Synaptic responses evoked by mechanical stimulation of the mucosa in morphologically characterized myenteric neurons of the guinea-pig ileum

Abstract

Recordings were made from myenteric neurons of the guinea-pig ileum during reflexes evoked by mechanical stimulation of the mucosa. Impaled neurons were injected with dye (Lucifer yellow or biocytin), and their shapes were determined. All neurons were 5-12 mm from the stimulus, a brush stroke that deformed the mucosal villi. Neurons were classified as S-neurons or AH-neurons (Hirst et al., 1974). About 40% of S-neurons oral to a stimulus responded with bursts of fast EPSPs (average frequency, 15-40 Hz); these neurons were in ascending reflex pathways. About 60% of S-neurons anal to a stimulus responded with similar bursts of fast EPSPs or slow depolarizations; these neurons were in descending pathways. Only 2 of 48 AH-neurons responded, both in descending pathways. Most S-neurons in either ascending or descending pathways received inputs from at least 2 or 3 other neurons. Action potentials evoked during a response averaged 3-10 Hz in frequency, with occasional bursts at up to 100 Hz. The speed of conduction along the reflex pathways was about 0.5 m/sec. All S-neurons were uniaxonal, but they differed in size, dendritic morphology, and projections. The axons of S-neurons injected with biocytin were followed up to 7 mm within the myenteric plexus. Three S-neurons projected to the tertiary plexus and were probably longitudinal muscle motor neurons; 2 of these were in descending pathways. Five S-neurons projected along the intestine and had varicose collaterals in some ganglia. These neurons were probably interneurons; 3 were descending and 2 ascending, and all responded in the appropriate reflex pathway. Many S-neurons had short axons that entered the circular muscle and were probably circular muscle motor neurons. Others projected several millimeters along the intestine before entering the circular muscle or fading beyond detection. From this study, we have been able to deduce the circuits mediating ascending and descending mucosa-to-muscle reflexes. It is concluded that AH-neurons are primary sensory neurons and S-neurons are interneurons and muscle motor neurons in the circuits.

Dynamics of fast synaptic excitation during trains of stimulation in myenteric neurons of guinea-pig ileum

“…In isolated segments of guinea pig ileum, it has been shown that mechanical stimulation of mucosal villi generates short bursts of fEPSPs that occurred in the frequency range of 15 − 40 (Bornstein et al 1991). In similar experiments it was shown that if the mechanical stimulus is applied at intervals of less than 10 seconds, the amplitude of fEPSPs declined during repetitive stimulation (Smith et al, 1992).…”

“…Electrophysiological studies in myenteric neurons maintained in primary culture have shown that nAChRs desensitize much more quickly than P2X receptors expressed by the same neurons (Zhou and Galligan, 1998;Zhou et al, 2002;Brown and Galligan, 2003). Different receptor desensitization rates may have functional significance for the control of GI motility as it has been shown that mechanical stimulation of the mucosa in isolated segments of guinea-pig ileum elicits bursts of fEPSPs that occur at frequencies ranging between 15 − 40 Hz (Bornstein et al, 1991;Smith et al, 1992). Similar bursts of fEPSPs were also elicited when chemical stimulation was applied to mucosa (Bertrand et al, 1997).…”

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].…”

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

“…Modulatory cholinergic (Grider and Makhlouf, 1986;Smith and Fumess, 1988;Tonini and Costa, 1990) and noncholinergic Makhlouf, 1987, 1992; interneurons link the enteric motor neurons to afferent sensory neurons. The sensory neurons activated by muscle stretch and mucosal stimulation are distinct, converging on the same motor neurons (Bornstein et al, 1991a;Smith et al, 1992a). The two populations of sensory neurons can be activated concurrently by muscle stretch and mucosal stimulation leading to augmentation of the efferent response (Smith et al, 199 1;Yuan et al, 1991).…”