Functional Connectivity Between Auditory Areas Field L and CLM and Song System Nucleus HVC in Anesthetized Zebra Finches

Abstract

A key discovery that has emerged from studies of the vocal system in songbirds is that neurons in these regions respond preferentially to playback of the bird's own song (BOS). This BOS selectivity is not a general property of neurons in primary and secondary auditory forebrain regions, field L and caudolateral mesopallium (CLM). Moreover, anatomical studies have been unable to conclusively define a direct projection from field L and/or CLM to HVC, a central structure for integrating sensory and motor information in the vocal system. To examine the communication between these regions, we used simultaneous dual-electrode recording in anesthetized male zebra finches and cross-correlation analysis to estimate the functional connectivity between auditory areas, field L and CLM, and HVC. We found that ≥18% of neurons in field L and 33% of neurons in CLM are functionally connected to HVC, most with auditory forebrain leading-HVC latencies ranging from 0.5 to 15 ms. These results indicate that field L and CLM communicate extensively with HVC through both direct and indirect anatomical connections. To further explore the role of the auditory forebrain cells that are functionally connected with HVC, we assessed their responsiveness and selectivity for a variety of natural and synthetic auditory stimuli. We found that field L and CLM neurons that are functionally connected to HVC exhibit generic auditory forebrain properties including the lack of BOS selectivity. This finding puts further constraints on the neural architecture and the nature of the nonlinearity that leads to BOS-selective auditory responses in the vocal control nuclei.