Simon, S.; Saha, S.; Munda, S.; Joby, J.; Cherian, T.; Jacob, G.; Das, J.; Bhadra, D.; Arun, S.

Natural behaviors are challenging to study because they involve large variations in sensory inputs and motor outputs across trials. Even the simple act of eating can involve seeing food from many angles and reaching for it differently each time. The prevailing view is that natural behaviors are more noisy compared to controlled tasks, and involve mixing of sensorimotor information. Alternatively, natural behaviors might elicit reliable neural signatures in high-level visual and motor regions which contain invariant representations, and involve correlated sensory and motor information that leads to apparent mixing. Here, we provide evidence for the latter possibility through wireless recordings in freely moving monkeys performing natural tasks as well as controlled screen tasks. During natural interactions with food, neural activity was decodable with striking fidelity, equivalent to that of food images. Key events during these interactions elicited distinct and reliable neural signatures that reflected the encoding priorities of each region. Visual and motor regions were clearly dissociated in screen tasks, but were dissociated only at specific events in the natural task. Neurons active while seeing food were reactivated during sleep. Taken together, our results reveal that reliable neural signatures in high-level sensory and motor regions form the neural substrates for natural behaviors.