The neurobiological adaptations that enable humans and a few other species to communicate using learned vocal signals, e.g. speech, are not well understood. Imaging data have led to the proposal that speech is not only lateralized, but also processed both in an auditory (ventral, temporal) stream that serves acoustic object identification and in an auditory-motor (dorsal, frontal) stream that maps sounds onto pre-motor vocal areas. Neurobiological investigation of this proposal at the circuit level requires an established animal model that engages in vocal learning. The current project will use the songbird model to study the dual stream proposal in detail because 1) songbirds are the most easily studied of the very few animal taxa that learn to produce vocal signals for social communication as humans do;and 2) songs appear to be processed differently in two anatomically and functionally distinct areas of the songbird forebrain, as seems true for speech. We propose to develop a novel paradigm, using awake and behaving songbirds, to evaluate the effects of exposure history and behavioral salience on auditory processing by recording in both the auditory and vocal pre-motor areas, which may play an important role in perceptual processing of complex communication signals as well as in vocal production. To this end, we will manipulate behavioral salience before and during physiological recordings, using three approaches. 1) Birds will learn to discriminate the unique songs of other individuals in a behavioral paradigm, followed by acute multielectrode recording in auditory and motor structures bilaterally to test the effects of behavioral reinforcement on responses to training stimuli 2) Birds with chronically implanted electrodes that target auditory and motor structures will undergo discrimination training, enabling changes in sensory processing associated with behavioral learning to be studied in real time. 3) A novel method for combining discrimination training with acute neurophysiological recording in head-fixed birds will be developed. This will enable high quality simultaneous recording from different neural structures bilaterally during behavior, combining the strengths of the first two methods. The proposed work is significant in two ways. First, it aims to both exploit existing methods for collecting neural data from auditory areas during behavior and also to develop a novel paradigm for multielectrode recording from awake songbirds during performance of a discrimination task. This innovative approach will allow for real time assessment of the auditory processing that underlies the discrimination of relevant vocal communication signals. Second, these approaches will for the first time enable simultaneous recording during task performance from both sensory structures and the vocal motor pathway, which may have an important role in perceptual processing that is only revealed in a task context, as has been suggested by studies showing overlap of speech production and perceptual function. This will test the dual stream proposal and may reveal important principles relevant to both normal and abnormal speech processing.
Using an animal model of vocal learning that has many parallels with human speech acquisition, the proposed project will develop new methods and approaches to study 1) how experience and behavioral context change the way sounds are processed in the brain, and 2) how information that flows from auditory to vocal motor areas may contribute to perceptual processing. The results will be relevant to evaluating the dual stream hypothesis for speech processing. A better understanding of the brain mechanisms involved in decoding complex vocal signals, including contributions from the two hemispheres, may help in understanding and potentially treating auditory processing disorders in humans.