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GABA mediates autoreceptor feedback inhibition in the rat carotid body via presynaptic GABA_B receptors and TASK-1

Ian M. Fearon, Min Zhang, Cathy Vollmer and Colin A. Nurse

Background K⁺ channels exert control over neuronal excitability by regulating resting potential and input resistance. Here, we show that GABA_B receptor-mediated activation of a background K⁺ conductance modulates transmission at rat carotid body chemosensory synapses in vitro. Carotid body chemoreceptor (type I) cells expressed GABA_B(1) and GABA_B(2) subunits as well as endogenous GABA. The GABA_B receptor agonist baclofen activated an anandamide- and Ba²⁺-sensitive TASK-1-like background K⁺ conductance in chemoreceptor cell clusters, but was without effect on voltage-gated Ca²⁺ channels. Hydroxysaclofen (50 µM), 5-aminovaleric acid (100 µM) and CGP 55845 (100 nM), selective GABA_B receptor blockers, potentiated the hypoxia-induced receptor potential; this effect was abolished by pre-treatment with pertussis toxin (PTX; 500 ng ml^-1), an inhibitor of G_i, or by H-89 (50 µM), a selective inhibitor of protein kinase A. The protein kinase C inhibitor chelerythrine chloride (100 µM) was without effect on this potentiation. GABA_B receptor blockers also caused depolarisation of type I cells in clusters, and enhanced spike discharge in spontaneously firing cells. In functional co-cultures of type I clusters and petrosal sensory neurones, GABA_B receptor blockers potentiated hypoxia-induced postsynaptic chemosensory responses mediated by the fast-acting transmitters ACh and ATP. Thus GABA_B receptor-mediated activation of TASK-1 or a related channel provides a presynaptic autoregulatory feedback mechanism that modulates fast synaptic transmission in the rat carotid body.

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