Skip to main content

Advertisement

Springer Nature Link
Log in

Effects of single and repeated heat stress on anxiety-like behavior and locomotor activity in medaka fish

  • Original Article
  • Biology
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

In this study, we examined whether a single heat stress incident and long-term repeated heat stress could affect behavioral and neural responses in male medaka fish Oryzias latipes. By using the novel tank diving test, we found that 7-day repeated heat stress led to anxiety-like behaviors and suppressed locomotor activity, whereas fluoxetine treatment during repeated heat stress led to anxiolytic behaviors. Furthermore, a single heat stress incident increased hyper-locomotor activity. A single heat stress incident decreased mRNA expression of tryptophan hydroxylase 2 (tph2), a rate-limiting enzyme in serotonin biosynthesis, while a single heat stress increased mRNA expression of tyrosine hydroxylase 1 (th1) and tyrosine hydroxylase 2 (th2), catalyzing dopamine biosynthesis in the brain. Plasma cortisol concentration increased after a single stress, repeated stress, and fluoxetine treatment during repeated stress. These results suggest that medaka fish are a good model for assessing anxiety-like behavior induced by long-term repeated stress. Moreover, th1, th2, and tph2 in the brain would be key factors in the exploration of the central regulation of behavioral responses to a single and repeated stress in fish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Anichtchik OV, Kaslin J, Peitsaro N, Scheinin M, Panula P (2004) Neurochemical and behavioural changes in zebrafish Danio rerio after systemic administration of 6-hydroxydopamine and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J Neurochem 88:443–453

    CAS  PubMed  Google Scholar 

  • Ansai S, Hosokawa H, Maegawa S, Kinoshita M (2016) Chronic fluoxetine treatment induces anxiolytic responses and altered social behaviors in medaka, Oryzias latipes. Behav Brain Res 303:126–136

    CAS  PubMed  Google Scholar 

  • Ansai S, Hosokawa H, Maegawa S, Naruse K, Washio Y, Sato K, Kinoshita M (2017) Deficiency of serotonin in raphe neurons and altered behavioral responses in tryptophan hydroxylase 2-knockout medaka (Oryzias latipes). Zebrafish 14:495–507

    CAS  PubMed  Google Scholar 

  • Bai Y, Liu H, Huang B, Wagle M, Guo S (2016) Identification of environmental stressors and validation of light preference as a measure of anxiety in larval zebrafish. BMC Neurosci. https://doi.org/10.1186/s12868-016-0298-z

    Article  PubMed  PubMed Central  Google Scholar 

  • Basu N, Nakano T, Grau EG, Iwama GK (2001) The effects of cortisol on heat shock protein 70 levels in two fish species. Gen Comp Endocrinol 124:97–105

    CAS  PubMed  Google Scholar 

  • Burgado J, Harrell CS, Eacret D, Reddy R, Barnum CJ, Tansey MG, Miller AH, Wang H, Neigh GN (2014) Two weeks of predatory stress induces anxiety-like behavior with co-morbid depressive-like behavior in adult male mice. Behav Brain Res 275:120–125

    PubMed  PubMed Central  Google Scholar 

  • Carpenter RE, Watt MJ, Forster GL, Øverli Ø, Bockholt C, Renner KJ, Summers CH (2007) Corticotropin releasing factor induces anxiogenic locomotion in trout and alters serotonergic and dopaminergic activity. Horm Behav 52:600–611

    CAS  PubMed  PubMed Central  Google Scholar 

  • Champagne DL, Hoefnagels CCM, Kloet RE, Richardson MK (2010) Translating rodent behavioral repertoire to zebrafish (Danio rerio): Relevance for stress research. Behav Brain Res. https://doi.org/10.1016/j.bbr.2010.06.001

    Article  PubMed  Google Scholar 

  • Chen Y, Xu H, Zhu M, Liu K, Lin B, Luo R, Chen C, Li M (2017) Stress inhibits tryptophan hydroxylase expression in a rat model of depression. Oncotarget 8:63247–63257

    PubMed  PubMed Central  Google Scholar 

  • Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological Stress and Disease. Jama 298:1685–1687

    CAS  PubMed  Google Scholar 

  • Egan RJ, Bergner CL, Hart PC, Cachat JM, Canavello PR, Elegante MF, Elkhayat SI, Bartels BK, Tien AK, Tien DH, Mohnot S, Beeson E, Glasgow E, Amri H, Zukowska Z, Kalueff AV (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 205:38–44

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez SP, Broussot L, Marti F, Contesse T, Mouska X, Soiza-Reilly M, Marie H, Faure P, Barik J (2018) Mesopontine cholinergic inputs to midbrain dopamine neurons drive stress-induced depressive-like behaviors. Nat Commun. https://doi.org/10.1038/s41467-018-06809-7

    Article  PubMed  PubMed Central  Google Scholar 

  • Fraser TWK, Vindas MA, Fjelldal PG, Winberg S, Thörnqvist PO, Øverli Ø, Skjæraasen JE, Hansen TJ, Mayer I (2015) Increased reactivity and monoamine dysregulation following stress in triploid Atlantic salmon (Salmo salar). Comp Biochem Physiol A 185:125–131

    CAS  Google Scholar 

  • Fulcher N, Tran S, Shams S, Chatterjee D, Gerlai R (2017) Neurochemical and behavioral responses to unpredictable chronic mild stress following developmental isolation: The zebrafish as a model for major depression. Zebrafish 14:23–34

    CAS  PubMed  Google Scholar 

  • Gaikwad S, Stewart A, Hart P, Wong K, Piet V, Cachat J, Kalueff AV (2011) Acute stress disrupts performance of zebrafish in the cued and spatial memory tests: the utility of fish models to study stress-memory interplay. Behav Processes 87:224–230

    PubMed  Google Scholar 

  • Garcia-Iglesias BB, Mendoza-Garrido ME, Gutierrez-Ospina G, Rangel-Barajas C, Noyola-Diaz M, Terron JA (2013) Sensitization of restraint-induced corticosterone secretion after chronic restraint in rats: involvement of 5-HT7 receptors. Neuropharmacol 71:216–227

    CAS  Google Scholar 

  • Gardner KL, Hale MW, Oldfield S, Lightman SL, Plotsky PM, Lowry CA (2009) Adverse experience during early life and adulthood interact to elevate tph2 mRNA expression in serotonergic neurons within the dorsal raphe nucleus. Neurosci 163:991–1001

    CAS  Google Scholar 

  • Gesto M, Soengas JL, Miguez JM (2008) Acute and prolonged stress responses of brain monoaminergic activity and plasma cortisol levels in rainbow trout are modified by PAHs (naphthalene, beta-naphthoflavone and benzo(a)pyrene) treatment. Aquat Toxicol 86:341–351

    CAS  PubMed  Google Scholar 

  • Ghisleni G, Capiotti KM, Da Silva RS, Oses JP, Piato ÂL, Soares V, Bogo MR, Bonan CD (2012) The role of CRH in behavioral responses to acute restraint stress in zebrafish. Prog Neuropsychopharmacol Biol Psychiatry 36:176–182

    CAS  PubMed  Google Scholar 

  • Giacomini ACVV, Abreu MS, Giacomini LV, Siebel AM, Zimerman FF, Rambo CL, Moceline R, Bonan CD, Piato AL, Barcellos LJG (2016) Fluoxetine and diazepam acutely modulate stress induced-behavior. Behav Brain Res 296:301–310

    CAS  PubMed  Google Scholar 

  • Higuchi Y, Soga T, Parhar IS (2018) ocial defeat stress decreases mRNA for monoamine oxidase A and increases 5-HT turnover in the brain of male Nile tilapia (Oreochromis niloticus). Front Pharmacol. https://doi.org/10.3389/fphar.2018.01549

    Article  PubMed  Google Scholar 

  • Kagawa N (2013) Social rank-dependent expression of arginine vasotocin in distinct preoptic regions in male Oryzias latipes. J Fish Biol 82:354–363

    CAS  PubMed  Google Scholar 

  • Kagawa N, Mugiya Y (2000) Exposure of goldfish (Carassius auratus) to bluegills (Lepomis macrochirus) enhances expression of stress protein 70 mRNA in the brains and increases plasma cortisol levels. Zool Sci 17:1061–1066

    CAS  Google Scholar 

  • Kawabata Y, Hiraki T, Takeuchi A, Okubo K (2012) Sex differences in the expression of vasotocin/isotocin, gonadotropin-releasing hormone, and tyrosine and tryptophan hydroxylase family genes in the medaka brain. Neurosci 218:65–77

    CAS  Google Scholar 

  • Li H, Liu Y, Gao X, Liu L, Amuti S, Wu D, Jiang F, Huang L, Wang G, Zeng J, Ma B, Yuan Q (2019) Neuroplastin 65 modulates anxiety- and depression-like behavior likely through adult hippocampal neurogenesis and central 5-HT activity. FEBS J 286:3401–3415

    CAS  PubMed  Google Scholar 

  • Lima-Maximino M, Pyterson MP, do Carmo Silva RX, Gomes GCV, Rocha SP, Herculano AM, Rosemberg DB, Maximino C (2020) Phasic and tonic serotonin modulate alarm reactions and post-exposure behavior in zebrafish. J Neurochem 153:495–509

    PubMed  Google Scholar 

  • Lv H, Zhu C, Wu R, Ni H, Lian J, Xu Y, Xia Y, Shi G, Li Z, Caldwell RB, Caldwell RW, Yao L, Chen Y (2019) Chronic mild stress induced anxiety-like behaviors can be attenuated by inhibition of NOX2-derived oxidative stress. J Psychiatr Res 114:55–66

    PubMed  Google Scholar 

  • Mahar I, Bambico FR, Mechawar N, Nobrega JN (2014) Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects. Neurosci Biobehav Rev 38:173–192

    CAS  PubMed  Google Scholar 

  • Malagié I, Trillat AC, Jacquot C, Gardier AM (1995) Effects of acute fluoxetine on extracellular serotonin levels in the raphe: an in vivo microdialysis study. Eur J Pharmacol 286:213–217

    PubMed  Google Scholar 

  • Matsuda K, Hagiwara Y, Shibata H, Sakashita A, Wada K (2013) Ovine corticotropin-releasing hormone (oCRH) exerts an anxiogenic-like action in the goldfish, Carassius auratus. Gen Comp Endocrinol 188:118–122

    CAS  PubMed  Google Scholar 

  • Matsui H, Taniguchi Y, Inoue H, Uemura K, Takeda S, Takahashi R (2009) A chemical neurotoxin, MPTP induces Parkinson’s disease like phenotype, movement disorders and persistent loss of dopamine neurons in medaka fish. Neurosci Res 65:263–271

    CAS  PubMed  Google Scholar 

  • Matsumoto Y, Oota H, Asaoka Y, Nishina H, Watanabe K, Bujnicki JM, Oda S, Kawamura S, Mitani H (2009) Medaka: a promising model animal for comparative population genomics. BMC Res Notes. https://doi.org/10.1186/1756-0500-2-88

    Article  PubMed  PubMed Central  Google Scholar 

  • Maximino C, de Brito TM, da Silva Batista AW, Herculano AM, Morato S, Gouveia A (2010) Measuring anxiety in zebrafish: a critical review. Behav Brain Res 214:157–171

    PubMed  Google Scholar 

  • Moltesen M, Laursen DC, Thornqvist PO, Andersson MA, Winberg S, Hoglund E (2016) Effects of acute and chronic stress on telencephalic neurochemistry and gene expression in rainbow trout (Oncorhynchus mykiss). J Exp Biol 219:3907–3914

    PubMed  Google Scholar 

  • Munoz-Villegas P, Rodriguez VM, Giordano M, Juarez J (2017) Risk-taking, locomotor activity and dopamine levels in the nucleus accumbens and medial prefrontal cortex in male rats treated prenatally with alcohol. Pharmacol Biochem Behav 153:88–96

    CAS  PubMed  Google Scholar 

  • Nakayasu T, Watanabe E (2014) Biological motion stimuli are attractive to medaka fish. Anim Cogn 17:559–575

    PubMed  Google Scholar 

  • Otsuka A, Shimomura K, Niwa H, Kagawa N (2020) The presence of a conspecific induces risk-taking behaviour and enlargement of somata size of dopaminergic neurons in the brain of male medaka fish. J Fish Biol 96:1014–1023

    CAS  PubMed  Google Scholar 

  • Padilla S, Cowden J, Hinton DE, Yuen B, Law S, Kullman SW, Johnson R, Hardman RC, Flynn K, Au DW (2009) Use of medaka in toxicity testing. Curr Protoc Toxicol. https://doi.org/10.1002/0471140856.tx0110s39

    Article  PubMed  PubMed Central  Google Scholar 

  • Paterson G, Metcalfe CD (2008) Uptake and depuration of the anti-depressant fluoxetine by the Japanese medaka (Oryzias latipes). Chemosphere 74:125–130

    CAS  PubMed  Google Scholar 

  • Pickering AD (1992) Rainbow trout husbandry: management of the stress response. Aquaculture 100:125–139

    Google Scholar 

  • Pickering AD, Pottinger TG (1989) Stress responses and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiol Biochem 7:253–258

    CAS  PubMed  Google Scholar 

  • Rahman MS, Thomas P (2009) Molecular cloning, characterization and expression of two tryptophan hydroxylase (TPH-1 and TPH-2) genes in the hypothalamus of Atlantic croaker: down-regulation after chronic exposure to hypoxia. Neurosci 158:751–765

    CAS  Google Scholar 

  • Rahman MS, Thomas P (2014) Restoration of tryptophan hydroxylase functions and serotonin content in the Atlantic croaker hypothalamus by antioxidant treatment during hypoxic stress. Front Neurosci. https://doi.org/10.3389/fnins.2014.00130

    Article  PubMed  PubMed Central  Google Scholar 

  • Rambo CL, Mocelin R, Marcon M, Villanova D, Koakoski G, de Abreu MS, Oliveira TA, Barcellos LJG, Piato AL, Bonan CD (2017) Gender differences in aggression and cortisol levels in zebrafish subjected to unpredictable chronic stress. Physiol Behav 171:50–54

    CAS  PubMed  Google Scholar 

  • Robinson BL, Dumas M, Cuevas E, Gu Q, Paule MG, Ali SF, Kanungo J (2016) Distinct effects of ketamine and acetyl L-carnitine on the dopamine system in zebrafish. Neurotoxicol Teratol 54:52–60

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schjolden J, Pulman KG, Pottinger TG, Tottmar O, Winberg S (2006) Serotonergic characteristics of rainbow trout divergent in stress responsiveness. Physiol Behav 87:938–947

    CAS  PubMed  Google Scholar 

  • Shimomura Y, Inahata M, Komori M, Kagawa N (2019) Reduction of tryptophan hydroxylase expression in the brain of medaka fish after repeated heat stress. Zool Sci 36:223–230

    CAS  Google Scholar 

  • Thompson RR, Paul ES, Radford AN, Purser J, Mendl M (2016) Routine handling methods affect behaviour of three-spined sticklebacks in a novel test of anxiety. Behav Brain Res 306:26–35

    PubMed  PubMed Central  Google Scholar 

  • Tran S, Chatterjee D, Gerlai R (2014) Acute net stressor increases whole-body cortisol levels without altering whole-brain monoamines in zebrafish. Behav Neurosci 128:621–624

    PubMed  Google Scholar 

  • Tran S, Nowicki M, Fulcher N, Chatterjee D, Gerlai R (2016) Interaction between handling induced stress and anxiolytic effects of ethanol in zebrafish: a behavioral and neurochemical analysis. Behav Brain Res 298:278–285

    CAS  PubMed  Google Scholar 

  • Vijayan MM, Moon TW (1994) The stress response and the plasma disappearance of corticosteroid and glucose in a marine teleost, the sea raven. Can J Zool 72:379–386

    CAS  Google Scholar 

  • Vindas MA, Johansen IB, Folkedal O, Höglund E, Gorissen M, Flik G, Kristiansen TS, Øverli Ø (2016) Brain serotonergic activation in growth-stunted farmed salmon: adaption versus pathology. R Soc Open Sci. https://doi.org/10.1098/rsos.160030

    Article  PubMed  PubMed Central  Google Scholar 

  • Waring CP, Brown JA, Collins JE, Prunet P (1996) Plasma prolactin, cortisol, and thyroid responses of the brown trout (Salmo trutta) exposed to lethal and sublethal aluminium in acidic soft waters. Gen Comp Endocrinol 102:377–385

    CAS  PubMed  Google Scholar 

  • Wittbrodt J, Shima A, Schartl M (2002) Medaka-a model organism from the far East. Nat Rev Genet 3:53–64

    CAS  PubMed  Google Scholar 

  • Wong RY, Oxendine SE, Godwin J (2013) Behavioral and neurogenomic transcriptome changes in wild-derived zebrafish with fluoxetine treatment. BMC Genomics. https://doi.org/10.1186/1471-2164-14-348

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Liu X, Zhao L, Hu S, Li S, Piao F (2013) Subchronic exposure to arsenic disturbed the biogenic amine neurotransmitter level and the mRNA expression of synthetase in mice brains. Neurosci 241:52–58

    CAS  Google Scholar 

  • Zhao TT, Shin KS, Park HJ, Yi BR, Lee KE, Lee MK (2017) Effects of (-)-sesamin on chronic stress-induced anxiety disorders in mice. Neurochem Res 42:1123–1129

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Japan Society for the Promotion of Science (Tokyo, Japan; grant no. 18K05833).

Author information

Authors and Affiliations

  1. Faculty of Science and Technology, Department of Life Science, Kindai University, Higashiosaka, Osaka, 577-8502, Japan

    Airi Otsuka, Yuki Shimomura, Honoka Sakikubo, Kensuke Miura & Nao Kagawa

Authors
  1. Airi Otsuka
    View author publications

    Search author on:PubMed Google Scholar

  2. Yuki Shimomura
    View author publications

    Search author on:PubMed Google Scholar

  3. Honoka Sakikubo
    View author publications

    Search author on:PubMed Google Scholar

  4. Kensuke Miura
    View author publications

    Search author on:PubMed Google Scholar

  5. Nao Kagawa
    View author publications

    Search author on:PubMed Google Scholar

Contributions

YS and NK designed the research protocol. AO, YS, HS, KM, and NK conducted the experiments and analyzed the data. AO and NK wrote the paper.

Corresponding author

Correspondence to Nao Kagawa.

Ethics declarations

Conflict of interest

The authors have no competing interests to declare.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Otsuka, A., Shimomura, Y., Sakikubo, H. et al. Effects of single and repeated heat stress on anxiety-like behavior and locomotor activity in medaka fish. Fish Sci 88, 45–54 (2022). https://doi.org/10.1007/s12562-021-01561-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-021-01561-2

Keywords