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Npas4a expression in the teleost forebrain is associated with stress coping style differences in fear learning

  • 1.

    Baker, M. R., Hofmann, H. A. & Wong, R. Y. Neurogenomics of Behavioural Plasticity in Socioecological Contexts (Wiley, 2001).

    Book 

    Google Scholar 

  • 2.

    Koolhaas, J. M. et al. Coping styles in animals: Current status in behavior and stress-physiology. Neurosci. Biobehav. Rev. 23(7), 925–935 (1999).

    CAS 
    Article 

    Google Scholar 

  • 3.

    Koolhaas, J. M., de Boer, S. F., Coppens, C. M. & Buwalda, B. Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Front. Neuroendocrinol. 31(3), 307–321 (2010).

    CAS 
    Article 

    Google Scholar 

  • 4.

    Øverli, Ø. et al. Evolutionary background for stress-coping styles: Relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci. Biobehav. Rev. 31(3), 396–412 (2007).

    Article 

    Google Scholar 

  • 5.

    Brown, G. E. et al. Retention of acquired predator recognition among shy versus bold juvenile rainbow trout. Behav. Ecol. Sociobiol. 67(1), 43–51 (2013).

    Article 

    Google Scholar 

  • 6.

    Dougherty, L. R. & Guillette, L. M. Linking personality and cognition: a meta-analysis. Philos. Trans. R. Soc. B. Biol. Sci. https://doi.org/10.1098/rstb.2017.0282 (2018).

    Article 

    Google Scholar 

  • 7.

    Lucon-Xiccato, T. & Bisazza, A. Individual differences in cognition among teleost fishes. Behav. Process. 141, 184–195 (2017).

    Article 

    Google Scholar 

  • 8.

    Miller, N. Cognition in fishes. Behav. Process. https://doi.org/10.1016/j.beproc.2017.03.013 (2017).

    Article 

    Google Scholar 

  • 9.

    Sih, A. & Del Giudice, M. Linking behavioural syndromes and cognition: A behavioural ecology perspective. Philos. Trans. R. Soc. B. Biol. Sci. 367(1603), 2762–2772 (2012).

    Article 

    Google Scholar 

  • 10.

    Amy, M., van Oers, K. & Naguib, M. Worms under cover: Relationships between performance in learning tasks and personality in great tits (Parus major). Anim. Cogn. https://doi.org/10.1007/s10071-012-0500-3 (2012).

    Article 
    PubMed 

    Google Scholar 

  • 11.

    Bolhuis, J. E., Schouten, W. G. P., De, L. J. A., Schrama, J. W. & Wiegant, V. M. Individual coping characteristics, rearing conditions and behavioural flexibility in pigs. Behav. Brain Res. 152(2), 351–360 (2004).

    Article 

    Google Scholar 

  • 12.

    DePasquale, C., Wagner, T., Archard, G. A., Ferguson, B. & Braithwaite, V. A. Learning rate and temperament in a high predation risk environment. Oecologia 176(3), 661–667 (2014).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 13.

    Dugatkin, L. A. & Alfieri, M. S. Boldness, behavioral inhibition and learning. Ethol. Ecol. Evol. 15(1), 43–49 (2003).

    Article 

    Google Scholar 

  • 14.

    Mazza, V., Eccard, J. A., Zaccaroni, M., Jacob, J. & Dammhahn, M. The fast and the flexible: Cognitive style drives individual variation in cognition in a small mammal. Anim. Behav. https://doi.org/10.1016/j.anbehav.2018.01.011 (2018).

    Article 

    Google Scholar 

  • 15.

    Mesquita, F. O., Borcato, F. L. & Huntingford, F. A. Cue-based and algorithmic learning in common carp: A possible link to stress coping style. Behav. Process. 115, 25–29 (2015).

    Article 

    Google Scholar 

  • 16.

    Trompf, L. & Brown, C. Personality affects learning and trade-offs between private and social information in guppies, Poecilia reticulata. Anim. Behav. 88, 99–106 (2014).

    Article 

    Google Scholar 

  • 17.

    Budaev, S. V. & Zhuikov, A. Y. Avoidance learning and “personality” in the guppy (Poecilia reticulata). J. Comp. Psychol. 112(1), 92–94 (1998).

    Article 

    Google Scholar 

  • 18.

    Exnerová, A., Svádová, K. H., Fučíková, E., Drent, P. & Štys, P. Personality matters: Individual variation in reactions of naive bird predators to aposematic prey. Proc. R. Soc. B. Biol. Sci. https://doi.org/10.1098/rspb.2009.1673 (2010).

    Article 

    Google Scholar 

  • 19.

    Miller, K. A., Garner, J. P. & Mench, J. A. Is fearfulness a trait that can be measured with behavioural tests? A validation of four fear tests for Japanese quail. Anim Behav. https://doi.org/10.1016/j.anbehav.2005.08.018 (2006).

    Article 

    Google Scholar 

  • 20.

    Øverli, Ø. & Sørensen, C. On the role of neurogenesis and neural plasticity in the evolution of animal personalities and stress coping styles. Brain Behav. Evol. https://doi.org/10.1159/000447085 (2016).

    Article 
    PubMed 

    Google Scholar 

  • 21.

    Sørensen, C., Johansen, I. B. & Øverli, Ø. Neural plasticity and stress coping in teleost fishes. Gen. Comp. Endocrinol. https://doi.org/10.1016/j.ygcen.2012.12.003 (2013).

    Article 
    PubMed 

    Google Scholar 

  • 22.

    Wong, R. Y., Lamm, M. S. & Godwin, J. Characterizing the neurotranscriptomic states in alternative stress coping styles. BMC Genom. 16(1), 425 (2015).

    Article 

    Google Scholar 

  • 23.

    Oswald, M. E., Singer, M. & Robison, B. D. The quantitative genetic architecture of the bold-shy continuum in zebrafish, Denio rerio. PLoS ONE 8(7), e28865. https://doi.org/10.1371/journal.pone.0068828 (2013).

    CAS 
    Article 

    Google Scholar 

  • 24.

    Kfir, A. et al. Learning-induced modulation of the GABAB-mediated inhibitory synaptic transmission: Mechanisms and functional significance. J.. Neurophysiol. https://doi.org/10.1152/jn.00004.2014 (2014).

    Article 
    PubMed 

    Google Scholar 

  • 25.

    Lin, Y. et al. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature https://doi.org/10.1038/nature07319 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 26.

    Maya-Vetencourt, J. F. et al. Experience-dependent expression of NPAS4 regulates plasticity in adult visual cortex. J. Physiol. https://doi.org/10.1113/jphysiol.2012.234237 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 27.

    Heaney, C. F. & Kinney, J. W. Role of GABABreceptors in learning and memory and neurological disorders. Neurosci. Biobehav. Rev. https://doi.org/10.1016/j.neubiorev.2016.01.007 (2016).

    Article 
    PubMed 

    Google Scholar 

  • 28.

    Ploski, J. E., Monsey, M. S., Nguyen, T., DiLeone, R. J. & Schafe, G. E. The neuronal PAS domain protein 4 (Npas4) is required for new and reactivated fear memories. PLoS ONE https://doi.org/10.1371/journal.pone.0023760 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 29.

    Ramamoorthi, K. et al. Npas4 regulates a transcriptional program in CA3 required for contextual memory formation. Science https://doi.org/10.1126/science.1208049 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 30.

    Baker, M. R. & Wong, R. Y. Contextual fear learning and memory differ between stress coping styles in zebrafish. Sci. Rep. https://doi.org/10.1038/s41598-019-46319-0 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 31.

    Maren, S., Phan, K. L. & Liberzon, I. The contextual brain: Implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. https://doi.org/10.1038/nrn3492 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 32.

    Lal, P. et al. Identification of a neuronal population in the telencephalon essential for fear conditioning in zebrafish. BMC Biol. https://doi.org/10.1186/s12915-018-0502-y (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 33.

    Ganz, J. et al. Subdivisions of the adult zebrafish pallium based on molecular marker analysis. F1000 Res. https://doi.org/10.12688/f1000research.5595.2 (2015).

    Article 

    Google Scholar 

  • 34.

    de CarmoSilva, R. X., Lima-Maximino, M. G. & Maximino, C. The aversive brain system of teleosts: Implications for neuroscience and biological psychiatry. Neurosci. Biobehav. Rev. https://doi.org/10.1016/j.neubiorev.2018.10.001 (2018).

    Article 

    Google Scholar 

  • 35.

    Panula, P. et al. The comparative neuroanatomy and neurochemistry of zebrafish CNS systems of relevance to human neuropsychiatric diseases. Neurobiol. Dis. https://doi.org/10.1016/j.nbd.2010.05.010 (2010).

    Article 
    PubMed 

    Google Scholar 

  • 36.

    Wong, R. Y. et al. Comparing behavioral responses across multiple assays of stress and anxiety in zebrafish (Danio rerio). Behaviour 149(10–12), 1205–1240 (2012).

    Google Scholar 

  • 37.

    Kern, E. M. A., Robinson, D., Gass, E., Godwin, J. & Langerhans, R. B. Correlated evolution of personality, morphology and performance. Anim. Behav. 117, 79–86 (2016).

    Article 

    Google Scholar 

  • 38.

    Wong, R. Y., McLeod, M. M. & Godwin, J. Limited sex-biased neural gene expression patterns across strains in Zebrafish (Danio rerio). BMC Genom. 15(1), 905. https://doi.org/10.1186/1471-2164-15-905 (2014).

    Article 

    Google Scholar 

  • 39.

    Wong, R. Y., Oxendine, S. E. & Godwin, J. Behavioral and neurogenomic transcriptome changes in wild-derived zebrafish with fluoxetine treatment. BMC Genom. 14(1), 348 (2013).

    CAS 
    Article 

    Google Scholar 

  • 40.

    Goodman, A. C. & Wong, R. Y. Differential effects of ethanol on behavior and GABAA receptor expression in adult zebrafish (Danio rerio) with alternative stress coping styles. Sci. Rep. https://doi.org/10.1038/s41598-020-69980-2 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 41.

    Baker, M. R., Goodman, A. C., Santo, J. B. & Wong, R. Y. Repeatability and reliability of exploratory behavior in proactive and reactive zebrafish Danio rerio. Sci. Rep. https://doi.org/10.1038/s41598-018-30630-3 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 42.

    Johnson, Z. V. et al. Exploratory behaviour is associated with microhabitat and evolutionary radiation in Lake Malawi cichlids. Anim. Behav. https://doi.org/10.1016/j.anbehav.2019.11.006 (2020).

    Article 

    Google Scholar 

  • 43.

    Gerlai, R. Learning and memory in zebrafish (Danio rerio). Methods Cell Biol. https://doi.org/10.1016/bs.mcb.2016.02.005 (2016).

    Article 
    PubMed 

    Google Scholar 

  • 44.

    Norton, W. & Bally-Cuif, L. Adult zebrafish as a model organism for behavioural genetics. BMC Neurosci. https://doi.org/10.1186/1471-2202-11-90 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 45.

    Oliveira, R. F. Mind the fish: Zebrafish as a model in cognitive social neuroscience. Front. Neural Circuits https://doi.org/10.3389/fncir.2013.00131 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 46.

    Wong, R. Y., French, J. & Russ, J. B. Differences in stress reactivity between zebrafish with alternative stress coping styles. R. Soc. Open Sci. https://doi.org/10.1098/rsos.181797 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 47.

    Maren, S. Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci. https://doi.org/10.1146/annurev.neuro.24.1.897 (2001).

    Article 
    PubMed 

    Google Scholar 

  • 48.

    McCurley, A. T. & Callard, G. V. Characterization of housekeeping genes in zebrafish: Male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol. Biol. https://doi.org/10.1186/1471-2199-9-102 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 49.

    Wong, R. Y., Ramsey, M. E. & Cummings, M. E. Localizing brain regions associated with female mate preference behavior in a swordtail. PLoS ONE https://doi.org/10.1371/journal.pone.0050355 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 50.

    Wong, R. Y. & Cummings, M. E. Expression patterns of Neuroligin-3 and tyrosine hydroxylase across the brain in mate choice contexts in female swordtails. Brain Behav Evol https://doi.org/10.1159/000360071 (2014).

    Article 
    PubMed 

    Google Scholar 

  • 51.

    Wullimann, M. F., Rupp, B. & Reichert, H. Neuroanatomy of the zebrafish brain: A topological. Atlas https://doi.org/10.1007/978-3-0348-8979-7 (1996).

    Article 

    Google Scholar 

  • 52.

    Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N. & Golani, I. Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 125(1–2), 279–284 (2001).

    CAS 
    Article 

    Google Scholar 

  • 53.

    Wassertheil, S. & Cohen, J. Statistical power analysis for the behavioral sciences. Biometrics https://doi.org/10.2307/2529115 (1970).

    Article 

    Google Scholar 

  • 54.

    Starkings, S. IBM SPSS statistics 19 made simple by Colin D. Gray and Paul R. Kinnear. Int. Stat. Rev. https://doi.org/10.1111/j.1751-5823.2012.00187_13.x (2012).

    Article 

    Google Scholar 

  • 55.

    Richardson, J. T. E. Eta squared and partial eta squared as measures of effect size in educational research. Educ. Res. Rev. https://doi.org/10.1016/j.edurev.2010.12.001 (2011).

    Article 

    Google Scholar 

  • 56.

    Benito, E. & Barco, A. The neuronal activity-driven transcriptome. Mol. Neurobiol. https://doi.org/10.1007/s12035-014-8772-z (2015).

    Article 
    PubMed 

    Google Scholar 

  • 57.

    Vertkin, I. et al. GABA B receptor deficiency causes failure of neuronal homeostasis in hippocampal networks. Proc. Natl. Acad. Sci. https://doi.org/10.1073/pnas.1424810112 (2015).

    Article 
    PubMed 

    Google Scholar 

  • 58.

    von Trotha, J. W., Vernier, P. & Bally-Cuif, L. Emotions and motivated behavior converge on an amygdala-like structure in the zebrafish. Eur. J. Neurosci. https://doi.org/10.1111/ejn.12692 (2014).

    Article 

    Google Scholar 

  • 59.

    Ganz, J. et al. Subdivisions of the adult zebrafish subpallium by molecular marker analysis. J. Comp. Neurol. https://doi.org/10.1002/cne.22757 (2012).

    Article 
    PubMed 

    Google Scholar 

  • 60.

    Perathoner, S., Cordero-Maldonado, M. L. & Crawford, A. D. Potential of zebrafish as a model for exploring the role of the amygdala in emotional memory and motivational behavior. J. Neurosci. Res. https://doi.org/10.1002/jnr.23712 (2016).

    Article 
    PubMed 

    Google Scholar 

  • 61.

    Qiu, J. et al. Decreased Npas4 and Arc mRNA levels in the hippocampus of aged memory-impaired wild-type but not memory preserved 11β-HSD1 deficient mice. J. Neuroendocrinol. https://doi.org/10.1111/jne.12339 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 62.

    Vindas, M. A. et al. How do individuals cope with stress? Behavioural, physiological and neuronal differences between proactive and reactive coping styles in fish. J. Exp. Biol. https://doi.org/10.1242/jeb.153213 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 63.

    Øverli, Ø., Pottinger, T. G., Carrick, T. R., Øverli, E. & Winberg, S. Brain monoaminergic activity in rainbow trout selected for high and low stress responsiveness. Brain. Behav. Evol. https://doi.org/10.1159/000047238 (2001).

    Article 
    PubMed 

    Google Scholar 

  • 64.

    Walker, D. L., Toufexis, D. J. & Davis, M. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur. J. Pharmacol. https://doi.org/10.1016/S0014-2999(03)01282-2 (2003).

    Article 
    PubMed 

    Google Scholar 

  • 65.

    Goode, T. D. & Maren, S. Role of the bed nucleus of the stria terminalis in aversive learning and memory. Learn. Mem. https://doi.org/10.1101/lm.044206.116 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 66.

    Henckens, M. J. A. G. et al. CRF receptor type 2 neurons in the posterior bed nucleus of the stria terminalis critically contribute to stress recovery. Mol. Psychiatry https://doi.org/10.1038/mp.2016.133 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 67.

    Rink, E. & Wullimann, M. F. Connections of the ventral telencephalon (subpallium) in the zebrafish (Danio rerio). Brain Res. https://doi.org/10.1016/j.brainres.2004.03.027 (2004).

    Article 
    PubMed 

    Google Scholar 

  • 68.

    Boulton, K. et al. How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model. Ecol. Evol. 5(3), 618–633 (2015).

    Article 

    Google Scholar 

  • 69.

    Baugh, A. T. et al. Corticosterone responses differ between lines of great tits (Parus major) selected for divergent personalities. Gen. Comp. Endocrinol. 175(3), 488–494 (2012).

    CAS 
    Article 

    Google Scholar 

  • 70.

    Wong RY, French J, Russ JB (2018) Differences in stress reactivity between zebrafish with alternative stress coping styles. Dissertation (University of Nebraska at Omaha).

  • 71.

    Furukawa-Hibi, Y., Yun, J., Nagai, T. & Yamada, K. Transcriptional suppression of the neuronal PAS domain 4 (Npas4) gene by stress via the binding of agonist-bound glucocorticoid receptor to its promoter. J. Neurochem. https://doi.org/10.1111/jnc.12034 (2012).

    Article 
    PubMed 

    Google Scholar 

  • 72.

    Ibi, D. et al. Social isolation rearing-induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion-related behaviors in juvenile mice. J. Neurochem. https://doi.org/10.1111/j.1471-4159.2007.05207.x (2008).

    Article 
    PubMed 

    Google Scholar 

  • 73.

    Yun, J. et al. Chronic restraint stress impairs neurogenesis and hippocampus-dependent fear memory in mice: Possible involvement of a brain-specific transcription factor Npas4. J. Neurochem. https://doi.org/10.1111/j.1471-4159.2010.06893.x (2010).

    Article 
    PubMed 

    Google Scholar 

  • 74.

    Sun, X. & Lin, Y. Npas4: Linking neuronal activity to memory. Trends Neurosci. https://doi.org/10.1016/j.tins.2016.02.003 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 75.

    Makkar, S. R., Zhang, S. Q. & Cranney, J. Behavioral and neural analysis of GABA in the acquisition, consolidation, reconsolidation, and extinction of fear memory. Neuropsychopharmacology https://doi.org/10.1038/npp.2010.53 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 


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