Hierarchical circuits in the ventral auditory pathway

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Although there is a rich history relating single-neuron spiking activity to brain function, our understanding of the neural bases of perception and behavior depends on identifying information processing within neuronal circuits that operate over different spatial scales. Despite their importance as a canonical model of information flow, our understanding of whether and how such bidirectional hierarchically organized circuits contribute to auditory perception remains elusive, especially in primate models of hearing. The overarching goal of this Roi proposal is to fill this knowledge gap by identifying bidirectional, hierarchically organized circuits that contribute to auditory perception. We will use predictive coding (PC) -a highly influential theoretical framework for auditory statistical learning and perceptual inference- as an experimental lever to test whether its predictions are instantiated in cortical circuits of the ventral auditory pathway. We focus on the ventral pathway because, in rhesus monkeys, this pathway contributes causally to auditory perception. To test the circuit predictions of PC, we insert multi-contact electrode(s) orthogonally to the cortical laminae and record single-unit and neuronalpopulation activity in the core auditory cortex and in the ventral auditory pathway While recording, rhesus monkeys participate in passive listening paradigms and an active listening task. During passive listening, monkeys listen to sequences of auditory stimuli containing both predictable and unpredictable events, which allow probes of prediction-error and prediction-related activity. During active listening, monkeys implicitly learn to use auditory cues to predict the onset of an auditory target; this task is a direct behavioral assessment of the strength and temporal dynamics of auditory statistical learning. In Specific Aim #1, we identify the interlaminar circuitry underlying PC and its hierarchical organization along the ventral auditory pathway. In Specific Aim #2, we identify the feedforward and feedback circuitry between the prefrontal and auditory cortices that underlies PC. The findings from this proposal will provide invaluable insights into the functional organization of cortical circuits underlying PC and statistical learning along the ventral auditory pathway. In turn, these insights may lead to the formulation of testable hypotheses regarding the neurophysiological underpinnings of deficits in statistical learning that have been identified in clinical conditions such as autism and schizophrenia.