Active sensing involves the production of motor signals for the purpose of acquiring sensory information [1][2][3]. The most common form of active sensing, found across animal taxa and behaviors, involves the generation of movements-e.g. whisking [4][5][6], touching [7,8], sniffing [9,10], and eye movements [11]. Active-sensing movements profoundly affect the information carried by sensory feedback pathways [12][13][14][15] and are modulated by both top-down goals (e.g. measuring weight vs. texture [1,16]) and bottom-up stimuli (e.g. lights on/off [12]) but it remains unclear if 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 activesensing movements. Specifically, as fish performed the task of maintaining position inside the refuge [17][18][19][20][21][22], they dramatically up-or down-regulated 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].
Results
Active sensing is modulated by reafferent gainIn active sensing, an animal stimulates and/or regulates the information available to its own sensory systems via movement or, in a handful of specialized animals, via the generation of sensory signals such as electric fields or echolocation calls [25][26][27][28]. A hallmark of active sensing is that it is modulated in relation to changes in behavioral or sensory context. For example, as the weakly electric fish Eigenmannia virescens maintains its position within a refuge, it also produces small fore-aft body movements for active sensing [12]. These movements create a dynamic difference between the position of the fish and the refuge, i.e. a sensory slip analogous to retinal slip [23,29], albeit mediated by the propagation of electricity in water [28]. Active swimming movements in electric fishes likely prevent perceptual fading and enhance spatiotemporal patterns of sensory feedback [12,13,30] serving a similar role as small eye movements in vision [15,30,31].
