Long-range inhibition within the zebra finch song nucleus RA can coordinate the firing of multiple projection neurons

The zebra finch forebrain song control nucleus RA (robust nucleus of the ar chistriatum) generates a phasic and temporally precise neural signal that d rives vocal and respiratory motoneurons during singing. RA's output during singing predicts individual notes, even though afferent drive to RA from th e song nucleus HVc is more tonic, and predicts song syllables, independent of the particular notes that comprise the syllable. Therefore RA's intrinsi c circuitry transforms neural activity from HVc into a highly precise premo tor output. To understand how RA's intrinsic circuitry effects this transfo rmation, we characterized RA interneurons and projection neurons using intr acellular recordings in brain slices. RA interneurons fired fast action pot entials with steep current-frequency relationships and had small somata wit h thin aspinous processes that extended throughout large portions of the nu cleus; the similarity of their fine processes to those labeled with a gluta mic acid decarboxylase (GAD) antibody strongly suggests that these interneu rons are GABAergic. Electrical stimulation revealed that RA interneurons re ceive excitatory inputs from RA's afferents, the lateral magnocellular nucl eus of the anterior neostriatum (LMAN) and HVc, and from local axon collate rals of RA projection neurons. To map the functional connections that RA in terneurons make onto RA projection neurons, we focally uncaged glutamate, r evealing long-range inhibitory connections in RA. Thus these interneurons p rovide fast feed-forward and feedback inhibition to RA projection neurons a nd could help create the phasic pattern of bursts and pauses that character izes RA output during singing. Furthermore, selectively activating the inhi bitory network phase locks the firing of otherwise unconnected pairs of pro jection neurons: suggesting that local inhibition could coordinate RA outpu t during singing.