Surface Cooling Rapidly Induces Coordinated Activity in the Upper and Lower Airway Muscles of the Fetal Lamb in Utero

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Abstract
Stimulation of cutaneous thermoreceptors may be an important factor in the initiation of continuous breathing at birth. Maintenance of a patent airway is also important in the continuation of effective ventilation after birth, but whereas in the adult the principal pharyngeal dilator is the genioglossus muscle, in the fetus genioglossus phasic activity is not synchronous with that of the fetal diaphragm. To ascertain whether a cold stimulus that initiates continuous breathing would also induce synchronized inspiratory activity in the upper airway muscles of the fetus, we have cooled fetal lambs in utero and examined the response of the genioglossus and alae nasi muscles in relation to diaphragm activity. Deep regular breathing as recorded by diaphragmatic activity and tracheal pressure started within 1–102 s after cooling commenced and coordinated inspiratory activity was seen in the alae nasi within 2–356 s. Genioglossus activity became synchronized with that of the diaphragm within 11–356 s. Cooling was continued for 4 h but although in one fetus continuous breathing with associated inspiratory activity in the genioglossus and alae nasi muscles lasted throughout the 4-h period, in the others continuous breathing was not sustained and adaptation to the cold stimulus occurred after periods ranging from 27–218 min. The relationship between breathing, upper airway muscle activity, and sleep state passed through one or more different phases, including breathing through high voltage electrocortical activity, before the normal fetal pattern of episodic breathing restricted to the low voltage electrocortical state resumed. As breathing reverted to the normal fetal pattern, inspiratory activity was lost in the genioglossus. These observations suggest that afferent input arising from cutaneous thermoreceptors may be an important factor in initiating respiration at birth and in ensuring coordinated activity of the upper and lower airway and reducing the possibility of airway obstruction in the neonate.