An intracellular analysis of some intrinsic factors controlling neural output from inferior mesenteric ganglion of guinea pigs

Abstract

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.

Central innervation of neurones in the inferior mesenteric ganglion and of the large intestine of the cat

“…The threshold depolarization for initiation of a single action potential ranged from 5 to 18 mV. The voltage trajectory of an action potential was the same as that previously described for the inferior mesenteric ganglion of the guinea-pig (Weems & Szurszewski, 1978).…”

“…The distribution of preganglionic fibres arising from lumbar spinal segments L1-L6 to neurones of the inferior mesenteric ganglion was determined by recording synaptic responses intracellularly from neurones in the ganglion during electrical stimulation of the lumbar white rami. The methods used to record intracellularly from the ganglion cells have been described previously (Weems & Szurszewski, 1978).…”

A study of renal‐efferent neurones and their neural connexions within cat renal ganglia using intracellular electrodes.

“…This indicates that for some reason, a relatively large group of neurones of the renal ganglia had durations of the afterspike hyperpolarization that were approximately 2 times greater than the durations of the largest modal class of neurones. Since this duration can play an important role in determining the firing frequency of sympathetic, prevertebral neurones (Weems & Szurszewski, 1978), one wonders if the neurones of these two modal classes have different physiological roles. The duration of the afterspike hyperpolarizations produced by neurones located within superior cervical ganglia is modulated by norepinephrine (Horn & McAfee, 1980).…”

Reflex pathways in the abdominal prevertebral ganglia: evidence for a colo‐colonic inhibitory reflex.

“…These fibres are axons of neurones whose cell bodies lie in the periphery (McLennan & Pascoe, 1954;Job & Lundberg, 1952;Syromyatnikov & Skok, 1968). Intracellular recordings have been made from prevertebral ganglia (Croweroft & Szurszewski, 1971;Crowcroft, Holman & Szurszewski, 1971;Weems & Szurszewski, 1977, 1978Kreulen & Szurszewski, 1978b). These studies show that neurones in the inferior mesenteric ganglion, superior mesenteric ganglion, and coeliac ganglion of the guinea pig receive afferent input from the distal colon.…”