Auditory Responses in Multiple Sensorimotor Song System Nuclei Are Co-Modulated by Behavioral State

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Abstract
Auditory responsiveness in nucleus HVC, a high-order sensorimotor area of the avian song system, is modulated by changes in behavioral state. Modulation is not observed in the primary thalamo-recipient auditory area Field L, the indirect source of auditory input to HVC. In this study, we show that auditory responsiveness in nucleus interfacialis (NIf), the immediate auditory afferent to HVC, is modulated by behavioral state. While auditory responsiveness is generally greater in NIf during wakefulness and in HVC during sedation, simultaneous recordings reveal a co-variation of auditory response magnitude. This co-variation is observed both in awake birds, where responses are spontaneously variable, and in sedated birds during manipulations of arousal levels. Auditory responses in NIf and HVC, which are selective for the bird's own song (BOS) during sedation, become predominantly unselective during wakefulness. This loss of selectivity is accompanied by a decrease in the similarity of NIf and HVC response patterns. To explore the role of NIf in shaping HVC auditory responses, we pharmacologically manipulated NIf while recording in HVC. Injection of the GABAAagonist muscimol into NIf eliminated most spontaneous activity and all auditory responses in the ipsilateral HVC, while injections of the GABAAantagonist bicuculline increased HVC auditory responsiveness and selectivity. These findings indicate that HVC is not the initial site of behavioral state–dependent modulation in the song system. Together with the suppression of HVC auditory responses by muscimol in NIf, these results suggest that NIf plays an important role in the flow of auditory information to HVC.