A role for sensory areas in coordinating active sensing motions
Schroeder, Joseph Bradley
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Active sensing, which incorporates closed-loop behavioral selection of information during sensory acquisition, is an important feature of many sensory modalities. We used the rodent whisker tactile system as a platform for studying the role cortical sensory areas play in coordinating active sensing motions. We examined head and whisker motions of freely moving mice performing a tactile search for a randomly located reward, and found that mice select from a diverse range of available active sensing strategies. In particular, mice selectively employed a strategy we term contact maintenance, where whisking is modulated to counteract head motion and sustain repeated contacts, but only when doing so is likely to be useful for obtaining reward. The context dependent selection of sensing strategies, along with the observation of whisker repositioning prior to head motion, suggests the possibility of higher level control, beyond simple reflexive mechanisms. In order to further investigate a possible role for primary somatosensory cortex (SI) in coordinating whisk-by-whisk motion, we delivered closed-loop optogenetic feedback to SI, time locked to whisker motions estimated through facial electromyography. We found that stimulation regularized whisking (increasing overall periodicity), and shifted whisking frequency, changes that emulate behaviors of rodents actively contacting objects. Importantly, we observed changes to whisk timing only for stimulation locked to whisker protractions, possibly encoding that natural contacts are more likely during forward motion of the whiskers. Simultaneous neural recordings from SI show cyclic changes in excitability, specifically that responses to excitatory stimulation locked to whisker retractions appeared suppressed in contrast to stimulation during protractions that resulted in changes to whisk timing. Both effects are evident within single whisks. These findings support a role for sensory cortex in guiding whisk-by-whisk motor outputs, but suggest a coupling that depends on behavioral context, occurring on multiple timescales. Elucidating a role for sensory cortex in motor outputs is important to understanding active sensing, and may further provide novel insights to guide the design of sensory neuroprostheses that exploit active sensing context.