Modulation of locomotor activity in larval zebrafish during light adaptation

SUMMARY The neural basis of behavioral choice in vertebrates remains largely unknown. Zebrafish larvae have a defined locomotor repertoire as well as a simple nervous system and are therefore an attractive vertebrate system in which to study this process. Here we describe a high-throughput system for quantifying the kinematics of motor events in zebrafish larvae in order to measure the initiation frequency of different maneuvers. We use this system to analyze responses to photic stimuli and find that larvae respond to changes in illumination with both acute responses and extended behavioral programs. Reductions in illumination elicit large angle turns, distinct from startle responses, which orient larvae toward the source of light. In continuing darkness, larvae are transiently hyperactive before adopting a quiescent state. Indeed, locomotor activity is controlled by the state of light or dark adaptation similar to masking phenomena in higher vertebrates where light directly regulates motor activity. We propose that regulation of motor activity by photic stimuli in zebrafish larvae serves a behavioral goal of maximizing exposure to well lit environments optimal for feeding.

[1]  Alexander F. Schier,et al.  Hypocretin/Orexin Overexpression Induces An Insomnia-Like Phenotype in Zebrafish , 2006, The Journal of Neuroscience.

[2]  F. Rieke,et al.  The impact of photoreceptor noise on retinal gain controls , 2006, Current Opinion in Neurobiology.

[3]  Herwig Baier,et al.  Visual Prey Capture in Larval Zebrafish Is Controlled by Identified Reticulospinal Neurons Downstream of the Tectum , 2005, The Journal of Neuroscience.

[4]  Donald M. O’Malley,et al.  Prey Tracking by Larval Zebrafish: Axial Kinematics and Visual Control , 2005, Brain, Behavior and Evolution.

[5]  Aravinthan D. T. Samuel,et al.  Sensorimotor Integration: Locating Locomotion in Neural Circuits , 2005, Current Biology.

[6]  Herwig Baier,et al.  Channeling of red and green cone inputs to the zebrafish optomotor response , 2005, Visual Neuroscience.

[7]  Cori Bargmann,et al.  A circuit for navigation in Caenorhabditis elegans , 2005 .

[8]  Kevin L. Briggman,et al.  Optical Imaging of Neuronal Populations During Decision-Making , 2005, Science.

[9]  Melina E. Hale,et al.  Swimming of larval zebrafish: fin–axis coordination and implications for function and neural control , 2004, Journal of Experimental Biology.

[10]  Akira Muto,et al.  Retinal network adaptation to bright light requires tyrosinase , 2004, Nature Neuroscience.

[11]  J. Hurley,et al.  Visual Pigment Phosphorylation but Not Transducin Translocation Can Contribute to Light Adaptation in Zebrafish Cones , 2004, Neuron.

[12]  J. V. van Leeuwen,et al.  Swimming of larval zebrafish: ontogeny of body waves and implications for locomotory development , 2004, Journal of Experimental Biology.

[13]  Satchidananda Panda,et al.  Melanopsin Is Required for Non-Image-Forming Photic Responses in Blind Mice , 2003, Science.

[14]  M. Biel,et al.  Melanopsin and rod–cone photoreceptive systems account for all major accessory visual functions in mice , 2003, Nature.

[15]  S. Neuhauss Behavioral genetic approaches to visual system development and function in zebrafish. , 2003, Journal of neurobiology.

[16]  Donald M. O’Malley,et al.  Prey Capture by Larval Zebrafish: Evidence for Fine Axial Motor Control , 2002, Brain, Behavior and Evolution.

[17]  G. Cahill,et al.  Entraining Signals Initiate Behavioral Circadian Rhythmicity in Larval Zebrafish , 2002, Journal of biological rhythms.

[18]  Paolo Domenici,et al.  The Visually Mediated Escape Response in Fish: Predicting Prey Responsiveness and the Locomotor Behaviour of Predators and Prey , 2002 .

[19]  Uwe Redlin,et al.  NEURAL BASIS AND BIOLOGICAL FUNCTION OF MASKING BY LIGHT IN MAMMALS: SUPPRESSION OF MELATONIN AND LOCOMOTOR ACTIVITY , 2001, Chronobiology international.

[20]  D. O'Malley,et al.  Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. , 2000, The Journal of experimental biology.

[21]  E. N. Pugh,et al.  Molecular mechanisms of vertebrate photoreceptor light adaptation , 1999, Current Opinion in Neurobiology.

[22]  J. Fetcho,et al.  Laser Ablations Reveal Functional Relationships of Segmental Hindbrain Neurons in Zebrafish , 1999, Neuron.

[23]  N. Mrosovsky,et al.  Masking of locomotor activity in hamsters , 1999, Journal of Comparative Physiology A.

[24]  J. Aschoff,et al.  Masking and parametric effects of high-frequency light-dark cycles. , 1999, The Japanese journal of physiology.

[25]  G. Cahill,et al.  Circadian rhythmicity in the locomotor activity of larval zebrafish , 1998, Neuroreport.

[26]  M. Tabata,et al.  Circadian rhythms of demand‐feeding and locomotor activity in rainbow trout , 1998 .

[27]  W. Kristan,et al.  Population coding and behavioral choice , 1997, Current Opinion in Neurobiology.

[28]  J. Dowling,et al.  A New Form of Inherited Red-Blindness Identified in Zebrafish , 1997, The Journal of Neuroscience.

[29]  S. Easter,et al.  The development of vision in the zebrafish (Danio rerio). , 1996, Developmental biology.

[30]  S. Zamora,et al.  Demand feeding and locomotor circadian rhythms in the goldfish, Carassius auratus: Dual and independent phasing , 1996, Physiology & Behavior.

[31]  D. Grier,et al.  Methods of Digital Video Microscopy for Colloidal Studies , 1996 .

[32]  J B Hurley,et al.  A behavioral screen for isolating zebrafish mutants with visual system defects. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[33]  S. G. Reebs The anticipation of night by fry-retrieving convict cichlids , 1994, Animal Behaviour.

[34]  K. Hatta Role of the floor plate in axonal patterning in the zebrafish CNS , 1992, Neuron.

[35]  D. Faber,et al.  Localization of optic tectal input to the ventral dendrite of the goldfish Mauthner cell , 1987, Brain Research.

[36]  G. Helfman Fish Behaviour by Day, Night and Twilight , 1986 .

[37]  Peter Munk,et al.  Feeding behaviour and swimming activity of larval herring (Clupea harengus) in relation to density of copepod nauplii. , 1985 .

[38]  Dt. Clark Visual responses in developing zebrafish (Brachydanio rerio) , 1982 .

[39]  W F Brown,et al.  Light‐stimulus‐evoked blink reflex Methods, normal values, relation to other blink reflexes, and observations in multiple sclerosis , 1981, Neurology.

[40]  D A Newsome,et al.  Light suppresses melatonin secretion in humans. , 1980, Science.

[41]  B J Stahl,et al.  EARLY AND RECENT PRIMITIVE BRAIN FORMS , 1977, Annals of the New York Academy of Sciences.

[42]  D L Meyer,et al.  The Mauthner-initiated startle response in teleost fish. , 1977, The Journal of experimental biology.

[43]  Lawrence M. Dill,et al.  The escape response of the zebra danio (Brachydanio rerio) I. The stimulus for escape , 1974 .

[44]  Mahendra Somasundaram,et al.  New Developments in Electromyography and Clinical Neurophysiology. , 1974 .

[45]  H. J. Seddon,et al.  New Developments in Electromyography and Clinical Neurophysiology , 1974 .

[46]  C. Kimmel,et al.  The development and behavioral characteristics of the startle response in the zebra fish. , 1974, Developmental psychobiology.

[47]  W. Scheerer,et al.  The Blink Reflex Induced by Photic Stimuli , 1973 .

[48]  J. Weller,et al.  Rapid Light-Induced Decrease in Pineal Serotonin N-Acetyltransferase Activity , 1972, Science.

[49]  J. Aschoff,et al.  Exogenous and endogenous components in circadian rhythms. , 1960, Cold Spring Harbor symposia on quantitative biology.

[50]  Clyde E. Keeler,et al.  IRIS MOVEMENTS IN BLIND MICE , 1927 .