Closed-Loop Control of Active Sensing Movements Regulates Sensory Slip.

ABSTRACT

Active sensing involves the production of motor signals for the purpose of acquiring sensory information [1-3]. The most common form of active sensing, found across animal taxa and behaviors, involves the generation of movements-e.g., whisking [4-6], touching [7, 8], sniffing [9, 10], and eye movements [11]. Active sensing movements profoundly affect the information carried by sensory feedback pathways [12-15] and are modulated by both top-down goals (e.g., measuring weight versus texture [1, 16]) and bottom-up stimuli (e.g., lights on or off [12]), but it remains unclear whether and how these movements are controlled in relation to the ongoing feedback they generate. To investigate the control of movements for active sensing, we created an experimental apparatus for freely swimming weakly electric fish, Eigenmannia virescens, that modulates the gain of reafferent feedback by adjusting the position of a refuge based on real-time videographic measurements of fish position. We discovered that fish robustly regulate sensory slip via closed-loop control of active sensing movements. Specifically, as fish performed the task of maintaining position inside the refuge [17-22], they dramatically up- or downregulated fore-aft active sensing movements in relation to a 4-fold change of experimentally modulated reafferent gain. These changes in swimming movements served to maintain a constant magnitude of sensory slip. The magnitude of sensory slip depended on the presence or absence of visual cues. These results indicate that fish use two controllers one that controls the acquisition of information by regulating feedback from active sensing movements and another that maintains position in the refuge, a control structure that may be ubiquitous in animals [23, 24].