Fictive Gill and Lung Ventilation in the Pre- and Postmetamorphic Tadpole Brain Stem

Torgerson, C. S., M. J. Gdovin, and J. E. Remmers. Fictive gill and lung ventilation in the pre- and postmetamorphic tadpole brain stem. J. Neurophysiol. 80: 2015–2022, 1998. The pattern of efferent neural activity recorded from the isolated brain stem preparation of the tadpole Rana catesbeiana was examined to characterize fictive gill and lung ventilations during ontogeny. In vitro recordings from cranial nerve (CN) roots V, VII, and X and spinal nerve (SN) root II of premetamorphic tadpoles showed a coordinated sequence of rhythmic bursts occurring in one of two patterns, pattern1, high-frequency, low-amplitude bursts lacking corresponding activity in SN II and pattern 2, low-frequency, high-amplitude bursts with coincident bursts in SN II. These two patterns corresponded to gill and lung ventilatory burst patterns, respectively, recorded from nerve roots of decerebrate, spontaneously breathing tadpoles. Similar patterns were observed in brain stem preparations from postmetamorphic tadpoles except that they showed a greater frequency of lung bursts and they expressed fictive gill ventilation in SN II. The laryngeal branch of the vagus (Xl) displayed efferent bursts in phase with gill and lung activity, suggesting fictive glottal constriction during gill ventilation and glottal dilation during lung ventilation. The fictive gill ventilatory cycle of pre- and postmetamorphic tadpoles was characterized by a rostral to caudal sequence of CN bursts. The fictive lung ventilatory pattern in the premetamorphic animal was initiated by augmenting CN VII discharge followed by synchronous bursts in CN V, X, SN II, and Xl. By contrast, postmetamorphic patterns of fictive lung ventilation were characterized by lung burst activity in SN II that preceded burst onset in CN V and followed the lead burst in CN VII. We conclude that recruitment and timing of pattern 1 and pattern 2 rhythmic bursts recorded in vitro closely resemble that recorded during spontaneous respiratory behavior, indicating that the two patterns are the neural equivalent of gill and lung ventilation, respectively. Further, fictive gill and lung ventilatory patterns in postmetamorphic tadpoles differ in burst onset latency from premetamorphic tadpole patterns and resemble fictive oropharyngeal and pulmonary burst cycles in adult frogs.</jats:p

Ontogeny of Central Chemoreception During Fictive Gill and Lung Ventilation in an <i>In Vitro</i> Brainstem Preparation of <i>Rana Catesbeiana</i>

ABSTRACT An isolated brainstem preparation of the bullfrog tadpole, Rana catesbeiana, displays coordinated rhythmic bursting activities in cranial nerves V, VII and X in vitro. In decerebrate, spontaneously breathing tadpoles, we have previously shown that these bursts correspond to fluctuations in buccal and lung pressures and to bursts of activity in the buccal levator muscle H3a. This demonstrates that the rhythmic bursting activities recorded in vitro represent fictive gill and lung ventilation. To investigate the ontogeny of central respiratory chemoreception during the transition from gill to lung ventilation, we superfused the isolated brainstems of four larval stage groups with oxygenated artificial cerebrospinal fluid at various levels of . We measured shifts in the pattern of fictive respiratory output and the response to central hypercapnic stimulation throughout development. At normal (2.3 kPa), stage 3–9 tadpoles displayed rhythmic neural bursts associated with gill ventilation, while stages 10–14 and 15–19 tadpoles produced oscillating bursting activity associated with both gill and lung respiration, and tadpoles at stages 20–25 displayed neural activity predominantly associated with lung ventilation. In stage 3–9 tadpoles, variations in of the superfusate (0.5–6.0 kPa) caused almost no change in fictive gill or lung ventilation. By contrast, stage 10–14 tadpoles showed a significant hypercapnic response (P&amp;lt;0.05) in the amplitude and frequency of fictive gill ventilation, which was accompanied by a significant increase (P&amp;lt;0.05) in the burst amplitude and respiratory output of cranial nerve X over that occurring at all other stages. The amplitude and frequency of fictive gill ventilation in stages 15–19 increased significantly (P&amp;lt;0.05) in response to pH reduction, but became insensitive to hypercapnia at stages 20–25. The frequency of fictive lung ventilation was unresponsive to hypercapnia in stage 10–14, increased significantly by stage 15–19 (P&amp;lt;0.05) and became maximal (P&amp;lt;0.05) in stages 20–25. Overall, we describe the ontological development of central respiratory chemoreceptors driving respiratory output in the larval amphibian, demonstrating transfer in central chemoreceptive influence from gill to lung regulation during metamorphic stages. In addition, we provide novel evidence for the stimulatory influence of central chemoreceptors on fictive gill ventilation in response to CO2.</jats:p