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The role of midbrain tegmentum in the coordination of episodic breathing in carp (Cyprinus carpio) and rainbow trout (Oncorhynchus mykiss) O’Neill, Angela Elizabeth

Abstract

Because respiratory needs may vary due to activity level or oxygen availability, vertebrates must adjust their breathing to meet these changing levels of respiratory drive. In vertebrates, the basic respiratory rhythm is generated in the medulla; however, this rhythm is modified by both sensory feedback and input from higher centres to produce the broad range of vertebrate breathing patterns. In one such pattern, commonly produced during periods of reduced respiratory drive by some species in every vertebrate class, breaths are organized into groups (episodes) separated by periods without breathing (apneas). In carp, a site in the dorsal mesencephalic tegmentum, just ventrolateral to the oculomotor nucleus, appears to terminate apneas by initiating breathing episodes (Juch and Ballintijn, 1983). In order to test whether this site is necessary for the production of episodic breathing, I lesioned this midbrain tegmental site in decerebrate/spinalectomized carp (Cyprinus carpio) and trout (Oncorhynchus mykiss) using stereotaxic microinjections of 0.01mM kainic acid. Carp normally breathe episodically in normoxia and hyperoxia, while trout normally breathe continuously, only breathing episodically in extreme hyperoxia. Decerebrate/spinalectomized carp and trout breathed normally compared to intact fish in normoxia and hyperoxia, but not in severe hypoxia. Initially, the kainic acid provided a tonic stimulus which excited breathing; however, this stimulatory effect dissipated after approximately ninety minutes, when the kainic acid started killing neurons. In both carp and trout, lesioning this midbrain tegmental site altered the breathing pattern, increasing breathing frequency while decreasing amplitude such that total ventilation remained unchanged. The kainic acid microinjections eliminated apneas in fifty percent of carp (seven of fourteen) and reduced the occurrence of apneas in a further twenty-nine percent (four of fourteen). Histological analysis tentatively suggested that apneas were eliminated only in carp for which the kainic acid lesioned the midbrain tegmental site. Only four of nine trout breathed episodically, even in hyperoxia, and of these four trout, kainic acid eliminated apneas in one trout and reduced the occurrence of apneas in two others. This midbrain tegmental site does not normally influence the total level of respiratory drive, but does regulate breathing pattern, decreasing frequency and increasing amplitude. This site also appears to regulate episodic breathing in carp and trout; however, it is still unclear whether this site is essential to the production of this episodic pattern.

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