyperpolarization that was immediately followed by a slow depolarization 8 mV in amplitude and lasted 22 s. B, note that in presence of ongoing excitatory synaptic input from colonic mechanoreceptors, some of fast excitatory postsynaptic potentials (EPSPs) reached threshold for firing action potential during slow depolarization. Recordings were made from two different cells in two different preparations of right celiac ganglion. Dashed line indicates level of membrane potential before nerve stimulation. Although not shown, slow depolarization was resistant to nicotinic and muscarinic receptor antagonists.

Recording from J. H. Szurszewski and D. L. Kreulen


Figure 32.

Response of principal ganglion cell in guinea pig inferior mesenteric ganglion to single and repetitive stimulation of lumbar colonic nerve. In A and B, top trace is intracellularly recorded potential without depolarizing current pulses, middle trace is with depolarizing current pulses, and bottom trace is current monitor. In C, bottom two traces are continuous with middle two traces. Before nerve stimulation, intracellularly injected depolarizing current pulses applied through microelectrode were subthreshold for initiation of action potential. Lumbar colonic nerve stimulated with single stimulus in A and stimulated repetitively in B (10 Hz, 1 s) and C (30 Hz, 1 s). Note that amplitude and duration of slow depolarization after afterspike hyperpolarization and aftertrain hyperpolarization were dependent on frequency of nerve stimulation. Note also that depolarizing current pulses that were subthreshold for initiation of action potential evoked action potential during slow depolarization. Increase in excitability and slow depolarization were associated with increase in membrane resistance. Numbers below C indicate minutes after repetitive nerve stimulation. (Note break in tracing in C.)

From Crowcroft and Szurszewski 110


Figure 33.

Effect of administration of capsaicin in vitro on noncholinergic slow excitatory postsynaptic potentials (EPSPs) in principal ganglion cell in guinea pig inferior mesenteric ganglion. In A, B, C, upper trace is response to supramaximal stimulation of both hypogastric nerves (20 Hz, 4 s, open triangles), and lower trace is response to distension of segment of distal colon (20 cmH2O for 65 s, between arrows). Note that in B, 10 min after adding capsaicin, the electrically evoked EPSP was abolished and distension‐induced slow depolarization was attenuated to 2.2 mV, compared with A, 11.2 mV in normal Krebs solution. C, responses obtained 10 min after washing out capsaicin.

From Kreulen and Peters 323


Figure 34.

Substance P pathway between lumbar spinal cord, inferior mesenteric ganglion, and distal colon of guinea pig. Note that of two substance P pathways shown, only central pathway is proposed as participating in substance P‐dependent transmission in inferior mesenteric ganglion. Substance P terminals located between circular and longitudinal muscle layers, as described by Aldskogius et al. 8, are presumed to function as mechanoreceptors and nociceptors. SP, substance P pathway; SN, sympathetic neuron; MP, myenteric plexus; B.V., blood vessel; CM, enteric cholinergic motoneuron. Darkened enteric ganglion cells represent peripheral, cholinergic afferent mechanosensory pathway. All unmarked synapses are excitatory.



Figure 35.

Effect of leucine‐enkephalin (Leu‐Enk) on cholinergic synaptic transmission in principal ganglion cell in inferior mesenteric ganglion of guinea pig. A, C, response to electrical stimulation of intermesenteric nerve in normal Krebs solution before (A) and after (C) washout of leucine‐enkephalin. B, recording made with leucine‐enkephalin present in bathing solution. Each panel consists of three superimposed successive responses to nerve stimulation.

From Shu et al. 527


Figure 36.

Effect of leucine‐enkephalin on afferent, colonic mechanosensory synaptic input to principal ganglion cell in guinea pig inferior mesenteric ganglion. In A, B, C, top trace is colonic intraluminal pressure and bottom trace is intracellular recorded electrical activity. In A, activity in normal Krebs solution; in B, 6 min after leucine‐enkephalin was added to solution perfusing only inferior mesenteric ganglion; in C, 3–5 min after washout of leucine‐enkephalin. Note that in presence of leucine‐enkephalin, there was significant reduction in total synaptic input from colon and there was increase in basal intraluminal pressure.

From Shu et al. 527


Figure 37.

Enkephalin pathway between spinal cord and inferior mesenteric ganglion of guinea pig. Note that terminals containing enkephalin‐like material end presynaptically on substance P collaterals and on terminals of cholinergic afferent mechanosensory fibers. For simplicity, enkephalin endings on other cholinergic preganglionic fibers have been left out. SP, substance P pathway, IMLf, nucleus intermediolateralis pars funcularis; IMLp, nucleus intermediolateralis pars principalis; ENK, enkephalin pathway; SN, sympathetic neuron; MP, myenteric plexus; B.V. blood vessel; CM, enteric cholinergic motoneuron. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.



Figure 38.

Effect of vasoactive intestinal peptide (VIP) antiserum of noncholinergic slow excitatory postsynaptic potential (EPSP) recorded from principal ganglion cell in guinea pig inferior mesenteric ganglion. Hexamethonium (2 × 10−4 M) and atropine (2 × 10−6 M) were present throughout to block nicotinic and muscarinic receptors, respectively. A, repetitive stimulation of lumbar colonic nerve (20 Hz, 4 s) evoked noncholinergic slow EPSP 4 mV in amplitude. B, nonimmune‐rabbit serum applied by pressure ejection for 2 min. Stimulation of lumbar colonic nerves evoked noncholinergic slow EPSP 4.5 mV in amplitude. C, amplitude of noncholinergic slow EPSP was reduced to 2 mV during pressure ejection of rabbit VIP antiserum. All recordings made from same cell.

From Love and Szurszewski 391


Figure 39.

Effect of vasoactive intestinal peptide (VIP) antiserum on slow depolarization evoked by distension of segment of distal colon of guinea pig. Intracellular recording obtained from principal ganglion cell in inferior mesenteric ganglion. Throughout experiment, hexamethonium (2 × 10−4 M) and atropine (2 × 10−6 M) were present in Krebs solution, bathing only inferior mesenteric ganglion. In A, B, C, upper trace is intracellular recording; bottom trace is intraluminal colonic pressure. In A, increase in pressure in segment of colon to 15 cmH2O caused 4 mV depolarization of neuron in ganglion. In B, pressure ejection of rabbit VIP antiserum onto neuron greatly reduced amplitude of distension‐induced membrane depolarization. Two minutes after ending application of VIP antiserum and after washout of antiserum, distension of colon evoked noncholinergic slow depolarization 5 mV in amplitude. All recordings made from same neuron.

From Love and Szurszewski 391


Figure 40.

Vasoactive intestinal polypeptide (VIP) pathway between prevertebral ganglia (celiac and superior and inferior mesenteric ganglion) and colon of guinea pig. Note that it is being suggested that mechanosensory fibers containing VIP‐like material end on NA/— and NA/SOM prevertebral neurons. The NA/— neurons in turn innervate motor apparatus of gut, whereas NA/SOM neurons innervate DYN/VIP neurons thought to regulate mucosal function 106,198,404. NA/NPY, noradrenergic neuron with neuropeptide Y immunoreactivity; NA/—, noradrenergic neuron that has not been demonstrated to contain a neuropeptide; NA/SOM, noradrenergic neuron with somatostatin immunoreactivity; MP, myenteric plexus; CM, enteric cholinergic motor neuron; DYN/VIP, enteric neuron in the submucous plexus containing dynorphin and VIP immunoreactivity. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.



Figure 41.

Response of principal ganglion cell in guinea pig inferior mesenteric ganglion to repetitive nerve stimulation before (A) and after (C) desensitization to nonsulfated cholecystokinin‐8 (CCK‐8). Nonsulfated CCK‐8 was applied by pressure ejection in B. Before desensitization to nonsulfated CCK‐8, noncholinergic slow excitatory postsynaptic potential (EPSP) was 6 mV in amplitude and lasted 63 s (A). After desensitization (C), EPSP was 2 mV and 19 s in duration.

From Schumann and Kreulen 519. Copyright 1986, with permission of the American Society for Pharmacology and Experimental Therapeutics


Figure 42.

Peripheral CCK pathway. SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motor neuron; CCK, cholecystokinin. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.



Figure 43.

Peripheral dynorphin and bombesin pathways. SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motor neuron; Bom, bombesin; DYN, dynorphin. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway.



Figure 44.

Calcitonin gene‐related peptides (CGRP) pathway and other related pathways. Note that CGRP is colocalized in substance P (SP) pathway. In contrast, peripheral substance P pathway does not contain CGRP‐like immunoreactivity. Enkephalin (ENK) pathway is shown to inhibit release of CGRP and substance P from collaterals present in inferior mesenteric ganglion. IMLf, nucleus intermediolaterals pars funicularis; IMLp, nucleus intermediolateralis pars principalis; SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motoneuron; B.V., blood vessel. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.



Figure 45.

Neurotensin pathway and other related pathways. Note that central neurotensin pathway acts presynaptically in inferior mesenteric ganglion to cause release of substance P (SP) and calcitonin gene‐related peptide (CGRP) and also postsynaptically on sympathetic neuron to cause direct excitation. IMLp, nucleus intermediolateralis pars principalis; NT, neurotensin; SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motoneuron; B.V., blood vessel. Darkened enteric ganglion cells represent peripheral, cholinergic afferent pathway. All unmarked synapses are excitatory.



Figure 46.

Pathways for acetylcholine and noradrenergic neurons running between distal colon, inferior mesenteric ganglion, and lumbar spinal cord of guinea pig. Note that for completeness, mechanosensory cholinergic neuron is shown projecting to inferior mesenteric ganglion without cholinergic input from other enteric neurons. All open‐symbol synapses are excitatory. SN, sympathetic neuron; MP, myenteric plexus; CM, enteric cholinergic motoneuron; L, lumbar spinal cord; IMLp, nucleus intermediolateralis pars principalis; IMLf, nucleus intermediolateralis pars funicularis; IC, nucleus intercalatus spinalis; ICP2, nucleus intercalatus spinalis pars paraependymalis.



Figure 47.

Peptidergic pathways between distal colon, inferior mesenteric ganglion, and lumbar spinal cord of guinea pig. Note specific locations for neurotensin (NT) and enkephalin (ENK) neurons. Cholinergic, mechanosensory afferent pathway (darkened neurons) is included because one site of action for enkephalin pathway is to inhibit release of acetylcholine from terminals of this pathway. Note also that peptidergic mechanosensory pathways utilizing vasoactive intestinal polypeptide (VIP), cholecystokinin (CCK), bombesin (BOM), and dynorphin (DYN) as neurotransmitters are shown as occurring within same neuron and also in subpopulation of mechanosensory neurons distinct from cholinergic mechanosensory pathway. MP, myenteric plexus; SP, substance P; CGRP, calcitonin gene‐related peptide; NA, norepinephrine neuron; SOM, somatostatin; ACh, acetylcholine; B.V., blood vessel.

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Article Title: Physiology of prevertebral ganglia in mammals with special reference to inferior mesenteric ganglion
 

How to Cite

J. H. Szurszewski, B. F. King. Physiology of prevertebral ganglia in mammals with special reference to inferior mesenteric ganglion. Compr Physiol 2011, Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation: 519-592. First published in print 1989. doi: 10.1002/cphy.cp060115