The brainstem esophagomotor network pattern generator: A rodent model

Abstract

The evidence reviewed in this essay supports the following working model of the central function generator for esophageal peristalsis in the rat: solitarial subnucleus centralis (NTSc) neurons operate in a dual capacity as esophagomotor reflex interneurons and as command neurons programming respective outputs from nucleus ambiguus compact formation (AMBc) motoneurons during secondary and primary peristalsis. In both conditions, there is a critical requirement for cholinergic input which enables NTSc neurons to generate the timed sequence of AMBc motoneuronal activity. In primary peristalsis, the cholinergic coupling mechanism is activated centrally, probably via projections from deglutitive premotor neurons to the parvicellular reticular formation and thence to the NTS. In reflex (or secondary) peristalsis, the cholinergic input could in part be generated by cholinergic vagal viscerosensory fibers innervating the esophagus. Postulated connections between NTS deglutitive neurons and the parvicellular cholinergic neurons of the intermediate reticular formation have yet to be demonstrated. Premotor input from NTSc to AMBc is generated by somatostatinergic and excitatory aminoacidergic neurons. Coactivation of both inputs by cholinergic afferents is necessary to generate esophagomotor output from AMBc neurons. The model under study is derived from investigations into central mechanisms governing striated muscle peristaltic activity. Whether the basic operational principles revealed thus far apply to peristaltic pattern generation in species with a smooth muscle esophagus, requires further investigation.

Enteric co-innervation of motor endplates in the esophagus: state of the art ten years after

“…The compact formation of the nucleus ambiguus is influenced from projections originating in the central subnucleus of the nucleus of the solitary tract (Cunningham and Sawchenko, 1989;Barrett et al, 1994;Lu and Bieger, 1998) that, in turn, receives vagal afferents from the esophagus (Ross et al, 1985;Altschuler et al, 1989). The peripheral processes of afferents from esophageal muscle form baskets around myenteric ganglia, so-called IGLEs (Rodrigo et al, 1975), which have been postulated (Neuhuber, 1987) and later shown to act as tension receptors (Zagorodnyuk and Brookes, 2000) thus closing a reflex loop for esophageal motor control (Cunningham and Sawchenko, 1990;Bieger, 1993;Lu and Bieger, 1998).…”

“…It is now well established, as originally postulated by Meltzer (Meltzer, 1899), that the sequential and rhythmic patterns of swallowing are organized by a central pattern generator. The central pattern generator was previously described as a swallowing center that can be subdivided into three systems: an afferent system corresponding to the central and peripheral inputs to the center; an efferent system corresponding to the outputs from the center, consisting of the various motoneuron pools involved in swallowing; and an organizing system corresponding to the interneuronal network that programs the motor pattern (for review see Roman and Gonella, 1987;Bieger, 1993;Conklin and Christensen, 1994;Jean, 2001). In the tubular esophagus the mechanisms of peristalsis control are different between striated and smooth muscle, yet the peristaltic contraction sweeps from one to the other without a detectable break.…”

Local differences in vagal afferent innervation of the rat esophagus are reflected by neurochemical differences at the level of the sensory ganglia and by different brainstem projections

“…The central subnucleus of the NTS is the location of premotor neurons projecting to the compact formation of the AMB (Cunningham and Sawchenko, 1989;Barret et al, 1994;Lu and Bieger, 1998). Axons from these neurons terminate on esophageal motor endplates (Bieger and Hopkins, 1987;, thus closing a reflex loop for esophageal motor control (Cunningham and Sawchenko, 1990;Bieger, 1993;Lu and Bieger, 1998).…”

Brainstem pathways responsible for oesophageal control of gastric motility and tone in the rat

“…Jean and his associates found that a dorsal medullary region (later identified through anatomical studies as the NSTc by Ross, 1981) and a ventral medullary region (later identified as the compact formation of the nucleus ambiguus; Gillis et al 1989;Bieger, 1993) were both activated during autonomous swallowing behaviours and following electrical stimulation of the superior laryngeal nerve (Jean, 1972(Jean, , 1984Bieger, 1993). …”