Task Engagement in Songbird Auditory Forebrain

27 Sensory systems are dynamic. They must process a wide range of natural signals that facilitate 28 adaptive behaviors in a manner that depends on an organism’s constantly changing goals. A full 29 understanding of the sensory physiology that underlies adaptive natural behaviors must therefore 30 account for the activity of sensory systems in light of these behavioral goals. Here, we present a 31 novel technique that combines in vivo electrophysiological recording from awake, freely moving 32 songbirds with operant conditioning techniques that allow control over birds’ recognition of 33 conspecific song, a widespread natural behavior in songbirds. We show that engaging in a vocal 34 recognition task alters the response properties of neurons in the caudal mesopallium (CM), an 35 avian analogue of mammalian auditory cortex, in European starlings. Compared to awake, 36 passive listening, active engagement of subjects in an auditory recognition task results in neurons 37 responding to fewer song stimuli and a decrease in the trial-to-trial variability in their driven 38 firing rates. Mean firing rates also change during active recognition, but not uniformly. Relative 39 to non-engaged listening, active recognition causes increases in the driven firing rates in some 40 neurons, decreases in other neurons, and stimulus-specific changes in other neurons. These 41 changes lead to both an increase in stimulus selectivity, and an increase in the information 42 conveyed by the neurons about the animals’ behavioral task. This study demonstrates the 43 behavioral dependence of neural responses in the avian auditory forebrain, and introduces the 44 starling as a model for real-time monitoring of task-related neural processing of complex 45 auditory objects. 46 47