Control algorithms underlying the translational optomotor response

Abstract

The optomotor response (OMR) is central to the locomotory behavior in diverse animal species including insects, fish and mammals. Furthermore, the study of the OMR in larval zebrafish has become a key model system for investigating the neural basis of sensorimotor control. However, a comprehensive understanding of the underlying control algorithms is still outstanding. In fish it is often assumed that the OMR, by reducing average optic flow across the retina, serves to stabilize position with respect to the ground. Yet the degree to which this assumption is true, and how this could emerge from the intermittent burst dynamics of larval zebrafish swimming is unclear. Here, we combine detailed computational modeling with a new approach to free-swimming experiments, in which feedback gain - i.e., the degree of sensory feedback produced by swimming - is manipulated by varying the height of larval zebrafish above a moving stimulus. We develop an account of underlying feedback control mechanisms that describes not only bout initiation but also the control of swim speed during bouts. We observe that the degree to which fish stabilize their position is only partial and gain-dependent, suggesting that the OMR may not primarily function in fish to prevent drift. We find the speed profile during bouts follows a fixed temporal pattern independent of bout intensity, suggesting that bout termination and bout duration are not explicitly controlled. We also find that the reverse optic flow, experienced when the fish is swimming faster than the stimulus, plays a minimal role in control of the OMR despite carrying most of the sensory information about self-movement. These results shed new light on the underlying dynamics of the OMR in larval zebrafish and will be crucial for future work aimed at identifying the neural basis of this behavior. Author SummaryIn many animals vision is central to the control of locomotory behaviors. In particular, innate motor responses to optic flow allow flying animals to react to gusts of air and fish to changes of current. As fish are washed downstream, for example, movement of the riverbed image across the retina evokes forward movement in bouts (short periods of swimming followed by rest periods). It is typically assumed that this translational optomotor response stabilizes the fishs position to prevent it drifting downstream. In larval zebrafish, this response has become a key model system for investigating the neural basis of sensorimotor behaviors in a vertebrate. Here, we combine behavioral experiments and computational modeling to elucidate the underlying control algorithms. We unpick the detailed relationship between visual stimuli and the initiation, termination and intensity of swim bouts. We find initiation and intensity are controlled separately, and that termination is not explicitly controlled. Surprisingly we also found that the degree of stabilization is only partial and varies systematically with height above ground, raising questions of the function of this response. These findings shed new light on the underlying dynamics which will be crucial for future work to identify the neural basis of this behavior.