Circadian pacemaker neurons of the Madeira cockroach are inhibited and activated by GABAA and GABAB receptors

Abstract

GABA is the most abundant neurotransmitter in the circadian pacemaker circuits of mammals and insects. In the Madeira cockroach the accessory medulla (AME) in the brain′s optic lobes is the circadian clock that orchestrates rest‐activity rhythms in synchrony with light dark cycles. Three prominent GABAergic tracts connect the AME to termination sites of compound eye photoreceptors in the lamina and medulla. Parallel GABAergic light entrainment pathways were suggested to either advance or delay the clock for adjustment to changing photoperiods. In agreement with this hypothesis GABA activated or inhibited AME clock neurons, allowing for distinction of three different GABA response types. Here, we examined which GABA receptors are responsible for these response types. We found that both ionotropic GABA_A receptors and metabotropic GABA_B receptors were expressed in AME clock cells. Via different signaling pathways, either one of them could account for all three GABA response types. The muscimol‐dependently activated GABA_A receptor formed a chloride channel, while the SKF 97541‐dependently activated GABA_B receptor signaled via G‐proteins, apparently targeting potassium channels. Expression of chloride exporters or –importers determined whether GABA_A receptor activation hyper‐ or depolarized AME neurons. For GABA_B receptor responses second messenger gated channels present in the clock cells appeared to decide about the polarity of the GABA response. In summary, circadian clock neurons co‐expressed inhibitory and/or excitatory GABA_A and GABA_B receptors in various combinations, while cotransporter expression and the set of second messenger gated ion channels present allowed for distinct signaling in different clock neurons.

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