’What’ and ‘where’ brain-wide pathways are dominated by internal strategies

It is long thought that higher-order sensory processing is divided into two specialized cortical streams that encode in parallel either the identity of an object or its location (i.e., ‘what’ and ‘where’ streams). Here, using the mouse whisker system, we challenge this concept by demonstrating an existence of two alternating brain-wide (beyond cortex) subnetworks that are not primarily driven by external parameters, but rather by internal strategies. We combine simultaneous brain-wide neuronal recordings in mice trained to identify or locate a certain stimulus. We find that mice deploy either an active search or a passive sensation strategy during task performance. These strategies respectively drive two distinct and brain-wide subnetworks, frontal and posterior, regardless of the type of task performed. The posterior subnetwork encoded additional internal strategic parameters such as trial history, the first task of the day, and training history. A subgroup of trials that were not dominated by frontal cortex, contained meaningful task information in the posterior cortex and several thalamic areas. Integrated together, these two subnetworks may comprise normal cognitive function.