Neurotransmission at the interface of sympathetic and enteric divisions of the autonomic nervous system

Abstract

The sympathetic and enteric divisions of the autonomic nervous system are interactive in the determination of the functional state of the digestive tract. Activation of the sympathetic input suppresses digestive function primarily through release of norepinephrine at its synaptic interface with the enteric nervous system. The enteric nervous system functions like an independent minibrain in the initiation of the various programmed patterns of digestive tract behavior and moment-to-moment control as the neural microcircuits carry-out the behavioral patterns. Most of the postganglionic projections from sympathetic prevertebral ganglia terminate as synapses in myenteric and submucous ganglia of the enteric nervous system. Two primary actions of the sympathetic input are responsible for suppression of motility and secretion. First is presynaptic inhibitory action of norepinephrine to suppress release of neurotransmitters at fast and slow excitatory synapses in the enteric neural microcircuits and this effectively shuts-down the circuit. Second is inhibitory synaptic input to submucosal secretomotor neurons to the intestinal crypts. The alpha, adrenergic receptor subtype mediates both actions. Axons of secretomotor neurons to the crypts bifurcate to innervate and dilate the submucosal vasculature. Dilitation of the vasculature increases blood flow in support of increased secretion. Sympathetic inhibitory input to the secretomotor neurons therefore suppresses both secretion and blood flow. Activation of the sympathetic nervous system cannot explain the symptoms of secretory diarrhea and abdominal discomfort associated with psychologic and other forms of stress. Current evidence suggests that brain to mast cell connections account for stress-induced gastrointestinal symptoms. Degranulation of enteric mast cells by neural inputs releases inflammatory mediators that enhance excitability of intestinal secretomotor neurons while suppressing the release of norepinephrine from postganglionic sympathetic axons. This is postulated to underlie the secretory diarrhea and abdominal discomfort associated with stress.