Brain Stem Control of Swallowing: Neuronal Network and Cellular Mechanisms

Abstract

Swallowing movements are produced by a central pattern generator located in the medulla oblongata. It has been established on the basis of microelectrode recordings that the swallowing network includes two main groups of neurons. One group is located within the dorsal medulla and contains the generator neurons involved in triggering, shaping, and timing the sequential or rhythmic swallowing pattern. Interestingly, these generator neurons are situated within a primary sensory relay, that is, the nucleus tractus solitarii. The second group is located in the ventrolateral medulla and contains switching neurons, which distribute the swallowing drive to the various pools of motoneurons involved in swallowing. This review focuses on the brain stem mechanisms underlying the generation of sequential and rhythmic swallowing movements. It analyzes the neuronal circuitry, the cellular properties of neurons, and the neurotransmitters possibly involved, as well as the peripheral and central inputs which shape the output of the network appropriately so that the swallowing movements correspond to the bolus to be swallowed. The mechanisms possibly involved in pattern generation and the possible flexibility of the swallowing central pattern generator are discussed.

Characterization of neurons of the nucleus tractus solitarius pars centralis

“…The subnuclei of the NTS are viscerotopically organized [1,2,5]; however, the same subnucleus might receive sensory information from more than one peripheral organ [1,[5][6][7]11,16,22,25,30]. The subnucleus centralis (cNTS), however, receives sensory inputs originating almost exclusively from esophageal afferent fibers [1,8,9,16,23], thus, this nucleus may be a possible model for the study of NTS neurons devoted to the control of esophagus-mediated reflexes.…”

“…This reduced heterogeneity of morphological features may be ascribed to the relatively homogeneous sensory input from esophagus impinging on the cNTS [1,6,8,16,27].…”

“…Although sensory inputs from distinct peripheral organs, such as, for example, the aortic branch and the stomach, do not converge on single NTS neurons [26], the same subnucleus may receive sensory information from more than one peripheral organ. For example, neurons involved in arterial baroreflex circuits as well as neurons part of vago-vagal gastric reflexes are similarly located in the medial subnucleus of the NTS [1,[5][6][7]11,16,22,25,30]. The overlap of these viscerotopically organized areas makes the distinction of cells devoted to a particular function quite problematic, even though a recent report suggested that innovative techniques may be used to distinguish NTS neurons receiving discrete projections in a brainstem slice preparation [13].…”

“…The overlap of these viscerotopically organized areas makes the distinction of cells devoted to a particular function quite problematic, even though a recent report suggested that innovative techniques may be used to distinguish NTS neurons receiving discrete projections in a brainstem slice preparation [13]. The subnucleus centralis (cNTS), which is located adjacent to the tractus solitarius [5], receives inputs from vagal afferent fibers originating almost exclusively from the esophagus [1,6,8,16,27], making it an excellent model for the study of a population of second order neurons controlling esophageal-mediated reflexes.…”

“…A vast array of studies have shown that sensory vagal information to NTS neurons is excitatory and uses, principally, excitatory amino acids such as glutamate [3,[14][15][16][17]21,23,29,33]. Lu and Bieger recently reported that glutamate was the neurotransmitter mediating fast excitatory neurotransmission from vagal afferent fibers to cNTS neurons [23]; however, they did not characterize the glutamatergic receptors subtype(s) involved.…”