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Electrical and synaptic behavior of enteric neurons

Jackie D. Wood

10.1002/cphy.cp060114

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 Methods
1.1 Extracellular Recording
1.2 Intracellular Recording
1.3 Dissections
2 Extracellularly Recorded Electrical Activity
2.1 Classification of Units
2.2 Burst‐Type Units
2.3 Mechanosensitive Neurons
2.4 Single‐Spike Units
3 Intracellularly Recorded Electrical Activity
3.1 Histoanatomical Factors
3.2 Electrical Behavior of Neuronal Processes
4 Introduction to Electrical and Synaptic Behavior
4.1 Electrophysiological Classification
4.2 Electrical Behavior of Cell Bodies
5 Chemical Neurotransmission
5.1 Fast EPSPs
5.2 Slow EPSPs
5.3 Fast IPSPs
5.4 Slow IPSPs
5.5 Presynaptic Inhibition
5.6 Mechanisms and Significance
6 Denervation Effects
Figure 1. Figure 1.

Discharge of 4 different units detected by a single extracellular microelectrode in myenteric ganglion of cat small intestine.

From Wood and Mayer 224
Figure 2. Figure 2.

Electrical current flow in bathing solution surrounding a neuron during occurrence of an action potential. Membrane is depolarized at site of spike generation (C). Outward current flows from points A and B and becomes inward current in the depolarized region, resulting in electrical fields illustrated by arrows and solid lines. Size and polarity of a potential recorded between an electrode placed near the neuron and ground potential is determined by density and direction of flow of current in the fields. Dashed lines, isopotential points in electrical fields. If electrode tip is to the left or right of the isopotential lines near points A or B, recorded potential is positive. If electrode tip is between isopotential lines near point C, polarity is negative. If the action potential propagates under an electrode, the electrode first detects the outward current, then the inward current at the depolarization site, and again an outward current. This results in a triphasic waveform resembling the spike shown in Figure 3C.
Figure 3. Figure 3.

Extracellularly and intracellularly recorded action potentials in myenteric neurons. A: extracellularly recorded biphasic spike characteristic of a somal or nonpropagated action potential. B: extracellularly recorded triphasic spike characteristic of a propagated action potential. C: extracellularly recorded spike with complex waveform characteristic of composite action potentials produced by sequential firing of initial segment and soma of a neuron. D: intracellularly recorded action potential evoked by electrical‐field stimulation (arrow, stimulus artifact). Upper trace, transmembrane voltage; lower trace, first time derivative (dV/dT) of voltage change. The dV/dT simulates extracellularly recorded biphasic potential in A. E: electrotonic spike from initial segment (arrow) triggered a somal spike. The dV/dT of transmembrane voltage simulates extracellularly recorded complex spike in C. Vertical calibration, 15 μV for A; 10 μV for B; 20 μV for C; 20 mV or 60 V/s for D and E. Horizontal calibration, ∼2 ms for A, D, and E; 1 ms for B; 5 ms for C.
Figure 4. Figure 4.

Bridge circuit used to pass electrical current across membrane of a neuron. Single microelectrode is used to inject current into the cell soma and to record resulting electrotonic potential across the membrane. Bridge circuit functions to remove the voltage drop that occurs across the resistance of the microelectrode during current injection. This is accomplished by a differential amplifier that subtracts a voltage proportional to the injected current from the total potential change recorded from the electrode. Thus only the potential due to current flow across the resistance and capacitance of the membrane is recorded.
Figure 5. Figure 5.

Structural relations of intestinal wall showing layers that must be removed to expose myenteric or submucosal plexus for electrical recording.

From Wood 223a). In: Physiology of the Gastrointestinal Tract, © 1987, Raven Press, New York
Figure 6. Figure 6.

Photomicrograph of longitudinal muscle‐myenteric plexus preparation of guinea pig duodenum as viewed with Nomarski optics for electrical recording
Figure 7. Figure 7.

Discharge of burst‐type unit in myenteric plexus of cat small intestine. A: burst pattern recorded with a slow time base. B: single burst of spikes from same neuron recorded with an expanded time base. C: nonsequential spike interval histogram. Ordinate, number of intervals. Abscissa, interval duration in milliseconds. Recorded with extracellular micropipette filled with 1 M NaCl. Vertical calibration, 50 μV. Horizontal calibration, 5 s in A; 0.5 s in B.
Figure 8. Figure 8.

Histogram of interval distribution of consecutive spikes within bursts of an erratic burst‐type unit in myenteric plexus of cat small intestine. Ordinate, duration of sequential interspike intervals given on abscissa. N, number of intervals; vertical bars, standard deviation. Coefficient of variation (standard deviation/mean) is inserted above each interval.

From Wood and Mayer 224
Figure 9. Figure 9.

Histograms of interburst intervals of consecutive bursts of spikes recorded extracellularly from 2 steady burst‐type myenteric neurons in cat small intestine. N, number of intervals; X, mean interval duration.

From Wood and Mayer 224
Figure 10. Figure 10.

Sequential variation of interburst intervals for an erratic burster recorded extracellularly from myenteric plexus of guinea pig small intestine. Ordinate, time interval between 1st spike of sequential bursts. Abscissa, 575 consecutive interburst intervals that occurred over a time span of 23 min. Ordinate values of 0, periodic conversion from burst discharge to continous discharge of single spikes or doublets. Long‐duration interburst interval after each episode of continuous discharge.

From Wood 217
Figure 11. Figure 11.

Characteristics of discharge of an erratic burst‐type unit recorded extracellularly in myenteric plexus of guinea pig small intestine. Note conversion from burst pattern of discharge to pattern of continuous discharge and reversion to burst pattern (cf. Fig. 10). Record is continuous from top to bottom trace. Recorded with glass‐insulated Pt wire electrode with 20‐μm‐diam tip.

From Wood 217
Figure 12. Figure 12.

Dogiel morphological classification of enteric ganglion cells.

From Dogiel 45
Figure 13. Figure 13.

Interactions between burst units. A: coupling between “driver‐follower” discharge of burst‐type units in myenteric plexus of cat small intestine. Inset, record of coupling of discharge of 2 different neurons. Interspike‐interval histogram for same neurons has 2 peaks corresponding to different frequency of spike discharge of 2 units. Ordinate, number of intervals; abscissa, interval duration in milliseconds. Computer bin width 0.5 ms. B: inhibition of burst‐type discharge by activity of a 2nd neuron in myenteric plexus of cat small intestine. 1, Single burst of spikes with no inhibitory discharge of 2nd unit. 2, Same burst unit with reduced frequency of discharge associated with preceding discharge of 2nd neuron. 3, Discharge of 2nd unit occurred after 1st spike of burst and was coincident with suppression of discharge of burst unit. 4, Occurrence of inhibitory discharge after 2nd spike of burst. 5, Occurrence of inhibitory discharge after 4th spike of burst. 6, Occurrence of inhibitory discharge after 6th spike of burst. Recorded with stainless steel needle electrode.

From Wood and Mayer 225
Figure 14. Figure 14.

Discharge of slowly adapting mechanoreceptor in myenteric plexus of dog small intestine. Unit did not discharge spontaneously but responded to mechanical stimulation (horizontal bars). A: responses to mechanical stimulation in absence of drugs. Mechanical stimulation was transient forward‐reverse movement of glass‐insulated Pt wire electrode over ∼20 μm. B: response to sustained stimulus in presence of 5‐HT. C: responses to transient stimulation in presence of 5‐HT. Second response with higher discharge frequency was produced by stimulus of greater intensity. D: progressive increase in discharge frequency evoked by progressive advancement of electrode in presence of 5‐HT. E: response of same cell to transient stimulation after washout of 5‐HT and in presence of norepinephrine.

From Wood and Mayer 225
Figure 15. Figure 15.

Relation of interspike interval to intensity of stimulation for a slowly adapting mechanoreceptor in myenteric plexus of cat small intestine. Ordinate, mean interspike interval; abscissa, distance of electrode displacement.

From Wood and Mayer 226
Figure 16. Figure 16.

Discharge of slowly adapting mechanoreceptor in myenteric plexus coincident with contractile activity of small intestinal muscularis externa in cat. Upper traces in each record are from an indium‐filled glass pipette microelectrode that was pushed through longitudinal muscle into myenteric plexus. Lower traces, electrical activity of musculature recorded with a suction electrode placed in the vicinity of the microelectrode. A: electrical activity of musculature consisted of electrical slow waves with spikes at crests of some slow waves. This activity was detected by the microelectrode in the myenteric plexus, but no nervous discharge is apparent on upper trace. B: after small change in position of microelectrode, nerve spikes appear on upper trace. C: neuronal spike frequency increased after occurrence of muscle spikes on slow waves and associated contractile activity of the muscle
Figure 17. Figure 17.

Structure of myenteric neurons that send projections to central nervous system. Somas of ganglion cells were labeled by horseradish peroxidase that was transported antidromically from a placement site on intestinal mesentery.

Courtesy of E. Fehér
Figure 18. Figure 18.

Discharge pattern of tonic‐type myenteric unit in cat small intestine. A: discharge of a train of spikes in response to mechanical stimulation. Mechanical stimulation was a transient forward‐reverse movement of a glass‐insulated Pt wire electrode with 20‐μm‐diam tip. B: relation between frequency of discharge of tonic‐type neurons of cat small intestinal myenteric plexus and 1‐s intervals after initiation of discharge. Four different units are represented.

From Wood and Mayer 226
Figure 19. Figure 19.

Interaction between discharge of a slowly adapting mechanosensitive unit and a unit that discharges trains of spikes. Small‐amplitude spikes on each record are from mechanosensitive unit. Discharge of mechanosensitive unit preceded large‐amplitude single spikes in top trace and trains of spikes in middle trace. Discharge of mechanoreceptor could not be detected during trainlike discharge of middle trace but resumed on bottom trace. Records were made with a glass‐insulated Pt wire electrode and are continuous.

From Wood 217
Figure 20. Figure 20.

Interconversion between tonic‐type and burst‐type discharge in small intestinal myenteric plexus of cat. A: discharge of spike train in response to mechanical stimulation (horizontal bar) followed by conversion to burst‐type discharge. Mechanical stimulation was a transient forward‐reverse movement of glass‐insulated PT wire electrode. Upper 3 traces, continuous records. Fourth trace, continuous with 3rd trace and shows consecutive bursts of spikes with times between consecutive bursts given in seconds. B: waveform of action potential of trainlike discharge. C: waveform of action potential of burst‐type discharge.

From Wood and Mayer 226
Figure 21. Figure 21.

Extracellular recording of discharge of single‐spike unit in myenteric plexus of cat small intestine. A: ongoing discharge in Tyrode's solution. B: elevation of Mg2+ to 10.2 mM in the solution did not affect discharge of the unit. C: nicotine (1 μM) excited the single‐spike unit. D: spike‐interval histogram computed for discharge shown in A. E: spike‐interval histogram computed in presence of elevated Mg2+. Ordinate, number of intervals. Abscissa, interval duration in milliseconds. Computer bin width 1 ms.

From Wood 223a). In: Physiology of the Gastrointestinal Tract, © 1987, Raven Press, New York
Figure 22. Figure 22.

Three kinds of intracellularly recorded electrical changes in myenteric neuron of guinea pig small intestine. Electrical stimulation of interganglionic fiber activated both a neurite extending from the neuron and an axon that formed a nicotinic synapse with the cell. Arrows: fast EPSP, electrotonic spike invading somal membrane, and somal spike triggered by electrotonic spike from the neurite.
Figure 23. Figure 23.

Refractory period of soma and neurites of myenteric neurons in guinea pig small intestine recorded intracellularly. Twin extracellular stimulus pulses were applied to surface of ganglia. Time interval between twin pulses was progressively shortened, until first the somal spikes and then the electrotonic invasions were not elicited by the second pulses. A: superimposed traces, refractory period for the somal spike was longer than for the spike conducted in the neurite. B: in another ganglion cell the refractory period for the somal spike was prolonged in association with a longer hyper‐polarizing afterpotential. Distance between stimulating and recording electrode for A was 80 μM and for B 110 μM. Stimulus pulse duration, 100 μs. (From 228
Figure 24. Figure 24.

Differential excitability between cell soma and 1 of its neurites in myenteric neuron of guinea pig small intestine. A: intrasomatic injection of depolarizing current pulse fired the soma and the neurite; however, the neurite fired more often (low‐amplitude electrotonic potentials) than the soma, indicating that the neurite membrane was more excitable than the soma. B: spontaneous occurrence of spikes in the neurite in the absence of spontaneous somal spikes in the same cell also suggests differential excitability.

Adapted from Wood 223a)
Figure 25. Figure 25.

Spontaneous spike discharge spreading electrotonically from the neurite into the soma of guinea pig myenteric neuron. Intracellularly recorded bursts of spikes in the neurite are similar to erratic burst‐type discharge of extracellular studies. A: continuous record of spikes in neurites and an occasional somal spike triggered by electrotonic current from the neurite spike. B: continuous record of decrease in interburst interval and conversion from bursts to trains of activity. C: prolonged silent period of cyclical discharge pattern of the neurite.

From Wood and Mayer 228
Figure 26. Figure 26.

Resting potential of enteric neurons is a K+ equilibrium potential determined partly by Ca2+‐dependent K+ channels. Graphs, relation between resting membrane potential of an AH/type 2 neuron and logarithm of external K+ concentration in presence and absence of Ca2+‐entry blockade with elevated Mg2+. Goldman‐Katz equation was used to fit solid lines to data points. Intracellular ion concentrations were assumed to be in millimoles per liter: K+ = 140; Na+ = 10; Cl− = 10. Permeability ratio that were used for plotting each curve are given. Inset shows superimposed the averaged electrotonic potentials produced by injection of constant‐current hyperpolarizing pulses in Krebs solution (top trace) and in Krebs with elevated Mg2+ and reduced Ca2+ (bottom trace). Permeability ratio for K+ was reduced >50% during blockade of Ca2+ entry. Increased amplitude of bottom trace in inset reflects increased input resistance associated with decreased K+ conductance.

From Grafe et al. 78
Figure 27. Figure 27.

Intracellular recording of postspike hyperpolarization in an AH/type 2 myenteric neuron of guinea pig small intestine. A: 2 action potentials evoked by stimulation of a nerve process in an interganglionic connective were followed by prolonged hyperpolarizing afterpotentials. Decreased amplitude of electrotonic potentials produced by hyperpolarizing current pulses reflects decreased input resistance during afterhyperpolarization. B: action potential and postspike hyperpolarization in same cell recorded on expanded time base. Prolonged afterhyperpolarizationn was delayed following positive afterpotential of spike.

From Wood and Mayer 228
Figure 28. Figure 28.

Electrical behavior of an S/type 1 neuron in myenteric plexus of guinea pig small intestine. A: repetitive spike discharge evoked by intracellular injection of depolarizing current. Frequency of discharge increased with increasing strength of injected current. B: repetitive discharge continued during prolonged injection of depolarizing current. Frequency of discharge to prolonged depolarization was also directly related to degree of depolarization. Upper traces, voltage records; bottom traces, current.
Figure 29. Figure 29.

Electrical slow waves in myenteric neuron of guinea pig small intestine. A; intrasomal injection of constant‐current hyperpolarizing pulses revealed progressive increase in input resistance during hyperpolarizing phase of slow wave and progressive decrease in input resistance during depolarizing phase of slow wave. Action potentials at offset of hyperpolarizing pulses occurred at crests of slow waves and reflected enhanced excitability at this stage of the wave. B: electrotonic potential at trough of a slow wave recorded on an expanded time base. C: electrotonic potential recorded near crest of wave. D: electrotonic potential with spike at the offset recorded at crest of a slow wave.
Figure 30. Figure 30.

Examples of fast EPSPs in myenteric neurons of guinea pig gastrointestinal tract. A: fast EPSP without action potential recorded in small intestine. B: fast EPSPs that triggered action potentials recorded in small intestine; 3 traces are superimposed. C: fast EPSP with action potential recorded from gastric fundus. D: fast EPSP with action potential recorded from distal colon.

C courtesy of M. Schemann; D courtesy of P. Wade
Figure 31. Figure 31.

Fast EPSP and response to ACh in AH/type 2 myenteric neuron of guinea pig small intestine. A: summation of afterhyperpolarization during repetitive spike discharge evoked by fiber tract stimulation. B: fast EPSP evoked by fiber tract stimulation in same neuron. C: response to microejected pulse of ACh in same cell.
Figure 32. Figure 32.

Properties of slow synaptic excitation in AH/type 2 myenteric neuron of guinea pig small intestine. A; slow EPSP and spike discharge evoked by electrical stimulation of interganglionic connective. Onset and offset of stimulation are indicated. B: slow depolarization of somal membrane by injected current did not enhance excitability and lead to spike discharge. C: spike‐interval histogram for train of spikes in A. Ordinate, number of intervals; abscissa, interval duration in milliseconds. Computer bin width, 1 ms. A and B: upper traces, transmembrane voltage; lower traces, current. Dashed line, resting membrane potential. Separation between stimulating and recording electrode was 600 μm.

From Wood and Mayer 229
Figure 33. Figure 33.

Properties of slow synaptic excitation in AH/type 2 myenteric neuron in guinea pig small intestine: example of augmented excitability during slow EPSP. A: intrasomal injection of long‐duration depolarizing current pulse failed to evoke spike discharge when neuron was in resting state. B: intrasomal injection of current in same cell evoked repetitive spike discharge when applied immediately after fiber tract stimulation released the transmitter for slow EPSP. Upper traces, transmembrane voltage. Lower traces, current records.
Figure 34. Figure 34.

Equivalent electrical circuit for slow synaptic excitation. High resting potential and low input resistance of AH/type 2 neurons result from high K+ conductance (gK) in Ca2+‐dependent K+ channels. Elevated levels of free cytosolic Ca2+ apparently hold these channels open at rest. Activation of receptors for the slow EPSP decreases inward Ca2+ current and reduces intracellular Ca2+. This leads to a decrease in Ca2+‐dependent K+ conductance, which accounts for increased input resistance and membrane depolarization. CM, membrane capacitance; gM, other ionic conductances of membrane. EM, equilibrium potential for other ionic conductances; EK, equilibrium potential for K+.
Figure 35. Figure 35.

Mimicry of slow synaptic excitation by forskolin‐induced activation of adenylate cyclase and elevation of cAMP in AH/type 2 myenteric neuron of guinea pig intestine. Arrow, application of 20‐ms pulse of 0.5 mM forskolin. Constant‐current depolarizing pulses were injected repetitively throughout the experiment. Forskolin depolarized the cell and enhanced excitability, as evidenced by spontaneous spike discharge and increased frequency of spike discharge during depolarizing pulses.
Figure 36. Figure 36.

Schematic diagram of steps in excitatory and inhibitory transduction of peptidergic signals in AH/type 2 neurons. Receptors for cholecystokinin (CCK), vasoactive intestinal polypeptide (VIP), and GRP‐bombesin (GRP, gastrin‐releasing peptide) are coupled to adenylate cyclase. Activation of the cyclase through these receptors leads to elevation of cAMP, protein phosphroylation, and ultimately the changes in membrane electrical behavior that account for slow synaptic excitation. Receptors for adenosine and other purines are also coupled to adenylate cyclase. Activation of these receptors inhibits cyclase and leads to inhibition of excitability. Excitatory signal transduction for substance P and calcitonin gene‐related peptide (CGRP) appears to not involve cAMP. Receptors for these messengers are either coupled directly to membrane channels or a different second‐messenger system is involved in signal transduction.

Courtesy of J. M. Palmer
Figure 37. Figure 37.

Functional significance of slow synaptic excitation in AH/type 2 neurons: gating mechanism. A: diagram of experiment demonstrating somal gating. Intracellular electrode (2) recorded electrical behavior of the soma (1). Fiber tract stimulation (4) fired both a process from the cell body (3) and an axon that synapsed with it (5). B: repetitive stimulation of fiber tract increased the probability that antidromic invasion of the soma by a spike in the process (3) would fire the somal membrane. Repetitive depolarizing pulses were injected into the soma during fiber tract stimulation. Each stimulus pulse to the fiber tract (sharp vertical deflections) evoked a spike in the process, and the spike invaded the soma electrotonically. Only after 7.75 s of repetitive fiber tract stimulation and development of the slow EPSP did each antidromic spike fire the soma (sharp vertical deflections of increased size). C: antidromic spikes and 1 somal spike from B recorded on expanded time base. Antidromic spikes became progressively larger as slow EPSP developed and ultimately reached threshold for firing a somal spike. Increased amplitude and slowed decay of antidromic potentials reflected increase in membrane resistance and time constant as the slow EPSP developed. When the soma fired, spike information was conducted away from the soma in the other processes of the multipolar neuron to other points in the plexus. Observations suggest that the somal membrane is specialized for a gating function that controls the spread of spike information between neurites that emerge from opposing poles of the soma. At rest, somal gate is closed. During the slow EPSP, somal gate is opened for transfer of spike information from one neurite to the other. Horizontal calibration 1 for B and 5 ms for C. Vertical calibration ∼60 mV.

From Wood and Mayer 229
Figure 38. Figure 38.

Slow synaptic inhibition in an AH/type 2 neuron of guinea pig small intestine.
Figure 39. Figure 39.

Presynaptic autoinhibition in AH/type 2 myenteric neuron of guinea pig small intestine. A: fast EPSP evoked by stimulation of an interganglionic connective. Arrow, stimulus artifact. B: treatment with eserine (10 μM) suppressed acetylcholinesterase and permitted accumulation of acetylcholine (ACh) at synaptic terminal. Activation of presynaptic cholinergic receptors suppressed release of ACh with consequent reduction in amplitude of the EPSP. C: application of atropine (10 μM) in presence of eserine restored the amplitude of the EPSP and prolonged its duration. This was due to blockade by atropine of presynaptic muscarinic receptors. D: application of hexamethonium (100 μM) in the presence of eserine and atropine suppressed the EPSP by blocking the nicotinic postsynaptic receptors.


Figure 1.

Discharge of 4 different units detected by a single extracellular microelectrode in myenteric ganglion of cat small intestine.

From Wood and Mayer 224


Figure 2.

Electrical current flow in bathing solution surrounding a neuron during occurrence of an action potential. Membrane is depolarized at site of spike generation (C). Outward current flows from points A and B and becomes inward current in the depolarized region, resulting in electrical fields illustrated by arrows and solid lines. Size and polarity of a potential recorded between an electrode placed near the neuron and ground potential is determined by density and direction of flow of current in the fields. Dashed lines, isopotential points in electrical fields. If electrode tip is to the left or right of the isopotential lines near points A or B, recorded potential is positive. If electrode tip is between isopotential lines near point C, polarity is negative. If the action potential propagates under an electrode, the electrode first detects the outward current, then the inward current at the depolarization site, and again an outward current. This results in a triphasic waveform resembling the spike shown in Figure 3C.



Figure 3.

Extracellularly and intracellularly recorded action potentials in myenteric neurons. A: extracellularly recorded biphasic spike characteristic of a somal or nonpropagated action potential. B: extracellularly recorded triphasic spike characteristic of a propagated action potential. C: extracellularly recorded spike with complex waveform characteristic of composite action potentials produced by sequential firing of initial segment and soma of a neuron. D: intracellularly recorded action potential evoked by electrical‐field stimulation (arrow, stimulus artifact). Upper trace, transmembrane voltage; lower trace, first time derivative (dV/dT) of voltage change. The dV/dT simulates extracellularly recorded biphasic potential in A. E: electrotonic spike from initial segment (arrow) triggered a somal spike. The dV/dT of transmembrane voltage simulates extracellularly recorded complex spike in C. Vertical calibration, 15 μV for A; 10 μV for B; 20 μV for C; 20 mV or 60 V/s for D and E. Horizontal calibration, ∼2 ms for A, D, and E; 1 ms for B; 5 ms for C.



Figure 4.

Bridge circuit used to pass electrical current across membrane of a neuron. Single microelectrode is used to inject current into the cell soma and to record resulting electrotonic potential across the membrane. Bridge circuit functions to remove the voltage drop that occurs across the resistance of the microelectrode during current injection. This is accomplished by a differential amplifier that subtracts a voltage proportional to the injected current from the total potential change recorded from the electrode. Thus only the potential due to current flow across the resistance and capacitance of the membrane is recorded.



Figure 5.

Structural relations of intestinal wall showing layers that must be removed to expose myenteric or submucosal plexus for electrical recording.

From Wood 223a). In: Physiology of the Gastrointestinal Tract, © 1987, Raven Press, New York


Figure 6.

Photomicrograph of longitudinal muscle‐myenteric plexus preparation of guinea pig duodenum as viewed with Nomarski optics for electrical recording



Figure 7.

Discharge of burst‐type unit in myenteric plexus of cat small intestine. A: burst pattern recorded with a slow time base. B: single burst of spikes from same neuron recorded with an expanded time base. C: nonsequential spike interval histogram. Ordinate, number of intervals. Abscissa, interval duration in milliseconds. Recorded with extracellular micropipette filled with 1 M NaCl. Vertical calibration, 50 μV. Horizontal calibration, 5 s in A; 0.5 s in B.



Figure 8.

Histogram of interval distribution of consecutive spikes within bursts of an erratic burst‐type unit in myenteric plexus of cat small intestine. Ordinate, duration of sequential interspike intervals given on abscissa. N, number of intervals; vertical bars, standard deviation. Coefficient of variation (standard deviation/mean) is inserted above each interval.

From Wood and Mayer 224


Figure 9.

Histograms of interburst intervals of consecutive bursts of spikes recorded extracellularly from 2 steady burst‐type myenteric neurons in cat small intestine. N, number of intervals; X, mean interval duration.

From Wood and Mayer 224


Figure 10.

Sequential variation of interburst intervals for an erratic burster recorded extracellularly from myenteric plexus of guinea pig small intestine. Ordinate, time interval between 1st spike of sequential bursts. Abscissa, 575 consecutive interburst intervals that occurred over a time span of 23 min. Ordinate values of 0, periodic conversion from burst discharge to continous discharge of single spikes or doublets. Long‐duration interburst interval after each episode of continuous discharge.

From Wood 217


Figure 11.

Characteristics of discharge of an erratic burst‐type unit recorded extracellularly in myenteric plexus of guinea pig small intestine. Note conversion from burst pattern of discharge to pattern of continuous discharge and reversion to burst pattern (cf. Fig. 10). Record is continuous from top to bottom trace. Recorded with glass‐insulated Pt wire electrode with 20‐μm‐diam tip.

From Wood 217


Figure 12.

Dogiel morphological classification of enteric ganglion cells.

From Dogiel 45


Figure 13.

Interactions between burst units. A: coupling between “driver‐follower” discharge of burst‐type units in myenteric plexus of cat small intestine. Inset, record of coupling of discharge of 2 different neurons. Interspike‐interval histogram for same neurons has 2 peaks corresponding to different frequency of spike discharge of 2 units. Ordinate, number of intervals; abscissa, interval duration in milliseconds. Computer bin width 0.5 ms. B: inhibition of burst‐type discharge by activity of a 2nd neuron in myenteric plexus of cat small intestine. 1, Single burst of spikes with no inhibitory discharge of 2nd unit. 2, Same burst unit with reduced frequency of discharge associated with preceding discharge of 2nd neuron. 3, Discharge of 2nd unit occurred after 1st spike of burst and was coincident with suppression of discharge of burst unit. 4, Occurrence of inhibitory discharge after 2nd spike of burst. 5, Occurrence of inhibitory discharge after 4th spike of burst. 6, Occurrence of inhibitory discharge after 6th spike of burst. Recorded with stainless steel needle electrode.

From Wood and Mayer 225


Figure 14.

Discharge of slowly adapting mechanoreceptor in myenteric plexus of dog small intestine. Unit did not discharge spontaneously but responded to mechanical stimulation (horizontal bars). A: responses to mechanical stimulation in absence of drugs. Mechanical stimulation was transient forward‐reverse movement of glass‐insulated Pt wire electrode over ∼20 μm. B: response to sustained stimulus in presence of 5‐HT. C: responses to transient stimulation in presence of 5‐HT. Second response with higher discharge frequency was produced by stimulus of greater intensity. D: progressive increase in discharge frequency evoked by progressive advancement of electrode in presence of 5‐HT. E: response of same cell to transient stimulation after washout of 5‐HT and in presence of norepinephrine.

From Wood and Mayer 225


Figure 15.

Relation of interspike interval to intensity of stimulation for a slowly adapting mechanoreceptor in myenteric plexus of cat small intestine. Ordinate, mean interspike interval; abscissa, distance of electrode displacement.

From Wood and Mayer 226


Figure 16.

Discharge of slowly adapting mechanoreceptor in myenteric plexus coincident with contractile activity of small intestinal muscularis externa in cat. Upper traces in each record are from an indium‐filled glass pipette microelectrode that was pushed through longitudinal muscle into myenteric plexus. Lower traces, electrical activity of musculature recorded with a suction electrode placed in the vicinity of the microelectrode. A: electrical activity of musculature consisted of electrical slow waves with spikes at crests of some slow waves. This activity was detected by the microelectrode in the myenteric plexus, but no nervous discharge is apparent on upper trace. B: after small change in position of microelectrode, nerve spikes appear on upper trace. C: neuronal spike frequency increased after occurrence of muscle spikes on slow waves and associated contractile activity of the muscle



Figure 17.

Structure of myenteric neurons that send projections to central nervous system. Somas of ganglion cells were labeled by horseradish peroxidase that was transported antidromically from a placement site on intestinal mesentery.

Courtesy of E. Fehér


Figure 18.

Discharge pattern of tonic‐type myenteric unit in cat small intestine. A: discharge of a train of spikes in response to mechanical stimulation. Mechanical stimulation was a transient forward‐reverse movement of a glass‐insulated Pt wire electrode with 20‐μm‐diam tip. B: relation between frequency of discharge of tonic‐type neurons of cat small intestinal myenteric plexus and 1‐s intervals after initiation of discharge. Four different units are represented.

From Wood and Mayer 226


Figure 19.

Interaction between discharge of a slowly adapting mechanosensitive unit and a unit that discharges trains of spikes. Small‐amplitude spikes on each record are from mechanosensitive unit. Discharge of mechanosensitive unit preceded large‐amplitude single spikes in top trace and trains of spikes in middle trace. Discharge of mechanoreceptor could not be detected during trainlike discharge of middle trace but resumed on bottom trace. Records were made with a glass‐insulated Pt wire electrode and are continuous.

From Wood 217


Figure 20.

Interconversion between tonic‐type and burst‐type discharge in small intestinal myenteric plexus of cat. A: discharge of spike train in response to mechanical stimulation (horizontal bar) followed by conversion to burst‐type discharge. Mechanical stimulation was a transient forward‐reverse movement of glass‐insulated PT wire electrode. Upper 3 traces, continuous records. Fourth trace, continuous with 3rd trace and shows consecutive bursts of spikes with times between consecutive bursts given in seconds. B: waveform of action potential of trainlike discharge. C: waveform of action potential of burst‐type discharge.

From Wood and Mayer 226


Figure 21.

Extracellular recording of discharge of single‐spike unit in myenteric plexus of cat small intestine. A: ongoing discharge in Tyrode's solution. B: elevation of Mg2+ to 10.2 mM in the solution did not affect discharge of the unit. C: nicotine (1 μM) excited the single‐spike unit. D: spike‐interval histogram computed for discharge shown in A. E: spike‐interval histogram computed in presence of elevated Mg2+. Ordinate, number of intervals. Abscissa, interval duration in milliseconds. Computer bin width 1 ms.

From Wood 223a). In: Physiology of the Gastrointestinal Tract, © 1987, Raven Press, New York


Figure 22.

Three kinds of intracellularly recorded electrical changes in myenteric neuron of guinea pig small intestine. Electrical stimulation of interganglionic fiber activated both a neurite extending from the neuron and an axon that formed a nicotinic synapse with the cell. Arrows: fast EPSP, electrotonic spike invading somal membrane, and somal spike triggered by electrotonic spike from the neurite.



Figure 23.

Refractory period of soma and neurites of myenteric neurons in guinea pig small intestine recorded intracellularly. Twin extracellular stimulus pulses were applied to surface of ganglia. Time interval between twin pulses was progressively shortened, until first the somal spikes and then the electrotonic invasions were not elicited by the second pulses. A: superimposed traces, refractory period for the somal spike was longer than for the spike conducted in the neurite. B: in another ganglion cell the refractory period for the somal spike was prolonged in association with a longer hyper‐polarizing afterpotential. Distance between stimulating and recording electrode for A was 80 μM and for B 110 μM. Stimulus pulse duration, 100 μs. (From 228



Figure 24.

Differential excitability between cell soma and 1 of its neurites in myenteric neuron of guinea pig small intestine. A: intrasomatic injection of depolarizing current pulse fired the soma and the neurite; however, the neurite fired more often (low‐amplitude electrotonic potentials) than the soma, indicating that the neurite membrane was more excitable than the soma. B: spontaneous occurrence of spikes in the neurite in the absence of spontaneous somal spikes in the same cell also suggests differential excitability.

Adapted from Wood 223a)


Figure 25.

Spontaneous spike discharge spreading electrotonically from the neurite into the soma of guinea pig myenteric neuron. Intracellularly recorded bursts of spikes in the neurite are similar to erratic burst‐type discharge of extracellular studies. A: continuous record of spikes in neurites and an occasional somal spike triggered by electrotonic current from the neurite spike. B: continuous record of decrease in interburst interval and conversion from bursts to trains of activity. C: prolonged silent period of cyclical discharge pattern of the neurite.

From Wood and Mayer 228


Figure 26.

Resting potential of enteric neurons is a K+ equilibrium potential determined partly by Ca2+‐dependent K+ channels. Graphs, relation between resting membrane potential of an AH/type 2 neuron and logarithm of external K+ concentration in presence and absence of Ca2+‐entry blockade with elevated Mg2+. Goldman‐Katz equation was used to fit solid lines to data points. Intracellular ion concentrations were assumed to be in millimoles per liter: K+ = 140; Na+ = 10; Cl− = 10. Permeability ratio that were used for plotting each curve are given. Inset shows superimposed the averaged electrotonic potentials produced by injection of constant‐current hyperpolarizing pulses in Krebs solution (top trace) and in Krebs with elevated Mg2+ and reduced Ca2+ (bottom trace). Permeability ratio for K+ was reduced >50% during blockade of Ca2+ entry. Increased amplitude of bottom trace in inset reflects increased input resistance associated with decreased K+ conductance.

From Grafe et al. 78


Figure 27.

Intracellular recording of postspike hyperpolarization in an AH/type 2 myenteric neuron of guinea pig small intestine. A: 2 action potentials evoked by stimulation of a nerve process in an interganglionic connective were followed by prolonged hyperpolarizing afterpotentials. Decreased amplitude of electrotonic potentials produced by hyperpolarizing current pulses reflects decreased input resistance during afterhyperpolarization. B: action potential and postspike hyperpolarization in same cell recorded on expanded time base. Prolonged afterhyperpolarizationn was delayed following positive afterpotential of spike.

From Wood and Mayer 228


Figure 28.

Electrical behavior of an S/type 1 neuron in myenteric plexus of guinea pig small intestine. A: repetitive spike discharge evoked by intracellular injection of depolarizing current. Frequency of discharge increased with increasing strength of injected current. B: repetitive discharge continued during prolonged injection of depolarizing current. Frequency of discharge to prolonged depolarization was also directly related to degree of depolarization. Upper traces, voltage records; bottom traces, current.



Figure 29.

Electrical slow waves in myenteric neuron of guinea pig small intestine. A; intrasomal injection of constant‐current hyperpolarizing pulses revealed progressive increase in input resistance during hyperpolarizing phase of slow wave and progressive decrease in input resistance during depolarizing phase of slow wave. Action potentials at offset of hyperpolarizing pulses occurred at crests of slow waves and reflected enhanced excitability at this stage of the wave. B: electrotonic potential at trough of a slow wave recorded on an expanded time base. C: electrotonic potential recorded near crest of wave. D: electrotonic potential with spike at the offset recorded at crest of a slow wave.



Figure 30.

Examples of fast EPSPs in myenteric neurons of guinea pig gastrointestinal tract. A: fast EPSP without action potential recorded in small intestine. B: fast EPSPs that triggered action potentials recorded in small intestine; 3 traces are superimposed. C: fast EPSP with action potential recorded from gastric fundus. D: fast EPSP with action potential recorded from distal colon.

C courtesy of M. Schemann; D courtesy of P. Wade


Figure 31.

Fast EPSP and response to ACh in AH/type 2 myenteric neuron of guinea pig small intestine. A: summation of afterhyperpolarization during repetitive spike discharge evoked by fiber tract stimulation. B: fast EPSP evoked by fiber tract stimulation in same neuron. C: response to microejected pulse of ACh in same cell.



Figure 32.

Properties of slow synaptic excitation in AH/type 2 myenteric neuron of guinea pig small intestine. A; slow EPSP and spike discharge evoked by electrical stimulation of interganglionic connective. Onset and offset of stimulation are indicated. B: slow depolarization of somal membrane by injected current did not enhance excitability and lead to spike discharge. C: spike‐interval histogram for train of spikes in A. Ordinate, number of intervals; abscissa, interval duration in milliseconds. Computer bin width, 1 ms. A and B: upper traces, transmembrane voltage; lower traces, current. Dashed line, resting membrane potential. Separation between stimulating and recording electrode was 600 μm.

From Wood and Mayer 229


Figure 33.

Properties of slow synaptic excitation in AH/type 2 myenteric neuron in guinea pig small intestine: example of augmented excitability during slow EPSP. A: intrasomal injection of long‐duration depolarizing current pulse failed to evoke spike discharge when neuron was in resting state. B: intrasomal injection of current in same cell evoked repetitive spike discharge when applied immediately after fiber tract stimulation released the transmitter for slow EPSP. Upper traces, transmembrane voltage. Lower traces, current records.



Figure 34.

Equivalent electrical circuit for slow synaptic excitation. High resting potential and low input resistance of AH/type 2 neurons result from high K+ conductance (gK) in Ca2+‐dependent K+ channels. Elevated levels of free cytosolic Ca2+ apparently hold these channels open at rest. Activation of receptors for the slow EPSP decreases inward Ca2+ current and reduces intracellular Ca2+. This leads to a decrease in Ca2+‐dependent K+ conductance, which accounts for increased input resistance and membrane depolarization. CM, membrane capacitance; gM, other ionic conductances of membrane. EM, equilibrium potential for other ionic conductances; EK, equilibrium potential for K+.



Figure 35.

Mimicry of slow synaptic excitation by forskolin‐induced activation of adenylate cyclase and elevation of cAMP in AH/type 2 myenteric neuron of guinea pig intestine. Arrow, application of 20‐ms pulse of 0.5 mM forskolin. Constant‐current depolarizing pulses were injected repetitively throughout the experiment. Forskolin depolarized the cell and enhanced excitability, as evidenced by spontaneous spike discharge and increased frequency of spike discharge during depolarizing pulses.



Figure 36.

Schematic diagram of steps in excitatory and inhibitory transduction of peptidergic signals in AH/type 2 neurons. Receptors for cholecystokinin (CCK), vasoactive intestinal polypeptide (VIP), and GRP‐bombesin (GRP, gastrin‐releasing peptide) are coupled to adenylate cyclase. Activation of the cyclase through these receptors leads to elevation of cAMP, protein phosphroylation, and ultimately the changes in membrane electrical behavior that account for slow synaptic excitation. Receptors for adenosine and other purines are also coupled to adenylate cyclase. Activation of these receptors inhibits cyclase and leads to inhibition of excitability. Excitatory signal transduction for substance P and calcitonin gene‐related peptide (CGRP) appears to not involve cAMP. Receptors for these messengers are either coupled directly to membrane channels or a different second‐messenger system is involved in signal transduction.

Courtesy of J. M. Palmer


Figure 37.

Functional significance of slow synaptic excitation in AH/type 2 neurons: gating mechanism. A: diagram of experiment demonstrating somal gating. Intracellular electrode (2) recorded electrical behavior of the soma (1). Fiber tract stimulation (4) fired both a process from the cell body (3) and an axon that synapsed with it (5). B: repetitive stimulation of fiber tract increased the probability that antidromic invasion of the soma by a spike in the process (3) would fire the somal membrane. Repetitive depolarizing pulses were injected into the soma during fiber tract stimulation. Each stimulus pulse to the fiber tract (sharp vertical deflections) evoked a spike in the process, and the spike invaded the soma electrotonically. Only after 7.75 s of repetitive fiber tract stimulation and development of the slow EPSP did each antidromic spike fire the soma (sharp vertical deflections of increased size). C: antidromic spikes and 1 somal spike from B recorded on expanded time base. Antidromic spikes became progressively larger as slow EPSP developed and ultimately reached threshold for firing a somal spike. Increased amplitude and slowed decay of antidromic potentials reflected increase in membrane resistance and time constant as the slow EPSP developed. When the soma fired, spike information was conducted away from the soma in the other processes of the multipolar neuron to other points in the plexus. Observations suggest that the somal membrane is specialized for a gating function that controls the spread of spike information between neurites that emerge from opposing poles of the soma. At rest, somal gate is closed. During the slow EPSP, somal gate is opened for transfer of spike information from one neurite to the other. Horizontal calibration 1 for B and 5 ms for C. Vertical calibration ∼60 mV.

From Wood and Mayer 229


Figure 38.

Slow synaptic inhibition in an AH/type 2 neuron of guinea pig small intestine.



Figure 39.

Presynaptic autoinhibition in AH/type 2 myenteric neuron of guinea pig small intestine. A: fast EPSP evoked by stimulation of an interganglionic connective. Arrow, stimulus artifact. B: treatment with eserine (10 μM) suppressed acetylcholinesterase and permitted accumulation of acetylcholine (ACh) at synaptic terminal. Activation of presynaptic cholinergic receptors suppressed release of ACh with consequent reduction in amplitude of the EPSP. C: application of atropine (10 μM) in presence of eserine restored the amplitude of the EPSP and prolonged its duration. This was due to blockade by atropine of presynaptic muscarinic receptors. D: application of hexamethonium (100 μM) in the presence of eserine and atropine suppressed the EPSP by blocking the nicotinic postsynaptic receptors.

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Article Title: Electrical and synaptic behavior of enteric neurons
 

How to Cite

Jackie D. Wood. Electrical and synaptic behavior of enteric neurons. Compr Physiol 2011, Supplement 16: Handbook of Physiology, The Gastrointestinal System, Motility and Circulation: 465-517. First published in print 1989. doi: 10.1002/cphy.cp060114