Sensory Cues Modulate Smooth Pursuit and Active Sensing Movements

Abstract

Animals routinely use autogenous movement to regulate the information encoded by their sensory systems. Weakly electric fish use fore–aft movements to regulate visual and electrosensory feedback as they maintain position within a moving refuge. During refuge tracking, fish produce two categories of movements: smooth pursuit that is approximately linear in its relation to the movement of the refuge and ancillary active sensing movements that are nonlinear. We identified four categories of nonlinear movements which we termed scanning, wiggle, drift, and reset. To examine the relations between sensory cues and production of both linear smooth pursuit and nonlinear active sensing movements, we altered visual and electrosensory cues for refuge tracking and measured the fore–aft movements of the fish. Specifically, we altered the length and structure of the refuge and performed experiments with light and in complete darkness. Linear measures of tracking performance were better for shorter refuges (less than a body length) than longer ones (>1.5 body lengths). The magnitude of nonlinear active sensing movements was strongly modulated by light cues but also increased as a function of both longer refuge length and decreased features. Specifically, fish shifted swimming movements from smooth pursuit to scanning when tracking in dark conditions. Finally, fish appear to use nonlinear movements as an alternate tracking strategy in longer refuges: the fish may use more drifts and resets to avoid exiting the ends of the refuge.

Mutually promoting or constraining? Disentangling the superimposed effect of velocity and illuminance on fish motion in low‐velocity flows with a novel metric

“…We further studied the optically relevant effects by examining the v of the test individuals because swimming speed can timely represent the real‐time biological status of fish. The evidence from zebrafish ( Danio rerio ) denoted that evoked anxiety could be characterised by faster swimming with spontaneous rapid turns and increased maximum swimming speed (Egan et al, 2009; Pozo Cano & Sánchez Vázquez, 2015), while the fish also used the active longitudinal movement to locate positions in case of refuge tracking (Uyanik et al, 2019). In this study, the dissimilar light‐induced accelerated swimming of the two species possibly originated from different physiological mechanisms.…”

Organisms use mode-switching to solve the explore-vs-exploit problem

“…A key difference would be that the signal in question would arise from an internal representation of sensory uncertainty, rather than overall level of sensory excitation. Such a reflex-like action could produce stereotyped forms of interactions with the external environment in relation to sensing [14].…”

“…For example, neurophysiological recordings show that sensory salience can be encoded in brain circuits via synchronization and desynchronization of spiking activity [39]. Such population coding of salience [40][41][42], when coupled with a threshold, could trigger discrete bursts of motor activity for sensing [14]. Motor circuits for the production of discrete bursts of movement occur in spinal circuits [43].…”

“…The experimental apparatus was similar to that used in previous studies [2,[10][11][12]14]. See [2] for more detailed description of the apparatus.…”

“…and goal-driven exploitative movements [10,13] using the same locomotor system [14,15]. Critically, this behavior illustrates how explore and exploit movements are often in conflict with one another: fish produce back-and-forth exploratory movements [2,3,9] to detect and maintain their position within a stationary refuge.…”