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Extrabranchial chemoreceptors involved in respiratory reflexes in the neotropical fish Colossoma macropomum (the tambaqui)


1 Department of Zoology, University of British Columbia, 6270 University
Boulevard, Vancouver, British Columbia, Canada V6T 1Z4
2 Department of Physiological Sciences, Federal University of São
Carlos, 13565-905 São Carlos SP, Brazil
Present address: Physiology Division, Department of Medicine, University of
California, San Diego, La Jolla, CA 92093-0623, USA
Present address: Department of Zoophysiology, Göteborg University, Box
463S-405 30, Göteborg, Sweden
* e-mail: milsom{at}zoology.ubc.ca
Accepted 3 April 2002
In a previous study, complete denervation of the gills in the tambaqui Colossoma macropomum did not eliminate the increase in breathing amplitude seen during exposure of this species to hypoxia. The present study was designed to examine other sites of putative O2-sensitive receptors that could be involved in this reflex action. Superfusion of the exposed brain of decerebrate, spinalectomized fish did not reveal the presence of central chemoreceptors responsive to hyperoxic, hypoxic, hypercarbic, acidic or alkaline solutions. Subsequent central transection of cranial nerve IX and X, removing not only all innervation of the gills but also sensory input from the lateral-line, cardiac and visceral branches of the vagus nerve, did not eliminate the increase in breathing amplitude that remained following peripheral gill denervation alone. Administration of exogenous catecholamines (10 and 100 nmol kg-1 adrenaline) to fish with intact brains and minimal surgical preparation reduced both respiratory frequency and amplitude, suggesting that humoral release of adrenaline also could not be responsible for the increase in breathing amplitude that remained following gill denervation. Denervation of the mandibular branches of cranial nerve V and the opercular and palatine branches of cranial nerve VII in gill-denervated fish (either peripheral gill denervation or central section of cranial nerves IX and X), however, did eliminate the response. Thus, our data suggest that hypoxic and hyperoxic ventilatory responses as well as ventilatory responses to internal and external injections of NaCN in the tambaqui arise from O2-sensitive receptors in the orobranchial cavity innervated by cranial nerves V and VII and O2-sensitive receptors on the gills innervated by cranial nerves IX and X.
Our results also revealed the presence of receptors in the gills that account for all of the increase in ventilation amplitude and part of the increase in ventilation frequency during hyperoxic hypercarbia, a group or groups of receptors, which may be external to the orobranchial cavity (but not in the central nervous system), that contribute to the increase in ventilation frequency seen in response to hyperoxic hypercarbia and the possible presence of CO2-sensitive receptors that inhibit ventilation frequency, possibly in the olfactory epithelium.
Key words: fish, tambaqui, Colossoma macropomum, chemoreceptor, hypoxia, hypercapnia, ventilation, gills, orobranchial cavity, cranial nerve, catecholamine
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