Abstract
This research was designed to investigate the role of the anterior ethmoidal nerve (AEN) during repetitive trained diving in rats, with specific attention to activation of afferent and efferent brainstem nuclei that are part of this reflexive response. The AEN innervates the nose and nasal passages and is thought to be an important component of the afferent limb of the diving response. Male Sprague-Dawley rats (N = 24) were trained to swim and dive through a 5 m underwater maze. Some rats (N = 12) had bilateral sectioning of the AEN, others a Sham surgery (N = 12). Twelve rats (6 AEN cut and 6 Sham) had 24 post-surgical dive trials over 2 h to activate brainstem neurons to produce Fos, a neuronal activation marker. Remaining rats were non-diving controls. Diving animals had significantly more Fos-positive neurons than non-diving animals in the caudal pressor area, ventral medullary dorsal horn, ventral paratrigeminal nucleus, nucleus tractus solitarius, rostral ventrolateral medulla, Raphe nuclei, A5, Locus Coeruleus, and Kölliker-Fuse area. There were no significant differences in brainstem Fos labeling in rats diving with and without intact AENs. Thus, the AENs are not required for initiation of the diving response. Other nerve(s) that innervate the nose and nasal passages, and/or suprabulbar activation of brainstem neurons, may be responsible for the pattern of neuronal activation observed during repetitive trained diving in rats. These results help define the central neuronal circuitry of the mammalian diving response.
Highlights
A reflexive response to diving in mammals is triggered when, upon submersion, the nerves innervating the nose and nasal passages are stimulated with water (Butler and Jones, 1997; McCulloch, 2012; Panneton, 2013)
We found that in rats both with and without intact anterior ethmoidal nerve (AEN) there is a significant increase in Fos labeling within the ventral medullary dorsal horn (MDH) and paratrigeminal nuclei during repetitive diving
Our results showed two areas of the brainstem involved in the afferent aspects of the diving response circuitry, the ventral superficial MDH and ventral paratrigeminal nucleus, had significant increases in Fos expression in rats with bilaterally sectioned AENs compared with their non-diving controls
Summary
A reflexive response to diving in mammals is triggered when, upon submersion, the nerves innervating the nose and nasal passages are stimulated with water (Butler and Jones, 1997; McCulloch, 2012; Panneton, 2013). This nasal stimulation initiates significant cardiorespiratory changes that inhibit basic homeostatic reflexes, such as baroreceptor and chemoreceptor reflexes. The central terminal projections of the AEN release glutamate (McCulloch et al, 2013) to activate secondary neurons within the ventral MDH and adjacent paratrigeminal nuclei The activation of these secondary neurons in turn, activates other brainstem neurons responsible for the efferent aspects of the diving response. Neurons in the caudal pressor area (CPA), nucleus of the solitary tract (NTS), raphe nuclei (Ra), rostrolventrolateral medulla (RVLM), catecholaminergic regions (A1, A2, A5, C1, and C2), locus coeruleus (LC), Kölliker-Fuse area (KF), and Parabrachial nucleus (PB) all show an increase in Fos expression during repetitive diving in rats trained to voluntarily swim underwater (McCulloch and Panneton, 2003; Panneton et al, 2010a, 2012a, 2014)
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