Reflex response and convergence of pharyngoesophageal and peripheral chemoreceptors in the nucleus of the solitary tract.
The pharynx is a common conduit for the passage of both ingested material and respiratory gases and may receive a dual control from medullary structures regulating deglutition and respiration. We sought both to compare the pattern of reflex response following stimulation of pharyngoesophageal and peripheral chemoreceptors and to assess whether these afferents converge in the nucleus of the solitary tract. In an arterially perfused working heart-brainstem preparation of mature rat, pharyngoesophageal receptors were stimulated by distension of the pharyngeal-oesophageal junction, whereas chemoreceptors were activated by sodium cyanide solution. In peripheral studies we recorded electromyographic activity from genioglossus, mylohyoideus and the lower thoracic oesophagus as well as hypoglossal, laryngeal and phrenic motor discharge. Sub-glottal pressure was also measured at constant airflow. In central studies, nucleus of the solitary tract neurons were recorded with blind whole-cell techniques. In peripheral studies spontaneous irregular electromyographic discharges (cycle length 99+/-26 s) occurred sequentially in genioglossus and mylohyoideus muscles (during the inter-phrenic nerve activity interval) and subsequently the oesophagus; these were accompanied by post-inspiratory discharges in both hypoglossal and laryngeal motor nerves and an atropine-sensitive bradycardia (-39+/-5 beats/min). Components of the reflex response elicited following stimulation of both pharyngoesophageal receptors and chemoreceptors were qualitatively similar and included: (i) expiratory-related increases in laryngeal pressure; (ii) sequential electromyographic discharge in genioglossus, mylohyoideus muscles and oesophagus; (iii) post-inspiratory burst discharge in hypoglossal, recurrent and superior laryngeal motor nerves; and (iv) an atropine-sensitive bradycardia (-38 to -95 beats/min). The chemoreceptor reflex-evoked responses were abolished after sinoaortic denervation. Of 135 whole-cell recordings of nucleus of the solitary tract neurons, 31 received a synaptic input from pharyngoesophageal receptors (22 excitatory and nine inhibitory). Cells excited by pharyngoesophageal receptor stimulation were either "spontaneously" bursting, which occurred during the inter-phrenic nerve activity interval (cycle length 79+/-22 s; n=9), or non-bursting (n=13). Of the 22 nucleus of the solitary tract neurons excited by pharyngoesophageal receptor stimulation, 77% received a convergent excitatory synaptic input from chemoreceptors (eight bursting and nine non-bursting neurons). Thus, stimulation of pharyngoesophageal receptors and chemoreceptors evoked common reflex response components including activation of hypoglossal, laryngeal adductor, cardiac vagal motoneurons and swallowing. Moreover, some excitatory pharyngoesophageal and chemoreceptors inputs typically converged on nucleus of the solitary tract neurons. The possibility that this convergence manifests a defensive reflex reaction is discussed.
Paton
J F
JF
Department of Physiology, School of Medical Sciences, University of Bristol, UK.
Li
Y W
YW
Kasparov
S
S
D000818:Animals; D001933:Brain Stem / Q000502:physiology; D002628:Chemoreceptor Cells / Q000502:physiology*; D004558:Electric Stimulation; D004576:Electromyography; D004594:Electrophysiology; D004947:Esophagus / Q000294:innervation / Q000502:physiology*; D006321:Heart / Q000502:physiology; D006439:Hemodynamics / Q000502:physiology; D008297:Male; D008564:Membrane Potentials / Q000502:physiology; D009119:Muscle Contraction / Q000502:physiology; D018408:Patch-Clamp Techniques; D010477:Perfusion; D017933:Peripheral Nervous System / Q000166:cytology / Q000502:physiology*; D010614:Pharynx / Q000294:innervation / Q000502:physiology*; D051381:Rats; D017207:Rats, Sprague-Dawley; D012018:Reflex / Q000502:physiology*; D017552:Solitary Nucleus / Q000166:cytology / Q000502:physiology*