Dopaminergic modulation of mitral cells and odor responses in the zebrafish olfactory bulb

Abstract

In the olfactory bulb, the modulatory neurotransmitter dopamine (DA) is coexpressed with GABA by local interneurons, but its role in odor processing remains obscure. Weexamined functionsof DAmediatedby D 2-like receptorsinthe olfactory bulbofadult zebrafish by pharmacology, whole-cell recordings, calcium imaging, and optogenetics. Bath application of DA had no detectable effect on odorant-evoked sensory input. DA directly hyperpolarized mitral cells (MCs) via D 2-like receptors and slightly increased their response gain. Consistent with this effect on input-output functions of MCs, small odorant responses were suppressed, whereas strong responses were enhancedinthe presenceofDA. These effects increased the root-mean-square contrastofpopulation activity patterns but did not reduce their correlations. Optical stimulation of interneurons expressing channelrhodopsin-2 evoked fast GABAergic inhibitory currents in mitral cells but failed to activate D 2 receptor-mediated currents when stimuli were short. Prolonged stimulus trains, however, activated a slow hyperpolarizing current that was blocked by an antagonist of D 2-like receptors. GABA and DA are therefore both released from interneuronsbyelectrical activityandhyperpolarizeMCs,butD 2-dependent dopaminergic effects occuronslower timescales.Additional effects of DA may be mediated by D 1-like receptors. These results indicate that DA acts on D 2-like receptors via asynchronous release and/or volume transmission and implicate DA in the slow adaptation of circuit function. The shift of the membrane potential away from spike threshold could adapt mitral cells to background input without compromising their sensitivity. © 2012 the authors.