Physiology of prevertebral ganglia in mammals with special reference to inferior mesenteric ganglion

Author(s):  
J. H. Szurszewski ◽  
B. F. King

The distribution and origin of substance P immunoreactive nerve elements have been studied in the guinea-pig prevertebral ganglia by the indirect immunohistochemical technique, using a monoclonal antibody to substance P. Non-varicose substance P immunoreactive nerve fibres enter or leave the ganglia in all nerves associated with them, traversing the ganglia in larger or smaller bundles. Networks, mainly singlestranded, of varicose substance P immunoreactive nerve fibres also permeate the ganglia, forming a loose meshwork among the neurons. Similar networks are present in the lumbar paravertebral ganglia. In all these ganglia, neuronal somata do not in general show substance P immunoreactivity. The various nerves connected with the inferior mesenteric ganglion have been cut, in single categories and in various combinations, and the ganglion examined, after intervals of up to six days. Cutting the colonic or hypogastric nerves, which connect the ganglion with the hindgut and pelvic organs, leads to accumulation of substance P immunoreactive material in their ganglionic stumps, extending retrogradely to intraganglionic non-varicose fibres traceable through into the intermesenteric and lumbar splanchnic nerves. There is some local depletion of intraganglionic varicose networks. Cutting the intermesenteric nerve, which connects the coeliac-superior mesenteric ganglion complex with the ganglion, leads to accumulation of substance P immunoreactive material in its cranial stump and depletion of its distal stump; a minimal depletion is detectable in the inferior mesenteric ganglion itself. Cutting the lumbar splanchnic nerves, which connect the ganglion with the upper lumbar spinal cord and dorsal root ganglia, leads to accumulation of substance P immunoreactive material in their proximal stumps and total depletion of their distal, ganglionic stumps; in the ganglion there is subtotal loss of non-varicose substance P immunoreactive fibres and of varicose nerve networks, and the few surviving non-varicose fibres are traceable across the ganglion from the intermesenteric nerve to the colonic and hypogastric nerves. Cutting the intermesenteric and lumbar splanchnic nerves virtually abolishes substance P immunoreactive elements from the ganglion within three days postoperatively. It is concluded that these arise centrally to the ganglion. Capsaicin treatm ent of guinea-pigs, which depletes substance P immunoreactivity of sensory neurons, was found to leave no more than minute occasional traces of substance P immunoreactivity in the prevertebral ganglia and in dorsal root ganglion cells and spinal laminae I and II; in the ileum, substance P immunoreactivity was abolished from the paravascular nerves and perivascular nerve networks, and from large nerve varicosities in the submucous plexus. The substance P immunoreactivity of the myenteric and submucous plexuses and of the nerve networks in the muscle and mucosal layers was however otherwise unaffected. Removal of the spinal cord caudally to the seventh thoracic segment without injury to the dorsal root ganglia is without detectable effect either on the substance P immunoreactive elements of the inferior mesenteric ganglion and associated nerves, or on the peri- and paravascular nerves of the hindgut mesenteric vessels. It is concluded that the intraganglionic substance P immunoreactive elements of the prevertebral ganglia are attributable to sensory neurons of the dorsal root ganglia, and that intraspinal and enteric neurons do not contribute significantly to them. It is further postulated with the support of indirect evidence that the intraganglionic networks of varicose substance P immunoreactive fibres, which have been shown to form synapses upon the postganglionic neurons, arise as collateral branches from the substance P immunoreactive sensory fibres which traverse the ganglia, and that these can subserve a short-loop reflex control over the excitability of the ganglionic neurons in advance of, and, or, in support of, or even independently of, the recruitment of central nervous circuits.


1978 ◽  
Vol 41 (2) ◽  
pp. 305-321 ◽  
Author(s):  
W. A. Weems ◽  
J. H. Szurszewski

1. In vitro studies were conducted on neurons within the inferior mesenteric ganglion (IMG) of guinea pigs to investigate how intrinsic features of the spike-generating process interact with preganglionic inputs to produce the output firing patterns of these neurons. Intracellular-electrode techniques were used to monitor and control electrical activity of IMG neurons. Preganglionic inputs were activated either synchronously by stimulating an attached nerve trunk or asynchronously by leaving the ganglion attached to a segment of terminal colon and activating the colonic-IMG mechanosensory system. 2. Ninety-seven percent of the neurons studied demonstrated an afterspike hyperpolarization (ASH). The ASH process was activated only by the occurrence of a spike and did not have a synaptically induced component. Further activation of this process was produced by two or more spikes having interspike intervals less than the duration of an ASH following a single spike. An aftertrain hyperpolarization (ATH) resulted from this progressive activation. The amplitude of both the ASH and the ATH decreased when the resting membrane potential was hyperpolarized by current injection or by increasing the external potassium ion concentration. 3. Neuronal excitability was reduced during the ASH. From this observation it was concluded that when IMG neurons operate in the occasional-firing mode, the ASH process prevents output frequency from greatly exceeding the reciprocal of the ASH duration produced by a single spike. 4. Two types of synaptically induced slow depolarizations were observed: a slow, long-latency depolarization and a short-latency depolarization (SLD). These depolarizations differed in their latency, onset, and duration. Both were capable of converting synchronous, preganglionic input from subthreshold (non-spike-activating) to threshold (spike-activating) activity. 5. Neurons having resting potentials more positive than -60 mV were capable of firing in the rhythmic-firing mode; 40% of these neurons demonstrated tonic- and 60% phasic-firing behavior. Frequency-current relations for tonic-discharging neurons were linear from the rhythmic-firing threshold to current levels approximately 2.5 times the threshold value. Minimal frequency for tonic firing and the slope of the linear portion of the frequency-current relation were indirectly related to the duration of the ASH. 6. This study suggests that sympathetic, noradrenergic neurons of the IMG can operate in either the occasional- or rhythmic-firing mode. In the physiologic state in vivo, most IMG neurons probably do not produce action potentials in excess of 10-15 Hz because of their intrinsic properties which regulate firing in both modes of operation.


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