Predictive saccade in the absence of smooth pursuit: interception of moving targets in the archer fish

SUMMARY Interception of fast-moving targets is a demanding task many animals solve. To handle it successfully, mammals employ both saccadic and smooth pursuit eye movements in order to confine the target to their area centralis. But how can non-mammalian vertebrates, which lack smooth pursuit, intercept moving targets? We studied this question by exploring eye movement strategies employed by archer fish, an animal that possesses an area centralis, lacks smooth pursuit eye movements, but can intercept moving targets by shooting jets of water at them. We tracked the gaze direction of fish during interception of moving targets and found that they employ saccadic eye movements based on prediction of target position when it is hit. The fish fixates on the target’s initial position for ∼0.2 s from the onset of its motion, a time period used to predict whether a shot can be made before the projection of the target exits the area centralis. If the prediction indicates otherwise, the fish performs a saccade that overshoots the center of gaze beyond the present target projection on the retina, such that after the saccade the moving target remains inside the area centralis long enough to prepare and perform a shot. These results add to the growing body of knowledge on biological target tracking and may shed light on the mechanism underlying this behavior in other animals with no neural system for the generation of smooth pursuit eye movements.

[1]  G. Roth Experimental analysis of the prey catching behavior ofHydromantes italicus Dunn (Amphibia, Plethodontidae) , 2004, Journal of comparative physiology.

[2]  Dan-Eric Nilsson,et al.  The evolution of eyes and visually guided behaviour , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  Mariano Sigman,et al.  Looking at Breakout: Urgency and predictability direct eye events , 2011, Vision Research.

[4]  S. Easter,et al.  Pursuit eye movements in goldfish (Carassius auratus). , 1972, Vision research.

[5]  J. Ewert 5 – The Visual System of the Toad: Behavioral and Physiological Studies on a Pattern Recognition System , 1976 .

[6]  Michael F. Land,et al.  From eye movements to actions: how batsmen hit the ball , 2000, Nature Neuroscience.

[7]  J. J.,et al.  The effects of water depth on prey detection and capture by juvenile coho salmon and steelhead , 2022 .

[8]  Thomas Schlegel,et al.  Small Circuits for Large Tasks: High-Speed Decision-Making in Archerfish , 2008, Science.

[9]  F. Rodríguez,et al.  Cognitive and emotional functions of the teleost fish cerebellum , 2005, Brain Research Bulletin.

[10]  M. Missal,et al.  Quantitative analysis of catch-up saccades during sustained pursuit. , 2002, Journal of neurophysiology.

[11]  Dan Milea,et al.  Prefrontal cortex is involved in internal decision of forthcoming saccades , 2007, Neuroreport.

[12]  M. Petrides,et al.  The effect of spatial and temporal information on saccades and neural activity in oculomotor structures. , 2002, Brain : a journal of neurology.

[13]  H. Hermann,et al.  Eye movements in the goldfish. , 1971, Vision research.

[14]  K. H. Lüling The Archer Fish , 1963 .

[15]  W. F. Blair,et al.  The Amphibian visual system : a multidisciplinary approach , 1976 .

[16]  S. Collin,et al.  A spitting image: specializations in archerfish eyes for vision at the interface between air and water , 2010, Proceedings of the Royal Society B: Biological Sciences.

[17]  C. Hawryshyn,et al.  Behavioural studies of fish vision: an analysis of visual capabilities , 1990 .

[18]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[19]  Paul W. Webb,et al.  EFFECTS OF MEDIAN-FIN AMPUTATION ON FAST-START PERFORMANCE OF RAINBOW TROUT (SALMO GAIRDNERI) , 1977 .

[20]  N. Sawtell,et al.  Cerebellum-like structures and their implications for cerebellar function. , 2008, Annual review of neuroscience.

[21]  Alan C. Evans,et al.  Functional neuroanatomy of smooth pursuit and predictive saccades , 2000, Neuroreport.

[22]  B. Torres,et al.  Connectivity of the goldfish optic tectum with the mesencephalic and rhombencephalic reticular formation , 2003, Experimental Brain Research.

[23]  M. Land Motion and vision: why animals move their eyes , 1999, Journal of Comparative Physiology A.

[24]  R. Segev,et al.  Visual acuity in the archerfish: behavior, anatomy, and neurophysiology. , 2012, Journal of vision.

[25]  S de Brouwer,et al.  Role of retinal slip in the prediction of target motion during smooth and saccadic pursuit. , 2001, Journal of neurophysiology.

[26]  Stefan Schuster,et al.  Animal Cognition: How Archer Fish Learn to Down Rapidly Moving Targets , 2006, Current Biology.

[27]  Klaus-Peter Hoffmann,et al.  Responses to moving visual stimuli in pretectal neurons of the small-spotted dogfish (Scyliorhinus canicula). , 2008, Journal of neurophysiology.

[28]  K. H. Lüling Morphologisch-anatomische und histologische untersuchungen am auge des schützenfisches Toxotes jaculatrix (Pallas 1766) (Toxotidae), nebst bemerkungen zum spuckgehaben , 1958, Zeitschrift für Morphologie und Ökologie der Tiere.

[29]  Maoz Shamir,et al.  Coding “What” and “When” in the Archer Fish Retina , 2010, PLoS Comput. Biol..

[30]  R. Krauzlis Recasting the smooth pursuit eye movement system. , 2004, Journal of neurophysiology.

[31]  C. Pierrot-Deseilligny,et al.  Eye movement control by the cerebral cortex , 2004, Current opinion in neurology.

[32]  E. J. Morris,et al.  Visual motion processing and sensory-motor integration for smooth pursuit eye movements. , 1987, Annual review of neuroscience.

[33]  B S Lanchester,et al.  Pursuit and prediction in the tracking of moving food by a teleost fish (Acanthaluteres spilomelanurus). , 1975, The Journal of experimental biology.

[34]  Ohad Ben-Shahar,et al.  Journal of Neuroscience Methods Measuring and Tracking Eye Movements of a Behaving Archer Fish by Real-time Stereo Vision Author's Personal Copy Author's Personal Copy , 2022 .