Neurobiology and dynamics of Active Sensing

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ABSTRACT: Two key principles define the core conceptual framework of our Conte Center. First, most sensory input is actively acquired by a motor and/or attentional sampling routine; e.g., rather than staring blankly and hoping that something will “fall” into our gaze, we Actively Scan the visible environment with eye movements. Even when fixating, we can actively (albeit covertly) scan the environment by shifting attention. Corresponding “scanning” of the auditory environment uses the more covert attentional sampling strategy, but is no less active. As a result, Active Sensing (i.e., strategic, goal-driven sampling of inputs) is “predictive” in that, it is guided by the subject's expectations (theories, models), accumulated through species' evolution, and refined by individuals' experience. Its central tenet is that sensing and perceiving can be fully understood only in the context of subjects' ongoing, goal-directed information-gathering activities. Second, neuronal oscillatory dynamics are critical mechanistic components of normal brain operation. Neuronal oscillations reflect rhythmic fluctuations of neuron ensembles between high and low excitability states. Mounting evidence indicates that such rhythmic activity is essential to normal brain operations, and that its disruption contributes to neuropsychiatric disorders. The idea that Active Sensing incorporates neuronal rhythms as fundamental instruments of operation represents an ongoing paradigm shift in systems neuroscience. Our Center is unified by support Cores and a set of mechanistic (linking) hypotheses concerning the “instrumental” functions of neuronal rhythms at local and network scales. The Center integrates electrocorticographic (ECoG) studies in humans with intracortical recordings in monkeys and computational modeling. Our Specific Aims are: AIM 1 – Exploit ECoG's strengths of distributed sampling and direct human brain recording to define dynamical circuits of top-down control and coordination across cortical areas in Active Sensing. To gain a sample size appropriate for our purposes, we will pool subjects across 5 surgical epilepsy centers using a common set of Active Sensing tasks, and a common data format. AIM 2 – Use recordings in nonhuman primates to elucidate and extend ECoG findings in humans. Laminar field potential (FP), current source density (CSD) and multiunit activity (MUA) profiles, along with single unit recordings will be obtained from monkeys performing tasks identical to those studied in humans. AIM 3 – Develop iterative interactions between computational and empirical studies of circuit dynamics at local (cell assembly) and global (brain network) levels. Tracking specific neuronal dynamics from the global-network level in humans down to the cellular and cell ensemble levels in monkeys will yield novel and unique insights into mechanisms of active brain operation. Statistical and Computational modeling will allow rapid exploration of possibilities suggested by ECoG and related multielectrode studies in monkeys, and will help in building accurately representing and integrating our findings across local and global scales.