Convergence of reflex pathways excited by distension and mechanical stimulation of the mucosa onto the same myenteric neurons of the guinea pig small intestine

Abstract

The effects on morphologically and electrophysiologically characterized myenteric neurons of activation of intestinal reflex pathways were examined in vitro. Opened segments of guinea pig small intestine were pinned serosa down in an organ bath that had two balloons set into its base. A 5-10-mm-wide strip of myenteric plexus between the balloons was exposed from the mucosal side, and neurons were impaled with microelectrodes. Reflex pathways were stimulated by inflation of the balloons to distend the intestinal wall, and by deforming the exposed mucosal villi with a brush. Impaled neurons were classified electrophysiologically as AH-neurons or S-neurons (Hirst et al., 1974) and were injected with biocytin to determine their shapes and projections. None of the 58 AH-neurons responded to distension. In contrast, 63 of 131 S-neurons responded to distension with a burst of fast EPSPs; about one-third of the responding S-neurons received input from ascending reflex pathways, one-third received input from descending reflex pathways, and one-third received input from both ascending and descending pathways. Most neurons in this last group supplied extensive varicose branches to the tertiary plexus and were probably longitudinal muscle motor neurons. Neurons receiving input from only one pathway usually projected in the direction of that pathway; many of these were circular muscle motor neurons. Almost all neurons responding to distension were also excited by deforming the villi. Responses evoked by distension or deforming the mucosa declined when stimuli were repeated at intervals less than 10 sec. This was seen in ascending and descending pathways but was more prominent in the former. Deforming the mucosa evoked a normal response even when the response to repeated distensions had disappeared. It is concluded that distension and deforming the mucosa excite separate populations of sensory neurons to activate reflex pathways that converge onto common motor neurons and probably onto common interneurons.

Synaptic Transmission at Functionally Identified Synapses in the Enteric Nervous System: Roles for Both Ionotropic and Metabotropic Receptors

“…1A) [11], and are termed S/uniaxonal neurons in the discussion below. One major role of the AH/Dogiel type II neurons is as intrinsic sensory (or primary afferent) neurons (for reviews see [12,34,35], while S/uniaxonal neurons are interneurons, muscle motor neurons and secretomotor neurons [12,13,113]. However, while this division is convenient, it remains somewhat controversial because AH/Dogiel type II neurons receive excitatory synaptic input (see below) and thus may act as interneurons under some conditions [123,124,133].…”

“…The interneurons act to excite other interneurons of the pathway and motor neurons supplying the circular muscle, with ascending interneurons contacting excitatory motor neurons and descending interneurons contacting inhibitory motor neurons. In guinea-pig ileum, both ascending and descending interneurons excite the excitatory motor neurons innervating the longitudinal muscle [113]. Because the interneurons run for significant distances within the myenteric plexus before contacting the motor neurons, the output of the reflex pathways is physically separated from the neural elements involved in sensory transduction.…”

“…Transmission between ascending interneurons and other ascending interneurons is via nAChR [55], while transmission between ascending interneurons and excitatory motor neurons supplying the circular muscle is via nAChR and NK 3 tachykinin receptors [126]. The pharmacology at specific synapses within the ascending reflex pathway excited by mucosal deformation is identical to that of the equivalent synapses of the pathway excited by distension [126], although the intrinsic sensory neurons involved are clearly distinct populations [12,35,113]. Thus, fast EPSPs mediated by nAChR play a role at every functionally defined synapse within the ascending excitatory pathway, but metabotropic receptors, and presumably slow EPSPs, are also important at some synapses.…”

Distinct populations of sensory neurons mediate the peristaltic reflex elicited by muscle stretch and mucosal stimulation

“…The efferent motor limb of the intestinal peristaltic reflex evoked by stretch applied to circular muscle consists oftwo components: an orad or ascending contraction accompanied by excitatory junction potentials (EJPs) and a caudad or descending relaxation accompanied by inhibitory junction potentials (IJPs) (Costa and Fumess, 1976;Grider and Makhlouf, 1986;Smith et al, 1990Smith et al, , 1992aYuan et al, 1991). The components reflect release of the excitatory motor transmitters acetylcholine (ACh) and the tachykinins substance P (SP) and neurokinin A (Grider and Makhlouf, 1986;Smith and Fumess, 1988;Grider, 1989a;Smith et al, 1990), and the inhibitory motor transmitters vasoactive intestinal peptide (VIP) and nitric oxide (NO) (Grider and Makhlouf, 1986;Grider, 1993).…”

Structural abnormalities associated with congenital megacolon in transgenic mice that overexpress the Hoxa‐4 gene

“…Collagen is not found within the ganglia and interganglionic connectives of the ENS; instead, support for the neural structures is derived from specialized supporting cells, which resemble the astrocytes of the central nervous system (CNS), and have been called enteric glia Gershon and Rothman, 1991). The ENS is the only region of the PNS that is capable of mediating reflex behavior in the absence of input from the CNS (Trendelenburg, 1917;Biilbring and Crema, 1959;Kosterlitz and Lees, 1964;Hendriks et al, 1990;Kirchgessner et al, 1992;Smith et al, 1992).…”