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Short- and long-term effects of nicotine and the histone deacetylase inhibitor phenylbutyrate on novel object recognition in zebrafish

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Abstract

Rationale

Zebrafish have a sophisticated color- and shape-sensitive visual system, so we examined color cue-based novel object recognition in zebrafish. We evaluated preference in the absence or presence of drugs that affect attention and memory retention in rodents: nicotine and the histone deacetylase inhibitor (HDACi) phenylbutyrate (PhB).

Objectives

The objective of this study was to evaluate whether nicotine and PhB affect innate preferences of zebrafish for familiar and novel objects after short- and long-retention intervals.

Methods

We developed modified object recognition (OR) tasks using neutral novel and familiar objects in different colors. We also tested objects which differed with respect to the exploratory behavior they elicited from naïve zebrafish.

Results

Zebrafish showed an innate preference for exploring red or green objects rather than yellow or blue objects. Zebrafish were better at discriminating color changes than changes in object shape or size. Nicotine significantly enhanced or changed short-term innate novel object preference whereas PhB had similar effects when preference was assessed 24 h after training. Analysis of other zebrafish behaviors corroborated these results.

Conclusions

Zebrafish were innately reluctant or prone to explore colored novel objects, so drug effects on innate preference for objects can be evaluated changing the color of objects with a simple geometry. Zebrafish exhibited recognition memory for novel objects with similar innate significance. Interestingly, nicotine and PhB significantly modified innate object preference.

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References

  • Avdesh A, Martin-Iverson MT, Mondal A, Chen M, Askraba S, Morgan N, Lardelli M, Groth DM, Verdile G, Martins RN (2012) Evaluation of color preference in zebrafish for learning and memory. J Alzheimers Dis 28:459–469

    PubMed  Google Scholar 

  • Balderas I, Rodriguez-Ortiz CJ, Salgado-Tonda P, Chavez-Hurtado J, McGaugh JL, Bermudez-Rattoni F (2008) The consolidation of object and context recognition memory involve different regions of the temporal lobe. Learn Mem 15:618–624

    Article  PubMed  PubMed Central  Google Scholar 

  • Bevins RA, Besheer J (2006) Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory. Nat Protoc 1:1306–1311

    Article  PubMed  Google Scholar 

  • Bilotta J, Risner ML, Davis EC, Haggbloom SJ (2005) Assessing appetitive choice discrimination learning in zebrafish. Zebrafish 2:259–268

    Article  PubMed  Google Scholar 

  • Braida D, Ponzoni L, Martucci R, Sala M (2014) A new model to study visual attention in zebrafish. Prog Neuro-Psychopharmacol Biol Psychiatry 55:80–86

    Article  Google Scholar 

  • Bredy TW, Barad M (2008) The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. Learn Mem 15:39–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan CH, Parmar A, Kily LKM, Ananthathevan A, Doshi A, Patel S (2011) Conditioned place preference models of drug dependence and relapse to drug seeking: studies with nicotine and ethanol. In: Kalueff and Cachat (ed) Zebrafish models in neurobehavioral research, Neuromethods 52, Humana Press, New Orleans, USA pp 163–180

  • Colwill RM, Raymond MP, Ferreira L, Escudero H (2005) Visual discrimination learning in zebrafish (Danio rerio). Behav Process 70:19–31

    Article  Google Scholar 

  • Darland T, Dowling JE (2001) Behavioral screening for cocaine sensitivity in mutagenized zebrafish. Proc Natl Acad Sci U S A 98:11691–11696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engeszer RE, Da Barbiano LA, Ryan MJ, Parichy DM (2007) Timing and plasticity of shoaling behaviour in the zebrafish, Danio rerio. Anim Behav 74:1269–1275

    Article  PubMed  PubMed Central  Google Scholar 

  • Engeszer RE, Ryan MJ, Parichy DM (2004) Learned social preference in zebrafish. Curr Biol 14:881–884

    Article  CAS  PubMed  Google Scholar 

  • Gaskin S, Tardif M, Cole E, Piterkin P, Kayello L, Mumby DG (2010) Object familiarization and novel-object preference in rats. Behav Process 83:61–71

    Article  Google Scholar 

  • Gerlai R (2011) Associative learning in zebrafish (Danio rerio). Methods Cell Biol 101:249–270

    Article  PubMed  Google Scholar 

  • Haettig J, Stefanko DP, Multani ML, Figueroa DX, McQuown SC, Wood MA (2011) HDAC inhibition modulates hippocampus-dependent long-term memory for object location in a CBP-dependent manner. Learn Mem 18:71–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hawk JD, Florian C, Abel T (2011) Post-training intrahippocampal inhibition of class I histone deacetylases enhances long-term object-location memory. Learn Mem 18:367–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalueff AV, Gebhardt M, Stewart AM, Cachat JM, Brimmer M, Chawla JS, Craddock C, Kyzar EJ, Roth A, Landsman S, Gaikwad S, Robinson K, Baatrup E, Tierney K, Shamchuk A, Norton W, Miller N, Nicolson T, Braubach O, Gilman CP, Pittman J, Rosemberg DB, Gerlai R, Echevarria D, Lamb E, Neuhauss SC, Weng W, Bally-Cuif L, Schneider H, Zebrafish Neuroscience Research Consortium (2013) Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond. Zebrafish 10:70–86

    Article  PubMed  PubMed Central  Google Scholar 

  • Karnik I, Gerlai R (2012) Can zebrafish learn spatial tasks? An empirical analysis of place and single CS-US associative learning. Behav Brain Res 233:415–421

    Article  PubMed  PubMed Central  Google Scholar 

  • Kedikian X, Faillace MP, Bernabeu R (2013) Behavioral and molecular analysis of nicotine-conditioned place preference in zebrafish. PLoS One 8:e69453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kily LJ, Cowe YC, Hussain O, Patel S, McElwaine S, Cotter FE, Brennan CH (2008) Gene expression changes in a zebrafish model of drug dependency suggest conservation of neuro-adaptation pathways. J Exp Biol 211:1623–1634

    Article  CAS  PubMed  Google Scholar 

  • Kim YS, Kim MJ, Koo TH, Kim JD, Koun S, Ham HJ, Lee YM, Rhee M, Yeo SY, Huh TL (2012) Histone deacetylase is required for the activation of Wnt/β-catenin signaling crucial for heart valve formation in zebrafish embryos. Biochem Biophys Res Commun 423:140–146

    Article  CAS  PubMed  Google Scholar 

  • Korzus E, Rosenfeld MG, Mayford M (2004) CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42:961–972

    Article  CAS  PubMed  Google Scholar 

  • Lau BY, Mathur P, Gould GG, Guo S (2011) Identification of a brain center whose activity discriminates a choice behavior in zebrafish. Proc Natl Acad Sci U S A 108:2581–2586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levin ED, Bencan Z, Cerutti DT (2007) Anxiolytic effects of nicotine in zebrafish. Physiol Behav 90:54–58

    Article  CAS  PubMed  Google Scholar 

  • Levin ED, Chen E (2004) Nicotinic involvement in memory function in zebrafish. Neurotoxicol Teratol 26:731–735

    Article  CAS  PubMed  Google Scholar 

  • Levin ED, Limpuangthip J, Rachakonda T, Peterson M (2006) Timing of nicotine effects on learning in zebrafish. Psychopharmacology 184:547–552

    Article  CAS  PubMed  Google Scholar 

  • Levine A, Huang Y, Drisaldi B, Griffin EA Jr, Pollak DD, Xu S, Yin D, Schaffran C, Kandel DB, Kandel ER (2011) Molecular mechanism for a gateway drug: epigenetic changes initiated by nicotine prime gene expression by cocaine. Sci Transl Med 3:107–109

    Article  Google Scholar 

  • Li L, Dowling JE (1997) A dominant form of inherited retinal degeneration caused by a non-photoreceptor cell-specific mutation. Proc Natl Acad Sci U S A 94:11645–11650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lieschke GJ, Currie PD (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8:353–367

    Article  CAS  PubMed  Google Scholar 

  • Lucon-Xiccato T, Dadda M (2014) Assessing memory in zebrafish using the one-trial test. Behav Process 106:1–4

    Article  Google Scholar 

  • Mathiasen JR, DiCamillo A (2010) Novel object recognition in the rat: a facile assay for cognitive function. Curr Protoc Pharmacol Chapter 5 Unit 5.59:1–15

  • May Z, Morrill A, Holcombe A, Johnston T, Gallup J, Fouad K, Schalomon M, Hamilton TJ (2016) Object recognition memory in zebrafish. Behav Brain Res 296:199–210

    Article  PubMed  Google Scholar 

  • Morris MJ, Karra AS, Monteggia LM (2010) Histone deacetylases govern cellular mechanisms underlying behavioral and synaptic plasticity in the developing and adult brain. Behav Pharmacol 21:409–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mussulini BH, Leite CE, Zenki KC, Moro L, Baggio S, Rico EP, Rosemberg DB, Dias RD, Souza TM, Calcagnotto ME, Campos MM, Battastini AM, de Oliveira DL (2013) Seizures induced by pentylenetetrazole in the adult zebrafish: a detailed behavioral characterization. PLoS One 8:e54515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ninkovic J, Bally-Cuif L (2006) The zebrafish as a model system for assessing the reinforcing properties of drugs of abuse. Methods 39:262–274

    Article  CAS  PubMed  Google Scholar 

  • Olincy A, Stevens KE (2007) Treating schizophrenia symptoms with an alpha7 nicotinic agonist, from mice to men. Biochem Pharmacol 74:1192–1201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira J, Silveira M, Chacon D, Luchiari A (2015) The zebrafish world of colors and shapes: preference and discrimination. Zebrafish 12:166–173

    Article  PubMed  Google Scholar 

  • Parker MO, Gaviria J, Haigh A, Millington ME, Brown VJ, Combe FJ, Brennan CH (2012) Discrimination reversal and attentional sets in zebrafish (Danio rerio). Behav Brain Res 232:264–268

    Article  PubMed  PubMed Central  Google Scholar 

  • Pastor V, Andrés ME, Bernabeu RO (2013) The effect of previous exposure to nicotine on nicotine place preference. Psychopharmacology 226:551–560

    Article  CAS  PubMed  Google Scholar 

  • Pastor V, Host L, Zwiller J, Bernabeu R (2011) Histone deacetylase inhibition decreases preference without affecting aversion for nicotine. J Neurochem 116:636–645

    Article  CAS  PubMed  Google Scholar 

  • Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, Agis-Balboa RC, Cota P, Wittnam JL, Gogol-Doering A, Opitz L, Salinas-Riester G, Dettenhofer M, Kang H, Farinelli L, Chen W, Fischer A (2010) Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328:753–756

    Article  CAS  PubMed  Google Scholar 

  • Puma C, Deschaux O, Molimard R, Bizot JC (1999) Nicotine improves memory in an object recognition task in rats. Eur Neuropsychopharmacol 9:323–327

    Article  CAS  PubMed  Google Scholar 

  • Robinson J, Schmitt EA, Harosi FI, Reece RJ, Dowling JE (1993) Zebrafish ultraviolet visual pigment: absorption spectrum, sequence, and localization. Proc Natl Acad Sci U S A 90:6009–6012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romieu P, Host L, Gobaille S, Sandner G, Aunis D, Zwiller J (2008) Histone deacetylase inhibitors decrease cocaine but not sucrose self-administration in rats. J Neurosci 28:9342–9348

    Article  CAS  PubMed  Google Scholar 

  • Roozendaal B, Hernandez A, Cabrera SM, Hagewoud R, Malvaez M, Stefanko DP, Haettig J, Wood MA (2010) Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. J Neurosci 30:5037–5046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spence R, Smith C (2008) Innate and learned colour preference in the zebrafish, Danio rerio. Ethology 114:582–588

    Article  Google Scholar 

  • Stefanko DP, Barrett RM, Ly AR, Reolon GK, Wood MA (2009) Modulation of long-term memory for object recognition via HDAC inhibition. Proc Natl Acad Sci USA 106:9447-52

  • Stewart A, Wong K, Cachat J, Gaikwad S, Kyzar E, Wu N, Hart P, Piet V, Utterback E, Elegante M, Tien D, Kalueff AV (2011) Zebrafish models to study drug abuse-related phenotypes. Rev Neurosci 22:95–105

    Article  CAS  PubMed  Google Scholar 

  • Stewart A, Wu N, Cachat J, Hart P, Gaikwad S, Wong K, Utterback E, Gilder T, Kyzar E, Newman A, Carlos D, Chang K, Hook M, Rhymes C, Caffery M, Greenberg M, Zadina J, Kalueff AV (2010) Pharmacological modulation of anxiety-like phenotypes in adult zebrafish behavioral models. Prog Neuro-Psychopharmacol Biol Psychiatry 35:1421–1431

    Article  Google Scholar 

  • Westerfield M (2007) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). 5th ed, Eugene: University of Oregon Press.

  • Winters M, Brauer M, Setton EM, Teschke K (2010) Built environment influences on healthy transportation choices: bicycling versus driving. Journal of Urban Health 87:969–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Wood MA, Hawk JD, Abel T (2006) Combinatorial chromatin modifications and memory storage: a code for memory? Learn Mem 13:241–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by grants of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and the University of Buenos Aires (R.B.), Argentina.

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Authors and Affiliations

  1. Department of Physiology and Institute of Physiology and Biophysics (IFIBIO), School of Medicine, University of Buenos Aires, Paraguay 2155 7th floor, C1121ABG, Ciudad Autónoma de Buenos Aires, Argentina

    MP Faillace, A Pisera-Fuster, MP Medrano, AC Bejarano & RO Bernabeu

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  1. MP Faillace
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  2. A Pisera-Fuster
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  3. MP Medrano
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  4. AC Bejarano
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Correspondence to RO Bernabeu.

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The Committee on Animal Research of the University of Buenos Aires approved all protocols for the use, housing, and care of experimental animals.

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Faillace, M., Pisera-Fuster, A., Medrano, M. et al. Short- and long-term effects of nicotine and the histone deacetylase inhibitor phenylbutyrate on novel object recognition in zebrafish. Psychopharmacology 234, 943–955 (2017). https://doi.org/10.1007/s00213-017-4532-x

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  • DOI: https://doi.org/10.1007/s00213-017-4532-x

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