Modeling anxiety using adult zebrafish: A conceptual review

Zebrafish (Danio rerio) are rapidly emerging as a useful animal model in neurobehavioral research. Mounting evidence shows the suitability of zebrafish to model various aspects of anxiety-related states. Here, we evaluate established and novel approaches to uncover the molecular substrates, genetic pathways and neural circuits of anxiety using adult zebrafish. Experimental approaches to modeling anxiety in zebrafish include novelty-based paradigms, pharmacological and genetic manipulations, as well as innovative video-tracking, 3D-reconstructions, bioinformatics-based searchable databases and omics-based tools. Complementing traditional rodent models of anxiety, we provide a conceptual framework for the wider application of zebrafish and other aquatic models in anxiety research. This article is part of a Special Issue entitled 'Anxiety and Depression'.

[1]  Hitoshi Okamoto,et al.  Identification of the Zebrafish Ventral Habenula As a Homolog of the Mammalian Lateral Habenula , 2010, The Journal of Neuroscience.

[2]  I. Liberzon,et al.  Exposure to extreme stress impairs contextual odour discrimination in an animal model of PTSD. , 2009, The international journal of neuropsychopharmacology.

[3]  Michael R. Taylor,et al.  Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression , 2005, Neuroscience.

[4]  Rainer W. Friedrich,et al.  Circuit Neuroscience in Zebrafish , 2010, Current Biology.

[5]  J. Cryan,et al.  Bupropion enhances brain reward function and reverses the affective and somatic aspects of nicotine withdrawal in the rat , 2003, Psychopharmacology.

[6]  A. Holmes,et al.  Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice , 2007, Behavioural Brain Research.

[7]  Evan J. Kyzar,et al.  Three-Dimensional Neurophenotyping of Adult Zebrafish Behavior , 2011, PloS one.

[8]  Bruce S. McEwen,et al.  INDUCTION OF CORTICOTROPIN-RELEASING HORMONE GENE EXPRESSION BY GLUCOCORTICOIDS: IMPLICATION FOR UNDERSTANDING THE STATES OF FEAR AND ANXIETY AND ALLOSTATIC LOAD , 1998, Psychoneuroendocrinology.

[9]  J. Fetcho.  Imaging neuronal activity with calcium indicators in larval zebrafish. , 2007, CSH protocols.

[10]  Robert Gerlai,et al.  Zebrafish antipredatory responses: A future for translational research? , 2010, Behavioural Brain Research.

[11]  Winford A. Gordon,et al.  Effects of scopolamine, pentobarbital, and amphetamine on radial arm maze performance in the rat , 1980, Pharmacology Biochemistry and Behavior.

[12]  M. Kas,et al.  Cross-species behavioural genetics: A starting point for unravelling the neurobiology of human psychiatric disorders , 2011, Progress in Neuro-psychopharmacology and Biological Psychiatry.

[13]  Zhang Jie,et al.  Trans-2-phenylcyclopropylamine induces nerve cells apoptosis in zebrafish mediated by depression of LSD1 activity , 2009, Brain Research Bulletin.

[14]  E. Eisenstein,et al.  A Behavioral Homeostasis Theory of Habituation and Sensitization: II. Further Developments and Predictions , 2006, Reviews in the neurosciences.

[15]  B. Key,et al.  Zebrafish as an experimental model: strategies for developmental and molecular neurobiology studies. , 2003, Methods in cell science : an official journal of the Society for In Vitro Biology.

[16]  Evan J. Kyzar,et al.  Behavioral effects of MDMA (‘ecstasy’) on adult zebrafish , 2011, Behavioural pharmacology.

[17]  J. Ballenger.  Current treatments of the anxiety disorders in adults , 1999, Biological Psychiatry.

[18]  A. Stewart,et al.  Modeling seizure-related behavioral and endocrine phenotypes in adult zebrafish , 2010, Brain Research.

[19]  J. Baeyens,et al.  The NMDA receptor antagonist dizocilpine (MK-801) stereoselectively inhibits morphine-induced place preference conditioning in mice , 1996, Psychopharmacology.

[20]  A. Carlsson,et al.  MK-801-induced hyperlocomotion: differential effects of M100907, SDZ PSD 958 and raclopride. , 1997, European journal of pharmacology.

[21]  I. Zhdanova,et al.  Gender differences in zebrafish responses to cocaine withdrawal , 2008, Physiology & Behavior.

[22]  F. Holsboer,et al.  Protein Biomarkers in a Mouse Model of Extremes in Trait Anxiety* , 2006, Molecular & Cellular Proteomics.

[23]  Evan J. Kyzar,et al.  Zebrafish models to study drug abuse-related phenotypes , 2011, Reviews in the neurosciences.

[24]  J. Krause,et al.  QTL Analysis of Behavioral and Morphological Differentiation Between Wild and Laboratory Zebrafish (Danio rerio) , 2006, Behavior genetics.

[25]  S. Hallgren,et al.  Anxiogenic behaviour induced by 17α-ethynylestradiol in male guppies (Poecilia reticulata) , 2011, Fish Physiology and Biochemistry.

[26]  Holly A Swain,et al.  Effects of dizocilpine (MK-801) on circling behavior, swimming activity, and place preference in zebrafish (Danio rerio). , 2004, Neurotoxicology and teratology.

[27]  Z. Hliňák,et al.  Modulary effects of oxytocin and carbetocin on stress-induced changes in rat behavior in the open-field. , 2009, Journal of physiology and pharmacology : an official journal of the Polish Physiological Society.

[28]  J. Livet,et al.  A technicolour approach to the connectome , 2008, Nature Reviews Neuroscience.

[29]  Siddharth Gaikwad,et al.  Characterization of behavioral and endocrine effects of LSD on zebrafish , 2010, Behavioural Brain Research.

[30]  D. Blanchard,et al.  The characterization and modelling of antipredator defensive behavior , 1990, Neuroscience & Biobehavioral Reviews.

[31]  R. Passingham.  The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[32]  D. Diamond,et al.  Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and prefrontal cortex , 2005, Biological Psychiatry.

[33]  Allan V. Kalueff,et al.  Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish , 2009, Behavioural Brain Research.

[34]  T. Nabeshima,et al.  Chronic restraint stress impairs neurogenesis and hippocampus‐dependent fear memory in mice: possible involvement of a brain‐specific transcription factor Npas4 , 2010, Journal of neurochemistry.

[35]  D. Lara,et al.  Distinctive effects of unpredictable subchronic stress on memory, serum corticosterone and hippocampal BDNF levels in high and low exploratory mice , 2011, Behavioural Brain Research.

[36]  C. Belzung,et al.  Genetic basis of anxiety-like behaviour: a critical review , 2002, Brain Research Bulletin.

[37]  G. Lieschke,et al.  Manipulation of gene expression during zebrafish embryonic development using transient approaches. , 2008, Methods in molecular biology.

[38]  R. Roth,et al.  TMT, a predator odor, elevates mesoprefrontal dopamine metabolic activity and disrupts short-term working memory in the rat , 2000, Brain Research Bulletin.

[39]  E. Serra,et al.  Natural preference of zebrafish (Danio rerio) for a dark environment. , 1999, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[40]  C. Belzung,et al.  Environmental enrichment in BALB/c mice Effects in classical tests of anxiety and exposure to a predatory odor , 2001, Physiology & Behavior.

[41]  M. Geyer,et al.  Dissociation of multiple effects of acute LSD on exploratory behavior in rats by ritanserin and propranolol , 2006, Psychopharmacology.

[42]  Siddharth Gaikwad,et al.  Deconstructing Adult Zebrafish Behavior with Swim Trace Visualizations , 2011 .

[43]  Evan J. Kyzar,et al.  Pharmacological modulation of anxiety-like phenotypes in adult zebrafish behavioral models , 2011, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[44]  Siddharth Gaikwad,et al.  Modeling Stress and Anxiety in Zebrafish , 2011 .

[45]  Emília P. Martins,et al.  Behavioral syndromes and the evolution of correlated behavior in zebrafish , 2007 .

[46]  R. Thisted,et al.  Distinct temporal phases in the behavioral pharmacology of LSD: dopamine D2 receptor-mediated effects in the rat and implications for psychosis , 2005, Psychopharmacology.

[47]  S. Jesuthasan,et al.  Fear, anxiety, and control in the zebrafish , 2012, Developmental neurobiology.

[48]  G. Riedel.  Long-term habituation to spatial novelty in blind cave fish (Astyanax hubbsi): role of the telencephalon and its subregions. , 1998, Learning & memory.

[49]  J. Crawley.  A monoamine oxidase inhibitor reverses the 'separation syndrome' in a new hamster separation model of depression. , 1985, European journal of pharmacology.

[50]  T. Svensson,et al.  Prazosin inhibits MK-801-induced hyperlocomotion and dopamine release in the nucleus accumbens. , 1996, European journal of pharmacology.

[51]  David J. Echevarria,et al.  A Novel Behavioral Test Battery to Assess Global Drug Effects Using the Zebrafish , 2008, International Journal of Comparative Psychology.

[52]  G. Griebel,et al.  The Mouse Defense Test Battery: pharmacological and behavioral assays for anxiety and panic. , 2003, European journal of pharmacology.

[53]  Siddharth Gaikwad,et al.  Behavioral and physiological effects of RDX on adult zebrafish. , 2012, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[54]  D. Barros,et al.  Behavioral and neurotoxic effects of arsenic exposure in zebrafish (Danio rerio, Teleostei: Cyprinidae). , 2009, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[55]  J. Krause,et al.  Learning in fishes: From three-second memory to culture , 2003 .

[56]  A. Stewart,et al.  Homebase behavior of zebrafish in novelty-based paradigms , 2010, Behavioural Processes.

[57]  E. sanders-Bush,et al.  Agonist-Directed Signaling of Serotonin 5-HT2C Receptors: Differences Between Serotonin and Lysergic Acid Diethylamide (LSD) , 1999, Neuropsychopharmacology.

[58]  R. Gerlai,et al.  Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects , 2000, Pharmacology Biochemistry and Behavior.

[59]  M. Geyer,et al.  5HT-2 mediation of acute behavioral effects of hallucinogens in rats , 2005, Psychopharmacology.

[60]  D. Diamond,et al.  Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female rats. , 2008, Learning & memory.

[61]  Noam Miller,et al.  Quantification of shoaling behaviour in zebrafish (Danio rerio) , 2007, Behavioural Brain Research.

[62]  V. Camus,et al.  Association between Repeated Unpredictable Chronic Mild Stress (UCMS) Procedures with a High Fat Diet: A Model of Fluoxetine Resistance in Mice , 2010, PloS one.

[63]  J. Wittbrodt,et al.  Medaka and zebrafish, an evolutionary twin study , 2004, Mechanisms of Development.

[64]  M. Geyer,et al.  A proposed animal model for hallucinogens based on LSD's effects on patterns of exploration in rats. , 1985, Behavioral neuroscience.

[65]  Siddharth Gaikwad,et al.  Phenotyping of Zebrafish Homebase Behaviors in Novelty-Based Tests , 2011 .

[66]  Theresa Burt de Perera,et al.  Fish can encode order in their spatial map. , 2004, Proceedings. Biological sciences.

[67]  E. Levin,et al.  Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety , 2009, Pharmacology Biochemistry and Behavior.

[68]  Hans A Hofmann,et al.  Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray , 2004, BMC Genomics.

[69]  E. Hirsch,et al.  c-fos protein-like immunoreactivity: Distribution in the human brain and over-expression in the hippocampus of patients with Alzheimer's disease , 1992, Neuroscience.

[70]  Robert Gerlai,et al.  Zebrafish (Danio rerio) responds differentially to stimulus fish: The effects of sympatric and allopatric predators and harmless fish , 2008, Behavioural Brain Research.

[71]  Rikuko Sekiguchi,et al.  The effect of MK-801 on openfield activities and object exploration and its sex difference , 1998 .

[72]  Su Guo,et al.  Identification of a brain center whose activity discriminates a choice behavior in zebrafish , 2011, Proceedings of the National Academy of Sciences.

[73]  A. Stewart,et al.  Acute stress disrupts performance of zebrafish in the cued and spatial memory tests: The utility of fish models to study stress–memory interplay , 2011, Behavioural Processes.

[74]  Siddharth Gaikwad,et al.  Measuring behavioral and endocrine responses to novelty stress in adult zebrafish , 2010, Nature Protocols.

[75]  Silvio Morato,et al.  Measuring anxiety in zebrafish: A critical review , 2010, Behavioural Brain Research.

[76]  D. Kupfer,et al.  Revisiting the effectiveness of standard antidepressants in bipolar disorder: are monoamine oxidase inhibitors superior? , 2009, Psychopharmacology bulletin.

[77]  Silvio Morato,et al.  Parametric analyses of anxiety in zebrafish scototaxis , 2010, Behavioural Brain Research.

[78]  Masahiko Hibi,et al.  Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish , 2008, Proceedings of the National Academy of Sciences.

[79]  Edward D. Levin,et al.  Anxiolytic effects of nicotine in zebrafish , 2007, Physiology & Behavior.

[80]  M. Concha,et al.  Zebrafish and medaka: model organisms for a comparative developmental approach of brain asymmetry , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[81]  M. Calcagnotto,et al.  Differences in Spatio-Temporal Behavior of Zebrafish in the Open Tank Paradigm after a Short-Period Confinement into Dark and Bright Environments , 2011, PloS one.

[82]  R. Layer,et al.  The NMDA receptor antagonist MK-801 elicits conditioned place preference in rats , 1993, Pharmacology Biochemistry and Behavior.

[83]  D. Diamond,et al.  Emotion-induced amnesia in rats: working memory-specific impairment, corticosterone-memory correlation, and fear versus arousal effects on memory. , 2003, Learning & memory.

[84]  J. Krause,et al.  Inter and intra-population variation in shoaling and boldness in the zebrafish (Danio rerio) , 2003, Naturwissenschaften.

[85]  R. Gerlai,et al.  Alarm substance induced behavioral responses in zebrafish (Danio rerio) , 2008, Behavioural Brain Research.

[86]  M. Bogo,et al.  Unpredictable chronic stress model in zebrafish (Danio rerio): Behavioral and physiological responses , 2011, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[87]  Richard A Rabin,et al.  Ethanol effects on three strains of zebrafish: model system for genetic investigations , 2003, Pharmacology Biochemistry and Behavior.

[88]  T. Koyama,et al.  Monoamine oxidase inhibitors reduce conditioned fear stress-induced freezing behavior in rats. , 2000, European journal of pharmacology.

[89]  R. E. Blaser,et al.  Behavioral measures of anxiety in zebrafish (Danio rerio) , 2010, Behavioural Brain Research.

[90]  Junichi Nakai,et al.  Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish , 2011, Proceedings of the National Academy of Sciences.

[91]  Robert Gerlai,et al.  Zebrafish (Danio rerio) responds to the animated image of a predator: Towards the development of an automated aversive task , 2009, Behavioural Brain Research.

[92]  G. Griebel,et al.  Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic , 2001, Neuroscience & Biobehavioral Reviews.

[93]  Gene A. Brewer,et al.  The Emotion Dysregulation Model of Anxiety: a preliminary path analytic examination. , 2010, Journal of anxiety disorders.

[94]  H-W Lee,et al.  Stimulation of DNA synthesis, activation of mitogen‐activated protein kinase ERK2 and nuclear accumulation of c‐fos in human aortic smooth muscle cells by ketamine , 2002, Cell proliferation.

[95]  M. Bogo,et al.  Antipsychotic drugs prevent the motor hyperactivity induced by psychotomimetic MK-801 in zebrafish (Danio rerio) , 2010, Behavioural Brain Research.

[96]  C. Conrad,et al.  Short CommunicationChronic stress leaves novelty-seeking behavior intact while impairing spatial recognition memory in the Y-maze , 2005, Stress.

[97]  Repeated treatment with imipramine, fluvoxamine and tranylcypromine decreases the number of escape failures by activating dopaminergic systems in a rat learned helplessness test. , 2001, Life sciences.

[98]  R. Landgraf,et al.  High vs Low Anxiety-Related Behavior Rats: An Animal Model of Extremes in Trait Anxiety , 2002, Behavior genetics.

[99]  J. Krause,et al.  Sex matters: a social context to boldness in guppies (Poecilia reticulata) , 2010 .

[100]  Olaf Ronneberger,et al.  Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems , 2011, Nature communications.

[101]  Cristina Saverino,et al.  The social zebrafish: Behavioral responses to conspecific, heterospecific, and computer animated fish , 2008, Behavioural Brain Research.

[102]  Sam Patrick Ogwang.  Inspection of a novel object by wild and laboratory Zebrafish (Danio rerio H.) in the presence and absence of alarm substance , 2008 .

[103]  Evan J. Kyzar,et al.  Experimental models for anxiolytic drug discovery in the era of omes and omics , 2011, Expert opinion on drug discovery.

[104]  Siddharth Gaikwad,et al.  Neurophenotyping of Adult Zebrafish Using the Light/Dark Box Paradigm , 2011 .

[105]  Ngoc Kim Nhung Nguyen,et al.  Zebrafish Behavior in Novel Environments: Effects of Acute Exposure to Anxiolytic Compounds and Choice of Danio rerio Line. , 2010, International journal of comparative psychology.

[106]  K. Miczek,et al.  Ultrasonic vocalizations in rat pups: effects of serotonergic ligands , 1998, Neuroscience & Biobehavioral Reviews.

[107]  Michael K. Richardson,et al.  Translating rodent behavioral repertoire to zebrafish (Danio rerio): Relevance for stress research , 2010, Behavioural Brain Research.

[108]  Chiranjib Chakraborty,et al.  Zebrafish: a complete animal model for in vivo drug discovery and development. , 2009, Current drug metabolism.

[109]  Silvio Morato,et al.  Scototaxis as anxiety-like behavior in fish , 2010, Nature Protocols.

[110]  Siddharth Gaikwad,et al.  The Developing Utility of Zebrafish in Modeling Neurobehavioral Disorders , 2010, International Journal of Comparative Psychology.

[111]  B. Shyu,et al.  Open Access Research , 2022 .

[112]  Akihiro Urasaki,et al.  Olfactory neural circuitry for attraction to amino acids revealed by transposon-mediated gene trap approach in zebrafish , 2009, Proceedings of the National Academy of Sciences.

[113]  D. Eilam,et al.  Home base behavior of rats (Rattus norvegicus) exploring a novel environment , 1989, Behavioural Brain Research.

[114]  Yoav Benjamini,et al.  Mouse Cognition-Related Behavior in the Open-Field: Emergence of Places of Attraction , 2008, PLoS Comput. Biol..

[115]  G. Griebel,et al.  Long-term impaired memory following predatory stress in mice , 2006, Physiology & Behavior.

[116]  L. Barcellos,et al.  Whole-body cortisol increases after direct and visual contact with a predator in zebrafish, Danio rerio , 2007 .

[117]  K. Purcell,et al.  The effects of psychological stress as a function of need and cognitive control. , 1959, Journal of personality.

[118]  J. Cachat,et al.  Mutant and Transgenic Zebrafish in Modeling Neurobehavioral Disorders , 2010 .

[119]  M. Ryan,et al.  Learned Social Preference in Zebrafish , 2004, Current Biology.

[120]  J. Zohar,et al.  The immediate early gene Arc is associated with behavioral resilience to stress exposure in an animal model of posttraumatic stress disorder , 2008, European Neuropsychopharmacology.

[121]  C. Claudianos,et al.  Big ideas for small brains: what can psychiatry learn from worms, flies, bees and fish? , 2011, Molecular Psychiatry.

[122]  Sonia J. Bishop,et al.  Neurocognitive mechanisms of anxiety: an integrative account , 2007, Trends in Cognitive Sciences.

[123]  Scott P. McRobert,et al.  The effect of sex and shoal size on shoaling behaviour in Danio rerio , 2005 .

[124]  H. Burgess,et al.  The neurogenetic frontier--lessons from misbehaving zebrafish. , 2008, Briefings in functional genomics & proteomics.

[125]  R. Adamec,et al.  NMDA Receptors Mediate Lasting Increases in Anxiety-Like Behavior Produced by the Stress of Predator Exposure—Implications for Anxiety Associated with Posttraumatic Stress Disorder , 1998, Physiology & Behavior.

[126]  S. Higashijima,et al.  The habenula is crucial for experience-dependent modification of fear responses in zebrafish , 2010, Nature Neuroscience.

[127]  Siddharth Gaikwad,et al.  Analyzing habituation responses to novelty in zebrafish (Danio rerio) , 2010, Behavioural Brain Research.

[128]  Javier DeFelipe,et al.  From the Connectome to the Synaptome: An Epic Love Story , 2010, Science.

[129]  Yuanye Ma,et al.  Environmental enrichment and chronic restraint stress in ICR mice: Effects on prepulse inhibition of startle and Y-maze spatial recognition memory , 2010, Behavioural Brain Research.

[130]  Cathleen Teh,et al.  The Habenula Prevents Helpless Behavior in Larval Zebrafish , 2010, Current Biology.

[131]  Adam M. Campbell,et al.  Influence of predator stress on the consolidation versus retrieval of long‐term spatial memory and hippocampal spinogenesis , 2006, Hippocampus.

[132]  A. Bidziński,et al.  The effects of repeated administration of diazepam, MK-801 and CGP 37849 on rat behavior in two models of anxiety , 1996, European Neuropsychopharmacology.

[133]  D. Murphy,et al.  What's wrong with my mouse model? Advances and strategies in animal modeling of anxiety and depression , 2007, Behavioural Brain Research.

[134]  Burton S. Rosner,et al.  Neuropharmacology , 1958, Nature.

[135]  J. Seckl,et al.  Site-specific regulation of corticosteroid and serotonin receptor subtype gene expression in the rat hippocampus following 3,4-methylenedioxymethamphetamine: role of corticosterone and serotonin , 1997, Neuroscience.

[136]  Laure Bally-Cuif,et al.  Adult zebrafish as a model organism for behavioural genetics , 2010, BMC Neuroscience.

[137]  M. Geyer,et al.  LSD-induced alterations of locomotor patterns and exploration in rats , 2004, Psychopharmacology.

[138]  S. Kulkarni,et al.  MK‐801 produces antianxiety effect in elevated plus‐maze in mice , 1991 .

[139]  H. Ewald.  A zebrafish model of schizophrenia and sickness behavior: MK-801 and endogenous NMDAR antagonism , 2009 .

[140]  N. Schork,et al.  Identification of Quantitative Trait Loci for Anxiety and Locomotion Phenotypes in Rat Recombinant Inbred Strains , 2004, Behavior genetics.

[141]  E. Giller,et al.  Glucocorticoid receptor number and cortisol excretion in mood, anxiety, and psychotic disorders , 1993, Biological Psychiatry.

[142]  Carsten Marr,et al.  Zebrafish reward mutants reveal novel transcripts mediating the behavioral effects of amphetamine , 2009, Genome Biology.

[143]  A. Shekhar,et al.  Exposure to an open-field arena increases c-Fos expression in a distributed anxiety-related system projecting to the basolateral amygdaloid complex , 2008, Neuroscience.

[144]  G M Rose,et al.  Exposing rats to a predator impairs spatial working memory in the radial arm water maze , 1999, Hippocampus.

[145]  J. Livet,et al.  Multicolor Brainbow imaging in zebrafish. , 2011, Cold Spring Harbor protocols.

[146]  Diogo R. Lara,et al.  Effects of anxiolytics in zebrafish: Similarities and differences between benzodiazepines, buspirone and ethanol , 2011, Pharmacology Biochemistry and Behavior.

[147]  Mark A Masino,et al.  Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. , 2003, Journal of neurophysiology.