Simultaneous intracellular recordings from enteric neurons reveal that myenteric ah neurons transmit via slow excitatory postsynaptic potentials

Simultaneous intracellular electrical recordings were made from pairs of neurons separated circumferentially by 100-200 microns of the myenteric plexus of the guinea-pig ileum in vitro. The recording electrodes were filled with the dye neurobiotin which was injected into impaled nerve cells, and later revealed histochemically. Intracellular current pulses were used to evoke action potentials via the recording electrode in one type of myenteric neuron, in most cases an AH neuron, while a second electrode was used to record from a simultaneously impaled S neuron or AH neuron. AH neurons are thought to be primary sensory neurons, whereas S neurons are interneurons and motor neurons. Ninety pairs of neurons were adequately tested for interaction. From these, 17 S neurons and three AH neurons that responded to AH neuron stimulation were detected. In each case, the response was a slow depolarization that was seen only in response to a train of stimuli at 10 Hz. The slow depolarizations were enhanced by passing depolarizing current and diminished by hyperpolarization. Responses were also diminished by lowering external Ca.2+ and elevating Mg2+. In all cases in which intracellular recording indicated communication between neurons, morphological evidence of connection was seen. In no case was there communication without connection, but in four instances, morphological connections appeared to exist, although no physiological evidence of communication was obtained.

[1]  G. Hirst,et al.  Two types of neurones in the myenteric plexus of duodenum in the guinea‐pig , 1974, The Journal of physiology.

[2]  J. Bornstein,et al.  Electrophysiology and enkephalin immunoreactivity of identified myenteric plexus neurones of guinea‐pig small intestine. , 1984, The Journal of physiology.

[3]  R. North,et al.  Slow synaptic potentials in neurones of the myenteric plexus. , 1980, The Journal of physiology.

[4]  S. Pompolo,et al.  DOGIEL TYPE-II NEURONS IN THE GUINEA-PIG SMALL-INTESTINE - ULTRASTRUCTURE IN RELATION TO OTHER CHARACTERISTICS , 1989 .

[5]  J. Wood,et al.  Serotonergic activation of tonic-type enteric neurons in guinea pig small bowel. , 1979, Journal of neurophysiology.

[6]  W. Armstrong,et al.  A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: Comparison with biocytin , 1991, Journal of Neuroscience Methods.

[7]  H. Tamir,et al.  Identification and stimulation by serotonin of intrinsic sensory neurons of the submucosal plexus of the guinea pig gut: activity- induced expression of Fos immunoreactivity , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  S. Brookes,et al.  Immunohistochemical identification of cholinergic neurons in the myenteric plexus of guinea-pig small intestine , 1991, Neuroscience.

[9]  R. North,et al.  Significance of slow synaptic potentials for transmission of excitation in guinea-pig myenteric plexus , 1985, Neuroscience.

[10]  J. Furness,et al.  Origins of synaptic inputs to calretinin immunoreactive neurons in the guinea-pig small intestine , 1993, Journal of neurocytology.

[11]  J. Bornstein,et al.  Ramifications of the axons of AH‐neurons injected with the intracellular marker biocytin in the myenteric plexus of the guinea pig small intestine , 1991, The Journal of comparative neurology.

[12]  P. Grafe,et al.  Fast excitatory postsynaptic potentials in AH (Type 2) neurons of guinea pig myenteric plexus , 1979, Brain Research.

[13]  J. Bornstein,et al.  Convergence of reflex pathways excited by distension and mechanical stimulation of the mucosa onto the same myenteric neurons of the guinea pig small intestine , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  W M Bayliss,et al.  The movements and innervation of the small intestine , 1899, The Journal of physiology.

[15]  R. North,et al.  Muscarinic synaptic potentials in guinea‐pig myenteric plexus neurones. , 1982, The Journal of physiology.

[16]  G. Lees,et al.  Slow intracellular potentials in AH-neurons of the myenteric plexus evoked by repetitive activation of synaptic inputs , 1984, Neuroscience.

[17]  M. Costa,et al.  A pharmacological analysis of the neuronal circuitry involved in distension-evoked enteric excitatory reflex , 1990, Neuroscience.

[18]  F. Edwards,et al.  Cholinergic neuromuscular transmission in the longitudinal muscle of the guinea‐pig ileum. , 1993, The Journal of physiology.

[19]  T. K. Smith,et al.  Reflex changes in circular muscle activity elicited by stroking the mucosa: an electrophysiological analysis in the isolated guinea-pig ileum. , 1988, Journal of the autonomic nervous system.

[20]  J C Bornstein,et al.  Synaptic responses evoked by mechanical stimulation of the mucosa in morphologically characterized myenteric neurons of the guinea-pig ileum , 1991, Journal of Neuroscience.

[21]  W. O'Neill,et al.  Calbindin‐like immunoreactivity in the central auditory system of the mustached bat, Pteronotus parnellii , 1991, The Journal of comparative neurology.

[22]  S. Brookes,et al.  Identification of motor neurons to the longitudinal muscle of the guinea pig ileum. , 1992, Gastroenterology.

[23]  P. Grafe,et al.  Evidence that substance P does not mediate slow synaptic excitation within the myenteric plexus , 1979, Nature.

[24]  R. North,et al.  Evidence that substance P is a neurotransmitter in the myenteric plexus , 1980, Nature.

[25]  J. Bornstein,et al.  Distension-evoked ascending and descending reflexes in the circular muscle of guinea-pig ileum: an intracellular study. , 1990, Journal of the autonomic nervous system.

[26]  G. Lees,et al.  Morphological studies of electrophysiologically-identified myenteric plexus neurons of the guinea-pig ileum , 1983, Neuroscience.

[27]  K. Morita,et al.  Substance P inhibits activation of calcium‐dependent potassium conductances in guinea‐pig myenteric neurones. , 1992, The Journal of physiology.

[28]  T. Iwanaga,et al.  Electrophysiology of guinea-pig myenteric neurons correlated with immunoreactivity for calcium binding proteins. , 1988, Journal of the autonomic nervous system.

[29]  R. Nishi,et al.  Neurons dissociated from rat myenteric plexus retain differentiated properties when grown in cell culture III. Synaptic interactions and modulatory effects of neurotransmitter candidates , 1985, Neuroscience.

[30]  J. Furness,et al.  Ultrastructure and synaptic relationships of calbindin-reactive, Dogiel type II neurons, in myenteric ganglia of guinea-pig small intestine , 1988, Journal of neurocytology.

[31]  H. Steinbusch,et al.  Neurons with 5-hydroxytryptamine-like immunoreactivity in the enteric nervous system: Their visualization and reactions to drug treatment , 1982, Neuroscience.

[32]  S. Brookes,et al.  Identification and immunohistochemistry of cholinergic and non-cholinergic circular muscle motor neurons in the guinea-pig small intestine , 1991, Neuroscience.

[33]  S. Brookes,et al.  Identification of myenteric neurons which project to the mucosa of the guinea-pig small intestine , 1991, Neuroscience Letters.

[34]  J. Wood,et al.  Slow synaptic excitation mediated by serotonin in Auerbach's plexus , 1978, Nature.

[35]  P. Holzer Ascending enteric reflex: multiple neurotransmitter systems and interactions. , 1989, The American journal of physiology.

[36]  J. Bornstein,et al.  Electrophysiological analysis of projections of enteric inhibitory motoneurones in the guinea‐pig small intestine. , 1986, The Journal of physiology.