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J Physiol Volume 556, Number 1, 255-266, April 1, 2004 DOI: 10.1113/jphysiol.2003.058321
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Indirect sensing of insulin-induced hypoglycaemia by the carotid body in the rat

I. Bin-Jaliah, P. D. Maskell and P. Kumar

Department of Physiology, Division of Medical Sciences, The Medical School, University of Birmingham, Birmingham B15 2TT, UK

The most physiologically important sensors for systemic glucoregulation are located in extra-cranial sites. Recent evidence suggests that the carotid body may be one such site. We assessed rat carotid body afferent neural output in response to lowered glucose, indirectly by measurement of ventilation, and directly by recording single or few-fibre chemoafferent discharge, in vitro. Insulin (0.4Ukg–1min–1)-induced hypoglycaemia (blood glucose reduced by ca 50% to 3.4 ± 0.1mmoll–1) significantly increased spontaneous ventilation in sham-operated animals but not in bilateral carotid sinus nerve sectioned (CSNX) animals. In both groups, metabolic rate (measured as ) was almost doubled during hypoglycaemia. The ventilatory equivalent was unchanged in the sham group leading to a maintained control level of Pa, CO2, but was significantly reduced in the CSNX group, giving rise to an elevation of 6.0 ± 1.3mmHg in Pa, CO2. When pulmonary ventilation in sham animals was controlled and maintained, phrenic neural activity increased during hypoglycaemia and was associated with a significant increase in Pa, CO2 of 5.1 ± 0.5mmHg. Baseline chemoreceptor discharge frequency, recorded in vitro, was not affected, and did not increase when the superfusate [glucose] was lowered from 10 mM to 2 mM by substitution with sucrose: 0.40 ± 0.20 Hz to 0.27 ± 0.15Hz, respectively (P > 0.20). We suggest therefore that any potential role of the carotid bodies in glucose homeostasis in vivo is mediated through its transduction of some other metabolically derived blood-borne factor rather than glucose per se and that this may also provide the link between exercise, metabolic rate and ventilation.

(Received 18 November 2003; accepted after revision 22 January 2004; first published online 23 January 2004)
Corresponding author P. Kumar: Department of Physiology, Division of Medical Sciences, The Medical School, University of Birmingham, Birmingham B15 2TT, UK.  Email: p.kumar{at}bham.ac.uk




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