Subthreshold membrane responses underlying sparse spiking to natural vocal signals in auditory cortex

Natural acoustic communication signals, such as speech, are typically high‐dimensional with a wide range of co‐varying spectro‐temporal features at multiple timescales. The synaptic and network mechanisms for encoding these complex signals are largely unknown. We are investigating these mechanisms in high‐level sensory regions of the songbird auditory forebrain, where single neurons show sparse, object‐selective spiking responses to conspecific songs. Using whole‐cell in vivo patch clamp techniques in the caudal mesopallium and the caudal nidopallium of starlings, we examine song‐driven subthreshold and spiking activity. We find that both the subthreshold and the spiking activity are reliable (i.e. the same song drives a similar response each time it is presented) and specific (i.e. responses to different songs are distinct). Surprisingly, however, the reliability and specificity of the subthreshold response was uniformly high regardless of when the cell spiked, even for song stimuli that drove no spikes. We conclude that despite a selective and sparse spiking response, high‐level auditory cortical neurons are under continuous, non‐selective, stimulus‐specific synaptic control. To investigate the role of local network inhibition in this synaptic control, we then recorded extracellularly while pharmacologically blocking local GABA ergic transmission. This manipulation modulated the strength and the reliability of stimulus‐driven spiking, consistent with a role for local inhibition in regulating the reliability of network activity and the stimulus specificity of the subthreshold response in single cells. We discuss these results in the context of underlying computations that could generate sparse, stimulus‐selective spiking responses, and models for hierarchical pooling.