Relation between electrophysiological class and neuropeptide content of guinea pig sympathetic prevertebral neurons

Abstract

1. Sympathetic neurons in superior mesenteric ganglion and inferior mesenteric ganglion (IMG) isolated from guinea pigs were classified as tonic, phasic, or long after hyperpolarizing (LAH) on the basis of their discharge characteristics and the different types of potassium currents recorded from them with the soma under single-microelectrode voltage clamp. 2. Passive electrical properties showed a progressive increase in input resistance across the prevertebral ganglia in the rostrocaudal direction when compared with those previously reported for the same classes of neurons in celiac ganglia (CG). 3. The proportions of tonic, phasic, and LAH neurons changed markedly in a rostrocaudal progression from 37, 14, and 49%, respectively, in the CG to 80, 18, and 2%, respectively, overall in the IMG. 4. Three populations of neurons distinguished immunohistochemically by their content of somatostatin (SOM), neuropeptide Y (NPY), or neither neuropeptide were present in different proportions in each prevertebral ganglion. The proportions of SOM, NPY, and no peptide neurons changed from 27, 34, and 39%, respectively, in the CG to 45, 20, and 35%, respectively, in the IMG. There was no significant difference in these distributions between the sexes. 5. Individual electrophysiologically characterized neurons were filled with biocytin and later examined for SOM immunoreactivity. All SOM-positive neurons (9/9) in the CG but only 7/10 in the IMG were tonic, whereas SOM-negative neurons were classified in all electrophysiological classes. 6. Other than this one group of sympathetic neurons (constituting nearly 30% of neurons in both CG and IMG), the three electrophysiological classes do not correlate directly with the three neurochemical types so far identified. This is consistent with the existence of more than three functional groups of sympathetic neurons in the prevertebral ganglia. The findings also suggest that a major inhibitory effect on mucosal secretion, as well as on motility, is mediated by peripheral reflex pathways along much of the length of the gastrointestinal tract.

Immediate-Early Gene Expression in the Inferior Mesenteric Ganglion and Colonic Myenteric Plexus of the Guinea Pig

“…Previous studies have demonstrated correlations between the neurochemistry, projections, major inputs, and presumably the function of neurons in the guinea pig celiac ganglion that supplies sympathetic nerves to the small bowel (Macrae et al, 1986;Keast et al, 1993;L uckensmeyer andKeast, 1995, 1996). These data also support the idea that immunohistochemically defined subsets of IMG neurons represent chemically coded groups with distinct functions.…”

“…Some IMG neurons also contain neuropeptide Y immunoreactivity (N PY neurons; ϳ20% of IMG neurons), and other subsets include those containing somatostatin (SOM neurons; ϳ75%), both N PY and SOM (N PY/SOM neurons; 4 -7%), or neither N PY nor SOM (Ϫ/Ϫ neurons; 1-5%) (Elf vin et al, 1993;Sann et al, 1995;Parr and Sharkey, 1996). Most or all NPY neurons project to the vasculature (Furness et al, 1983), whereas SOM and Ϫ/Ϫ neurons project to the myenteric and submucosal plexuses of the enteric nervous system (ENS) in the wall of the colon (Keast et al, 1993;Parr and Sharkey, 1996).…”

Different types of ganglion cell in the cardiac plexus of guinea‐pigs.

“…The idea that several types of cardiac ganglion cell may exist in the guinea-pig is supported by immunohistochemical studies; several different types of cardiac ganglion cell can be distinguished on the basis of their neuropeptide content (Steele, Gibbins, Morris & Mayer, 1994). In other peripheral ganglia, populations of ganglion cells with different combinations of neuropeptides have been found to have different electrical properties (Furness & Costa, 1987;Keast, McLachlan & Meckler, 1993 …”

Three electrophysiological classes of guinea pig sympathetic postganglionic neurone have distinct morphologies

“…Two firing patterns, phasic and tonic, have been described in various intact sympathetic ganglia isolated in vitro from several species (see Adams and Harper, 1995). Detailed analyses have identified a third class of cell in ganglia from guinea pigs (Cassell and McLachlan, 1987;Christian and Weinreich, 1988;McLachlan and Meckler, 1989;Keast et al, 1993), rabbits (Cassell and McLachlan, 1987) and rats (L. Melnichenko and E. McLachlan, unpublished observations). These have been called long-afterhyperpolarising (LAH) neurones; they discharge phasically but have an afterhyperpolarisation lasting seconds.…”

“…They form the predominant population in different anatomical locations: phasic (Ph ) neurones in the paravertebral chain, tonic (TI neurones in the inferior mesenteric ganglion, and LAH neurones in the coeliac ganglion. Further, the passive electrical properties of the neurones differ not only between the classes but also, within one class, between locations (Keast et al, 1993). Finally, neurones of each class receive different patterns of synaptic input: P h and LAH neurones receive at least one suprathreshold preganglionic input in addition to several subthreshold ones (Hirst and McLachlan, 1984;McLachlan and Meckler, 1989).…”