The Coordination of Breathing and Swallowing Across the Human Lifespan: Implications for Neural Control
Thesis DisciplineHealth Sciences
Degree GrantorUniversity of Canterbury
Degree NameDoctor of Philosophy
Our understanding of the neural control of breathing-swallowing coordination (BSC) is largely unclear. Although brainstem control is undoubtedly predominant, this research investigated the hypothesis that the cortex becomes increasingly influential in BSC between birth and adulthood. The main paradigm used to test this primary hypothesis was a comparison of BSC in conditions along a continuum of volitional through non-volitional swallowing on the basis of a decreasing level of cortical activation along this continuum. Voluntarily-initiated swallows during wakefulness were at one end of the continuum and reflexively-initiated swallows during sleep were at the other extreme. Non-volitional wakeful swallows were considered between these two conditions. The BSC of ten infants between birth and 1 year of age and twenty adults between the ages of 20 and 75 years was recorded using non-invasive time-locked recording methods. In order to apply the 'continuum-of-volition' paradigm to swallowing conditions in infants, BSC was monitored during nutritive (breast- or bottle-feeding), non-nutritive wake, and sleep swallows. Infants were monitored longitudinally to determine whether maturation of the cortex and corticobulbar tracts during the first year of life influenced the patterns of BSC. In adults, BSC was monitored during three non-nutritive conditions: volitional, spontaneous wake, and sleep conditions. Post-swallow expiration was found to be predominant in all conditions for all participants at all ages. In addition, the infant results revealed that nutritive BSC matured during the first year of life and differed to non-nutritive wakeful BSC, particularly in the first 2 months of life. Non-nutritive wakeful and sleep BSC did not differ from one another. In summary, the infant results support increasing cortical input into volitional nutritive BSC, an early impact of feeding on BSC, and no difference between BSC when asleep and non-volitional non-nutritive swallows when awake. The results obtained from adults revealed that irrespective of the level of arousal, volitional BSC is different to non-volitional BSC. These results imply that cortical influence on BSC is limited to conditions in which swallowing is voluntarily initiated. The combined interpretation of infant and adult results suggest that cortical influence over BSC, although increasing with maturation, is limited to the volitional swallowing conditions of feeding in infants and during non-nutritive but volitional swallows in adults. From this, it can be deduced that the most likely cortical sites involved in BSC are those involved in the voluntary initiation or planning of swallowing. Infant and adult swallowing apnoea duration (SAD) was also compared across all of the above conditions. SAD was influenced by feeding throughout the first year of life but was not influenced by level of arousal at any stage in the first year or in adulthood. Also, SAD did not change with age in any swallowing condition during infancy. However, comparison of non-nutritive wake SAD across the lifespan revealed that SAD of newborns and young adults is shorter than that of elderly adults, with no difference between consecutive age-groups: newborns, one-year-olds, and young adults. These results suggest SAD is largely mature at birth and impervious to descending suprabulbar influence. Finally, the effects of volitional swallowing and level of arousal on peak submental surface electromyography (SEMG) was investigated in adults. Like BSC, submental muscle activity was influenced only by volitional swallowing, being longer for volitional than non-volitional swallows without being influenced by level of arousal. Since peak submental SEMG activity represents a measure of relative hyolaryngeal excursion, these results suggest that the cortex has some degree of influence over this particular feature of pharyngeal-stage swallowing.