Abstract
Descending serotonergic, noradrenergic, and dopaminergic systems project diffusely to sensory, motor and autonomic spinal cord regions. Using neonatal mice, this study examined monoaminergic modulation of visceral sensory input and sympathetic preganglionic output. Whole-cell recordings from sympathetic preganglionic neurons (SPNs) in spinal cord slice demonstrated that serotonin, noradrenaline, and dopamine modulated SPN excitability. Serotonin depolarized all, while noradrenaline and dopamine depolarized most SPNs. Serotonin and noradrenaline also increased SPN current-evoked firing frequency, while both increases and decreases were seen with dopamine. In an in vitro thoracolumbar spinal cord/sympathetic chain preparation, stimulation of splanchnic nerve visceral afferents evoked reflexes and subthreshold population synaptic potentials in thoracic ventral roots that were dose-dependently depressed by the monoamines. Visceral afferent stimulation also evoked bicuculline-sensitive dorsal root potentials thought to reflect presynaptic inhibition via primary afferent depolarization. These dorsal root potentials were likewise dose-dependently depressed by the monoamines. Concomitant monoaminergic depression of population afferent synaptic transmission recorded as dorsal horn field potentials was also seen. Collectively, serotonin, norepinephrine and dopamine were shown to exert broad and comparable modulatory regulation of viscero-sympathetic function. The general facilitation of SPN efferent excitability with simultaneous depression of visceral afferent-evoked motor output suggests that descending monoaminergic systems reconfigure spinal cord autonomic function away from visceral sensory influence. Coincident monoaminergic reductions in dorsal horn responses support a multifaceted modulatory shift in the encoding of spinal visceral afferent activity. Similar monoamine-induced changes have been observed for somatic sensorimotor function, suggesting an integrative modulatory response on spinal autonomic and somatic function.
Highlights
The central nervous system receives sensory information from the visceral organs through two paths: the vagus nerve, which projects to the nucleus of the solitary tract [1] and through sympathetic and pelvic parasympathetic nerves, which pass through prevertebral and/or paravertebral ganglia to the thoracolumbar and sacral spinal cord [2,3]
In Vitro Spinal Cord and Sympathetic Chain Preparation In order to examine net modulatory actions on thoracic spinal efferents and visceral afferent evoked primary afferent depolarization (PAD), both ventral root efferent and dorsal root afferent responses to visceral sensory stimulation were assessed with DC recordings
Calcitonin gene-related peptide (CGRP)+ visceral afferents travel through sympathetic ganglia While many studies have shown that visceral afferents project to dorsal root ganglia (DRG) several segments away from their spinal nerves [14,15,16], few have suggested they reach the appropriate DRGs by traveling within the sympathetic chain [2,57]
Summary
The central nervous system receives sensory information from the visceral organs through two paths: the vagus nerve, which projects to the nucleus of the solitary tract [1] and through sympathetic and pelvic parasympathetic nerves, which pass through prevertebral and/or paravertebral ganglia to the thoracolumbar and sacral spinal cord [2,3]. Myelinated and unmyelinated visceral afferents [10,11,12] comprise a small percentage of dorsal root ganglia neurons in the thoracolumbar spinal regions [10,11,13], yet they project multi-segmentally and more diffusely than their somatic counterparts [14,15,16]. Stimulation of splanchnic nerve has been used to study visceral afferent inflow and has been shown to evoke both autonomic and somatic motor spinal reflexes [12,18,19,20,21]
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