Are cerebral and behavioural lateralization related to anxiety-like traits in the animal model zebrafish (Danio rerio)?

References

• Agrillo, C., & Dadda, M. (2007). Discrimination of the larger shoal in the poeciliid fish Girardinus falcatus. Ethology Ecology and Evolution, 19, 145–157.
   Web of Science ®Google Scholar
• Aizawa, H., Amo, R., & Okamoto, H. (2011). Phylogeny and ontogeny of the habenular structure. Frontiers in Neuroscience, 5, 138. doi:10.3389/fnins.2011.00138
   PubMed Web of Science ®Google Scholar
• Ampatzis, K., & Dermon, C. R. (2016). Sexual dimorphisms in swimming behavior, cerebral metabolic activity and adrenoceptors in adult zebrafish (Danio rerio). Behavioural Brain Research, 312, 385–393.
   PubMed Web of Science ®Google Scholar
• Bandelow, B., & Michaelis, S. (2015). Epidemiology of anxiety disorders in the 21st century. Dialogues in Clinical Neuroscience, 17, 327–335.
   PubMed Web of Science ®Google Scholar
• Barlow, D. H. (1991). Disorders of emotion. Psychological Inquiry, 2, 58–71.
   Google Scholar
• Bisazza, A., & De Santi, A. (2003). Lateralization of aggression in fish. Behavioural Brain Research, 141, 131–136.
   PubMed Web of Science ®Google Scholar
• Bisazza, A., Facchin, L., & Vallortigara, G. (2000). Heritability of lateralization in fish: Concordance of right-left asymmetry of detour responses between parents and offspring. Neuropsychologia, 38, 907–912.
   PubMed Web of Science ®Google Scholar
• Bisazza, A., Sovrano, V. A., & Vallortigara, G. (2001). Consistency among different tasks of left-right asymmetries in lines of fish originally selected for opposite direction of lateralization in a detour task. Neuropsychologia, 39, 1077–1085.
   PubMed Web of Science ®Google Scholar
• Blaser, R. E., & Rosemberg, D. B. (2012). Measures of anxiety in zebrafish (Danio rerio): Dissociation of black/white preference and novel tank test. PLoS ONE, 7, e36931.
   PubMed Web of Science ®Google Scholar
• Bonati, B., Csermely, D., Lopez, P., & Martin, J. (2010). Lateralization in the escape behaviour of the common wall lizard (Podarcis muralis). Behavioural Brain Research, 207, 1–6.
   PubMed Web of Science ®Google Scholar
• Brandler, W. M., & Paracchini, S. (2014). The genetic relationship between handedness and neurodevelopmental disorders. Trends in Molecular Medicine, 20, 83–90.
   PubMed Web of Science ®Google Scholar
• Chakravarty, S., Reddy, B. R., Sudhakar, S. R., Saxena, S., Das, T., Meghah, V., … Idris, M. M. (2013). Chronic unpredictable stress (CUS)-induced anxiety and related mood disorders in a zebrafish model: Altered brain proteome profile implicates mitochondrial dysfunction. PLoS ONE, 8, e63302.
   PubMed Web of Science ®Google Scholar
• Champagne, D. L., Hoefnagels, C. C. M., de Kloet, R. E., & Richardson, M. K. (2010). Translating rodent behavioral repertoire to zebrafish (Danio rerio): relevance for stress research. Behavioural Brain Research, 214, 332-342
   PubMed Web of Science ®Google Scholar
• Chen, J., Lei, L., Tian, L., Hou, F., Roper, C., Ge, X., … Huang, C. (2018). Developmental and behavioral alterations in zebrafish embryonically exposed to valproic acid (VPA): An aquatic model for autism. Neurotoxicology and Teratology, 66, 8–16.
   PubMed Web of Science ®Google Scholar
• Clayman, C. L., Malloy, E. J., Kearns, D. N., & Connaughton, V. P. (2017). Differential behavioral effects of ethanol pre-exposure in male and female zebrafish (Danio rerio). Behavioural Brain Research, 335, 174–184.
   PubMed Web of Science ®Google Scholar
• Concha, M. L., Burdine, R. D., Russell, C., Schier, A. F., & Wilson, S. W. (2000). A nodal signalling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron, 28, 399–409.
   PubMed Web of Science ®Google Scholar
• Concha, M. L., & Wilson, S. W. (2001). Asymmetry in the epithalamus of vertebrates. Journal of Anatomy, 199, 63–84.
   PubMed Web of Science ®Google Scholar
• Dadda, M., Domenichini, A., Piffer, L., Argenton, F., & Bisazza, A. (2010). Early differences in epithalamic left-right asymmetry influence lateralization and personality of adult zebrafish. Behavioural Brain Research, 206, 208–215.
   PubMed Web of Science ®Google Scholar
• Dharmaretnam, M., & Rogers, L. J. (2005). Hemispheric specialization and dual processing in strongly versus weakly lateralized chicks. Behavioural Brain Research, 162, 62–70.
   PubMed Web of Science ®Google Scholar
• Domenichini, A., Dadda, M., Facchin, L., Bisazza, A., & Argenton, F. (2011). Isolation and genetic characterization of mother-of-snow-white, a maternal effect allele affecting laterality and lateralized behaviors in zebrafish. PLoS ONE, 6, e25972.
   PubMed Web of Science ®Google Scholar
• Dreosti, E., Vendrell Llopis, N., Carl, M., Yaksi, E., & Wilson, S. W. (2014). Left-right asymmetry is required for the habenulae to respond to both visual and olfactory stimuli. Current Biology, 24, 440–445.
   PubMed Web of Science ®Google Scholar
• Duboc, V., Dufourcq, P., Blader, P., & Roussigné, M. (2015). Asymmetry of the brain: Development and Implications. Annual Review of Genetics, 49, 647–672.
   PubMed Web of Science ®Google Scholar
• Duboué, E. R., & Halpern, M. E. (2017). Genetic and transgenic approaches to study zebrafish brain asymmetry and lateralized behavior. In L. J. Rogers, & G. Vallortigara (Eds.), Lateralized brain functions. Neuromethods (pp. 553–589). New York, NY: Humana Press.
   Google Scholar
• Duboué, E. R., Hong, E., Eldred, K., & Halpern, M. (2017). Left habenular activity attenuates fear responses in larval zebrafish. Current Biology, 14, 2154–2162.
   Google Scholar
• Engels, A. S., Heller, W., Mohanty, A., Herrington, J. D., Banich, M. T., Webb, A. G., et al. (2007). Specificity of regional brain activity in anxiety types during emotion processing. Psychophysiology, 44, 352–363.
   PubMed Web of Science ®Google Scholar
• Facchin, L., Bisazza, A., & Vallortigara, G. (1999). What causes lateralization of detour behavior in fish? Evidence for asymmetries in eye use. Behavioural Brain Research, 103, 229–234
   PubMed Web of Science ®Google Scholar
• Facchin, L., Burgess, H. A., Siddiqi, M., Granato, M., & Halpern, M. E. (2009). Determining the function of zebrafish epithalamic asymmetry. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 1021–1032.
   PubMed Web of Science ®Google Scholar
• Facchin, L., Duboué, E. R., & Halpern, M. E. (2015). Disruption of epithalamic left-right asymmetry increases anxiety in zebrafish. Journal of Neuroscience, 35, 15847–15859.
   PubMed Web of Science ®Google Scholar
• Filgueiras, C. C., Abreu-Villac, Y., Krahe, T. E., & Manhaes, A. C. (2006). Unilateral hemispherectomy at adulthood asymmetrically affects immobile behavior of male Swiss mice. Behavioural Brain Research, 172, 33–38.
   PubMed Web of Science ®Google Scholar
• Fontana, B. D., Cleal, M., Clay, J. M., & Parker, M. O. (2019a). Zebrafish (Danio rerio) behavioral laterality predicts increased short-term avoidance memory but not stress-reactivity responses. Animal Cognition, 22, 1051–1061.
   PubMed Web of Science ®Google Scholar
• Fontana, B. D., Cleal, M., & Parker, M. O. (2019b). Female adult zebrafish (Danio rerio) show higher levels of anxiety-like behavior than males, but do not differ in learning and memory capacity. European Journal of Neuroscience, 14588.
   Web of Science ®Google Scholar
• Fontana, B. D., Mezzomo, N. J., Kalueff, A. V., & Rosemberg, D. B. (2018). The developing utility of zebrafish models of neurological and neuropsychiatric disorders: A critical review. Experimental Neurology, 299, 157–171.
   PubMed Web of Science ®Google Scholar
• Gamse, J. T., Kuan, Y. S., Macurak, M., Brösamle, C., Thisse, B., Thisse, C., & Halpern, M. E. (2005). Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target. Development, 132, 4869–4881.
   PubMed Web of Science ®Google Scholar
• Gamse, J. T., Thisse, C., Thisse, B., & Halpern, M. E. (2003). The parapineal mediates left-right asymmetry in the zebrafish diencephalon. Development, 130, 1059–1068.
   PubMed Web of Science ®Google Scholar
• Gatto, E., Agrillo, C., Brown, C., & Dadda, M. (2019). Individual differences in numerical skills are influenced by brain lateralization in guppies (Poecilia reticulata). Intelligence, 74, 12–17.
   Web of Science ®Google Scholar
• Gatto, E., Lucon-Xiccato, T., Savaşçi, B. B., Dadda, M., & Bisazza, A. (2017). Experimental setting affects the performance of guppies in a numerical discrimination task. Animal Cognition, 20, 187–198.
   PubMed Web of Science ®Google Scholar
• Güntürkün, O., Ströckens, F., & Ocklenburg, S. (2020). Brain lateralization: A comparative perspective. Physiological Reviews, 100, 1019–1063.
   PubMed Web of Science ®Google Scholar
• Heller, W., Nitschke, J. B., Etienne, M. A., & Miller, G. A. (1997). Patterns of regional brain activity differentiate types of anxiety. Journal of Abnormal Psychology, 106, 376–385.
   PubMed Web of Science ®Google Scholar
• Heuts, B. A. (1999). Lateralization of trunk muscle volume, and lateralization of swimming turns of fish responding to external stimuli. Behavioural Processes, 47, 113–124.
   PubMed Web of Science ®Google Scholar
• Howe, K., Clark, M. D., Torroja, C. F., Torrance, J., Berthelot, C., Muffato, M., … Stemple, D. K. (2013). The zebrafish reference genome sequence and its relationship to the human genome. Nature, 496, 498–503.
   PubMed Web of Science ®Google Scholar
• Ijaz, S., & Hoffman, E. J. (2016). Zebrafish: A translational model system for studying neuropsychiatric disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 55, 746–748.
   PubMed Web of Science ®Google Scholar
• Kalin, N. H., Larson, C., Shelton, S. E., & Davidson, R. J. (1998). Asymmetric frontal brain activity, cortisol, and behavior associated with fearful temperament in rhesus monkeys. Behavioral Neuroscience, 112, 286–292.
   PubMed Web of Science ®Google Scholar
• Kalueff, A. V., Stewart, A. M., & Gerlai, R. (2014). Zebrafish as an emerging model for studying complex brain disorders. Trends in Pharmacological Sciences, 35, 63–75.
   PubMed Web of Science ®Google Scholar
• Kozol, R. A., Cukier, H. N., Zou, B., Mayo, V., De Rubeis, S., Cai, G., … Dallman, J. E. (2015). Two knockdown models of the autism genes SYNGAP1 and SHANK3 in zebrafish produce similar behavioral phenotypes associated with embryonic disruptions of brain morphogenesis. Human Molecular Genetics, 24, 4006–4023.
   PubMed Web of Science ®Google Scholar
• Kuan, Y. S., Yu, H. H., Moens, C. B., & Halpern, M. E. (2007). Neuropilin asymmetry mediates a left-right difference in habenular connectivity. Development, 134, 857–865.
   PubMed Web of Science ®Google Scholar
• Leliveld, L. M. C., Langbeina, J., & Puppe, B. (2013). The emergence of emotional lateralization: Evidence in non-human vertebrates and implications for farm animals. Applied Animal Behaviour Science, 145, 1–14.
   Web of Science ®Google Scholar
• Liang, J. O., Etheridge, A., Hantsoo, L., Rubinstein, A. L., Nowak, S. J., Izpisua Belmonte, J. C., & Halpern, M. E. (2000). Asymmetric nodal signaling in the zebrafish diencephalon positions the pineal organ. Development, 127, 5101–5112.
   PubMed Web of Science ®Google Scholar
• Lindell, A. K., & Hudry, K. (2013). Atypicalities in cortical structure, handedness, and functional lateralization for language in autism spectrum disorders. Neuropsychology Review, 23, 257–270.
   PubMed Web of Science ®Google Scholar
• Lippolis, G., Bisazza, A., Rogers, L. J., & Vallortigara, G. (2002). Lateralisation of predator avoidance responses in three species of toads. Laterality: Asymmetries of Body, Brain and Cognition, 7, 163–183.
   PubMed Web of Science ®Google Scholar
• Long, S, & Ahmad, N. (2003). The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development, 130, 2303–2316.
   PubMed Web of Science ®Google Scholar
• Manuel, R., Gorissen, M., Roca, C. P., Zethof, J., van de Vis, H., Flik, G., & van den Bos, R. (2014). Inhibitory avoidance learning in zebrafish (Danio rerio): effects of shock intensity and unraveling differences in task performance. Zebrafish, 11, 341–352.
   PubMed Web of Science ®Google Scholar
• Maximino, C., de Brito, T. M., da Silva Batista, A. W., Herculano, A. M., Morato, S., & GouveiaJrA. (2010a). Measuring anxiety inzebrafish: A critical review. Behavioural Brain Research, 214, 157–171.
   PubMed Web of Science ®Google Scholar
• Maximino, C., de Brito, T. M., de Mattos Dias, C. G., GouveiaJr.A., & Morato, S. (2010b). Scototaxis as anxiety-like behavior in fish. Nature Protocols, 5, 209–216.
   PubMed Web of Science ®Google Scholar
• Maximino, C., de Brito, T. M., Moraes, F. D., Oliveira, F. V. C., Taccolini, I. B., Pereira, P. M., … Gouveia, A. (2007). A comparative analysis of the preference for dark environments in five teleosts. International Journal of Comparative Psychology, 20, 351–367.
   Google Scholar
• Mazzotti, G. A., & Boere, V. (2009). The right ear but not the left ear temperature is related to stress-induced cortisolaemia in the domestic cat (Felis catus). Laterality: Asymmetries of Body, Brain and Cognition, 14, 196–204.
   PubMed Web of Science ®Google Scholar
• Miklosi, A., & Andrew, R. J. (1999). Right eye use associated with decision to bite in zebrafish. Behavioural Brain Research, 105, 199–205.
   PubMed Web of Science ®Google Scholar
• Miletto Petrazzini, M. E., Pecunioso, A., Dadda, M., & Agrillo, C. (2019). The impact of brain lateralization and anxiety-like behaviour in an extensive operant conditioning task in zebrafish (Danio rerio). Symmetry, 11, 1395, doi:10.3390/sym11111395
   Google Scholar
• Miletto Petrazzini, M. E., Sovrano, V. A., Vallortigara, G., & Messina, A. (2020). Brain and Behavioral asymmetry: A Lesson from fish. Frontiers in Neuroanatomy, 14, 11, doi:10.3389/fnana.2020.00011
   PubMed Web of Science ®Google Scholar
• Montgomery, K. C. (1955). The relation between fear induced by novel stimulation and exploratory behavior. Journal of Comparative and Physiological Psychology, 48, 254–260.
   PubMed Web of Science ®Google Scholar
• Ocklenburg, S., & Güntürkün, O. (2012). Hemispheric asymmetries: The comparative view. Frontiers in Psychology, 3, 5, doi:10.3389/fpsyg.2012.00005
   PubMed Web of Science ®Google Scholar
• Parker, M. O., Millington, M. E., Combe, F. J., & Brennan, C. H. (2012). Housing conditions differentially affect physiological and behavioural stress responses of zebrafish, as well as the response to anxiolytics. PLoS ONE, 7(4), e34992.
   PubMed Web of Science ®Google Scholar
• Phillips, R. E., & Youngren, O. M. (1986). Unilateral kainic acid lesions reveal dominance of right archistriatum in avian fear behavior. Brain Research, 377, 216–220.
   PubMed Web of Science ®Google Scholar
• Piato, A. L., Capiotti, K. M., Tamborski, A. R., Oses, J. P., Barcellos, L. J., Bogo, M. R., … Bonan, C. D. (2011). Unpredictable chronic stress model in zebrafish (Danio rerio): Behavioral and physiological responses. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 35, 561–567.
   PubMed Web of Science ®Google Scholar
• Rihel, J., & Schier, A. F. (2012). Behavioral screening for neuroactive drugs in zebrafish. Developmental Neurobiology, 72, 373–385.
   PubMed Web of Science ®Google Scholar
• Rogers, L. J. (2014). Asymmetry of brain and behavior in animals: Its development, function, and human relevance. Genesis, 52, 555–571.
   PubMed Web of Science ®Google Scholar
• Rogers, L. J., & Vallortigara, G. (2015). When and why did brains break symmetry? Symmetry, 7, 2181–2194.
   Google Scholar
• Rogers, L. J., & Vallortigara, G. (2017). Lateralized brain functions: Methods in human and Non-human species. New York, NY: Humana Press.
   Google Scholar
• Rosemberg, D. B., Rico, E. P., Mussulini, B. H., Piato, A. L., Calcagnotto, M. E., Bonan, C. D., … Oliveira, D. L. (2011). Differences in spatio-temporal behavior of zebrafish in the open tank paradigm after a short-period confinement into dark and bright environments. PLoS ONE, 6, e19397.
   PubMed Web of Science ®Google Scholar
• Roussigné, M., Bianco, I. H., Wilson, S. W., & Blader, P. (2009). Nodal signalling imposes left-right asymmetry upon neurogenesis in the habenular nuclei. Development, 136, 1549–1557.
   PubMed Web of Science ®Google Scholar
• Roussigné, M., Blader, P., & Wilson, S. W. (2012). Breaking symmetry: The zebrafish as a model for understanding left-right asymmetry in the developing brain. Developmental Neurobiology, 72, 269–281.
   PubMed Web of Science ®Google Scholar
• Royer, C., Delcroix, N., Leroux, E., Alary, M., Razafimandimby, A., Brazo, P., … Dollfus, S. (2016). Functional and structural brain asymmetries in patients with schizophrenia and bipolar disorders. Schizophrenia Research, 161, 210–214.
   Web of Science ®Google Scholar
• Séguret, A., Collignon, B., & Halloy, J. (2016). Strain differences in the collective behaviour of zebrafish (Danio rerio) in heterogeneous environment. Royal Society Open Science, 3, 160451.
   PubMed Web of Science ®Google Scholar
• Singer, M. L., Oreschak, K., Rhinehart, Z., & Robison, B. D. (2016). Anxiolytic effects of fluoxetine and nicotine exposure on exploratory behavior in zebrafish. PeerJ, 4, e2352.
   PubMed Web of Science ®Google Scholar
• Siniscalchi, M., Sasso, R., Pepe, A. M., Vallortigara, G., & Quaranta, A. (2010). Dogs turn left to emotional stimuli. Behavioural Brain Research, 208, 516–521.
   PubMed Web of Science ®Google Scholar
• Sovrano, V. A., & Andrew, R. J. (2006). Eye use during viewing a reflection: Behavioural lateralisation in zebrafish larvae. Behavioural Brain Research, 167, 226–231.
   PubMed Web of Science ®Google Scholar
• Sovrano, V. A., Bisazza, A., & Vallortigara, G. (2001). Lateralization of response to social stimuli in fishes: A comparison between different methods and species. Physiology & Behavior, 74, 237–244.
   PubMed Web of Science ®Google Scholar
• Spence, R., Magurran, A. E., & Smith, C. (2011). Spatial cognition in zebrafish: The role of strain and rearing environment. Animal Cognition, 14, 607–612.
   PubMed Web of Science ®Google Scholar
• Stewart, A. M., Braubach, O., & Spitsbergen, J. (2014). Zebrafish models for translational neuroscience research: From tank to bedside. Trends in Neurosciences, 37, 264–278.
   PubMed Web of Science ®Google Scholar
• Stewart, A., Gaikwad, S., Kyzar, E., Green, J., Roth, A., & Kalueff, A. V. (2012). Modeling anxiety using adult zebrafish: A conceptual review. Neuropharmacology, 62, 135–143.
   PubMed Web of Science ®Google Scholar
• Sullivan, R. M, & Gratton, A. (1999). Lateralized effects of medial prefrontal cortex lesions on neuroendocrine and autonomic stress responses in rats. Journal of Neuroscience, 19, 2834–2840.
   PubMed Web of Science ®Google Scholar
• Tomaz, C., Verburg, M. S., Boere, V., Pianta, T. F., & Belo, M. (2003). Evidence of hemispheric specialization in marmosets (Callithrix penicillata) using tympanic membrane thermometry. Brazilian Journal of Medical and Biological Research, 36, 913–918.
   PubMed Web of Science ®Google Scholar
• Vallortigara, G., & Rogers, L. J. (2020). A function for the bicameral mind. Cortex, 124, 274–285.
   PubMed Web of Science ®Google Scholar
• Vignet, C., Bégout, M., Péan, S., Lyphout, L., Leguay, D., & Cousin, X. (2013). Systematic screening of behavioral responses in two zebrafish strains. Zebrafish, 10, 365–375.
   PubMed Web of Science ®Google Scholar
• Vital, C., & Martins, E. P. (2011). Strain differences in zebrafish (Danio rerio) social roles and their impact on group task performance. Journal of Comparative Psychology, 125, 278–285.
   PubMed Web of Science ®Google Scholar
• Volkova, K., Caspillo, N. R., Porseryd, T., Hallgren, S., Dinnetz, P., & Porsch-Hallstrom, I. (2015). Developmental exposure of zebrafish (Danio rerio) to 17alpha-ethinylestradiol affects non-reproductive behavior and fertility as adults, and increases anxiety in unexposed progeny. Hormones and Behavior, 73, 30–38.
   PubMed Web of Science ®Google Scholar
• Watkins, J., Miklosi, A., & Andrew, R. J. (2004). Early asymmetries in the behaviour of zebrafish larvae. Behavioural Brain Research, 151, 177–183.
   PubMed Web of Science ®Google Scholar
• Young, E. J., & Williams, C. L. (2013). Differential activation of amygdala Arc expression by positive and negatively valenced emotional learning conditions. Frontiers in Behavioral Neuroscience, 7, 191, doi:10.3389/fnbeh.2013.00191
   PubMed Web of Science ®Google Scholar
• Ziv, L., Muto, A., Schoonheim, P. J., Meijsing, S. H., Strasser, D., Ingraham, H. A., … Baier, H. (2013). An affective disorder in zebrafish with mutation of the glucocorticoid receptor. Molecular Psychiatry, 18, 681–691.
   PubMed Web of Science ®Google Scholar