Synaptic Mechanisms of Direction Selectivity in Primary Auditory Cortex

Frequency modulation (FM) is a prominent feature in animal vocalization and human speech. Although many neurons in the auditory cortex are known to be selective for FM direction, the synaptic mechanisms underlying this selectivity are not well understood. Previous studies of both visual and auditory neurons have suggested two general mechanisms for direction selectivity: (1) differential delays of excitatory inputs across the spatial/spectral receptive field and (2) spatial/spectral offset between excitatory and inhibitory inputs. In this study, we have examined the contributions of both mechanisms to FM direction selectivity in rat primary auditory cortex. The excitatory and inhibitory synaptic inputs to each cortical neuron were measured by in vivo whole-cell recording. The spectrotemporal receptive field of each type of inputs was mapped with random tone pips and compared with direction selectivity of the neuron measured with FM stimuli. We found that both the differential delay of the excitatory input and the spectral offset between excitation and inhibition are positively correlated with direction selectivity of the neuron. Thus, both synaptic mechanisms are likely to contribute to FM direction selectivity in the auditory cortex. Finally, direction selectivity measured from the spiking output is significantly stronger than that based on the subthreshold membrane potentials, indicating that the selectivity is further sharpened by the spike generation mechanism.