Abstract
The zebrafish is an ideal vertebrate model for neurobehavioral studies with translational relevance to humans. Many aspects of sleep have been studied, but we still do not understand how and why sleep deprivation alters behavioral and physiological processes. A number of hypotheses suggest its role in memory consolidation. In this respect, the aim of this study was to analyze the effects of sleep deprivation on memory in zebrafish (Danio rerio), using an object discrimination paradigm. Four treatments were tested: control, partial sleep deprivation, total sleep deprivation by light pulses, and total sleep deprivation by extended light. The control group explored the new object more than the known object, indicating clear discrimination. The partially sleep-deprived group explored the new object more than the other object in the discrimination phase, suggesting a certain degree of discriminative performance. By contrast, both total sleep deprivation groups equally explored all objects, regardless of their novelty. It seems that only one night of sleep deprivation is enough to affect discriminative response in zebrafish, indicating its negative impact on cognitive processes. We suggest that this study could be a useful screening tool for cognitive dysfunction and a better understanding of the effect of sleep-wake cycles on cognition.
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References
Akkerman S, Prickaerts J, Steinbusch HWM, Blokland A (2012) Object recognition testing: statistical considerations. Behav Brain Res 232:317–322
Alhola P, Polo-Kantola P (2007) Sleep deprivation: impact on cognitive performance. Neuropsychiatr Dis Treat 3:553–567
Andersen ML, Bignotto M, Tufik S (2004) Hormone treatment facilitates penile erection in castrated rats after sleep deprivation and cocaine. J Neuroendocrinol 16:154–159. doi:10.1111/j.0953-8194.2004.01145.x
Andersen ML, Antunes IB, Silva a A et al (2008) Effects of sleep loss on sleep architecture in Wistar rats: gender-specific rebound sleep. Prog Neuropsychopharmacol Biol Psychiatry 32:975–983. doi:10.1016/j.pnpbp.2008.01.007
Avdesh A, Chen M, Martin-iverson MT et al (2010) Natural colour preference in the zebrafish (Danio rerio). Proc Meas Behav 2010:155–157
Azpeleta C, Martinez-Alvarez RM, Delgado MJ et al (2010) Melatonin reduces locomotor activity and circulating cortisol in goldfish. Horm Behav 57:323–329
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
Binks PG, Waters WF, Hurry M (1999) Short-term total sleep deprivations does not selectively impair higher cortical functioning. Sleep 22:328–334
Blank M, Guerim LD, Cordeiro RF, Vianna MRM (2009) A one-trial inhibitory avoidance task to zebrafish: rapid acquisition of an NMDA-dependent long-term memory. Neurobiol Learn Mem 92:529–534. doi:10.1016/j.nlm.2009.07.001
Blumberg M (2010) Beyond dreams: do sleep-related movements contribute to brain development? Front Neurol 1:140. doi:10.3389/fneur.2010.00140
Colwill RM, Raymond MP, Ferreira L, Escudero H (2005) Visual discrimination learning in zebrafish (Danio rerio). Behav Processes 70:19–31. doi:10.1016/j.beproc.2005.03.001
Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data. Behav Brain Res 31:47–59
Euston DR, Tatsuno M, McNaughton BL (2007) Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318:1147–1150. doi:10.1126/science.1148979
Fetsko LA (2002) What can be learned from a fish: an analysis of visual discrimination in the zebrafish, Danio Rerio. Temple University, Philadelphia
Gandhi AV, Mosser EA, Oikonomou G, Prober DA (2015) Melatonin is required for the circadian regulation of sleep. Neuron 85:1193–1199
Guzman-Marin R, Suntsova N, Methippara M et al (2005) Sleep deprivation suppresses neurogenesis in the adult hippocampus of rats. Eur J Neurosci 22:2111–2116. doi:10.1111/j.1460-9568.2005.04376.x
Harrison Y, Horne JA, Rothwell A (2000) Prefrontal neuropsychological effects of sleep deprivation in young adults–a model for healthy aging? Sleep 23:1067–1073
Herculano-Houzel S (2015) Decreasing sleep requirement with increasing numbers of neurons as a driver for bigger brains and bodies in mammalian evolution. Proc R Soc B Biol Sci 282:20151853. doi:10.1098/rspb.2015.1853
Hobson JA, Steriade M (2011) Neuronal basis of behavioral state control. Comprehensive physiology. Wiley, Hoboken, pp 701–823
Johnston TD (1982) Selective costs and benefits in the evolution of learning. Adv Study Behav 12:65–106. doi:10.1016/S0065-3454(08)60046-7
Kalueff AV, Zimbardo PG (2007) Behavioral neuroscience, exploration, and K.C. Montgomery’s legacy. Brain Res Rev 53:328–331. doi:10.1016/j.brainresrev.2006.09.003
Killgore WDS (2010) Effects of sleep deprivation on cognition. Prog Brain Res pp 105–129
Kim D, Chae S, Lee J et al (2005) Variations in the behaviors to novel objects among five inbred strains of mice. Genes, Brain Behav 4:302–306
Kliethermes CL, Crabbe JC (2006) Pharmacological and genetic influences on hole-board behaviors in mice. Pharmacol Biochem Behav 85:57–65
Koban A, Cook R (2009) Rotational object discrimination by pigeons. J Exp Psychol Anim Behav Process 35:250
Kruschke JK (2013) Bayesian estimation supersedes the t test. J Exp Psychol Gen 142(2):573–603. doi:10.1037/a0029146
Kruschke J (2014) Doing Bayesian data analysis: a tutorial with R, JAGS, and Stan. Academic Press, Cambridge
Leconte P, Hennevin E, Bloch V (1974) Duration of paradoxical sleep necessary for the acquisition of conditioned avoidance in the rat. Physiol Behav 13:675–681. doi:10.1016/0031-9384(74)90239-X
Leibowitz SM, Lopes M-CC, Andersen ML, Kushida CA (2006) Sleep deprivation and sleepiness caused by sleep loss. Sleep Med Clin 1:31–45. doi:10.1016/j.jsmc.2005.11.010
Lima-Cabello E, Díaz-Casado ME, Guerrero JA et al (2014) A review of the melatonin functions in zebrafish physiology. J Pineal Res 57:1–9
Linden ER, Bern D, Fishbein W (1975) Retrograde amnesia: prolonging the fixation phase of memory consolidation by paradoxical sleep deprivation. Physiol Behav 14:409–412. doi:10.1016/0031-9384(75)90004-9
Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145–156. doi:10.1016/S0896-6273(01)00186-6
Lucon-Xiccato T, Dadda M (2014) Assessing memory in zebrafish using the one-trial test. Behav Process 106:1–4. doi:10.1016/j.beproc.2014.03.010
Lyamin O, Pryaslova J, Kosenko P, Siegel J (2007) Behavioral aspects of sleep in bottlenose dolphin mothers and their calves. Physiol Behav 92:725–733. doi:10.1016/j.physbeh.2007.05.064
Manuel R, Gorissen M, Stokkermans M et al (2015) The effects of environmental enrichment and age-related differences on inhibitory avoidance in zebrafish (Danio rerio Hamilton). Zebrafish 12:152–165
Marshall L, Born J (2007) The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn Sci 11:442–450. doi:10.1016/j.tics.2007.09.001
Mashoodh R, Stamp JA, Wilkinson M et al (2008) Lack of estradiol modulation of sleep deprivation-induced c-Fos in the rat brain. Physiol Behav 95:562–569. doi:10.1016/j.physbeh.2008.08.001
May Z, Morrill A, Holcombe A et al (2016) Object recognition memory in zebrafish. Behav Brain Res 296:199–210. doi:10.1016/j.bbr.2015.09.016
McGaugh JL (2000) Memory–a century of consolidation. Science 287:248–251. doi:10.1126/science.287.5451.248
McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1–28
Meerlo P, Koehl M, Van Der Borght K, Turek FW (2002) Sleep restriction alters the hypothalamic-pituitary-adrenal response to stress. J Neuroendocrinol 14:397–402. doi:10.1046/j.0007-1331.2002.00790.x
Melke J, Botros HG, Chaste P et al (2008) Abnormal melatonin synthesis in autism spectrum disorders. Mol Psychiatry 13:90–98
Mueller AD, Pollock MS, Lieblich SE et al (2008) Sleep deprivation can inhibit adult hippocampal neurogenesis independent of adrenal stress hormones. Am J Physiol Regul Integr Comp Physiol 294:R1693–R1703. doi:10.1152/ajpregu.00858.2007
Oliveira J, Silveira M, Chacon D, Luchiari A (2015) The zebrafish world of colors and shapes: preference and discrimination. Zebrafish 12:166–173. doi:10.1089/zeb.2014.1019
Pilcher JJ, Huffcutt AJ (1996) Effects of sleep deprivation on performance: a meta-analysis. Sleep 19:318–326
Poe GR, Nitz DA, McNaughton BL, Barnes CA (2000) Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res 855:176–180
Prince T-M, Abel T (2013) The impact of sleep loss on hippocampal function. Learn Mem 20:558–569. doi:10.1101/lm.031674.113
Raidy DJ, Scharff LFV (2005) Effects of sleep deprivation on auditory and visual memory tasks. Percept Mot Skills 101:451–467
Rasch B, Born J (2013) About sleep’s role in memory. Physiol Rev 93:681–766. doi:10.1152/physrev.00032.2012
Rasch B, Pommer J, Diekelmann S, Born J (2009) Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat Neurosci 12:396–397
Roffwarg HP, Muzio JN, Dement WC (1966) Ontogenetic development of the human sleep-dream cycle. Science 152:604–619. doi:10.1126/science.152.3722.604
Santos LC, Oliveira JR, Oliveira JJ et al (2016) Irish coffee: effects of alcohol and caffeine on object discrimination in zebrafish. Pharmacol Biochem Behav. doi:10.1016/j.pbb.2016.01.013
Schluessel V, Fricke G, Bleckmann H (2012) Visual discrimination and object categorization in the cichlid Pseudotropheus sp. Anim Cogn 15:525–537. doi:10.1007/s10071-012-0480-3
Schluessel V, Kraniotakes H, Bleckmann H (2014) Visual discrimination of rotated 3D objects in Malawi cichlids (Pseudotropheus sp.): a first indication for form constancy in fishes. Anim Cogn 17:359–371. doi:10.1007/s10071-013-0667-2
Schmidt MH (2014) The energy allocation function of sleep: a unifying theory of sleep, torpor, and continuous wakefulness. Neurosci Biobehav Rev 47:122–153. doi:10.1016/j.neubiorev.2014.08.001
Siebeck UE, Litherland L, Wallis GM (2009) Shape learning and discrimination in reef fish. J Exp Biol 212:2113–2119. doi:10.1242/jeb.028936
Siegel JM (2005) Clues to the functions of mammalian sleep. Nature 437:1264–1271. doi:10.1038/nature04285
Siegel JM (2008) Do all animals sleep? Trends Neurosci 31:208–213. doi:10.1016/j.tins.2008.02.001
Sigurgeirsson B, Thornorsteinsson H, Sigmundsdóttir S et al (2013) Sleep-wake dynamics under extended light and extended dark conditions in adult zebrafish. Behav Brain Res 256:377–390. doi:10.1016/j.bbr.2013.08.032
Sison M, Gerlai R (2010) Associative learning in zebrafish (Danio rerio) in the plus maze. Behav Brain Res 207:99–104. doi:10.1016/j.bbr.2009.09.043
Spence R, Smith C (2008) Innate and learned colour preference in the zebrafish, Danio rerio. Ethology 114:582–588
Spiegel K (2004) Brief communication: sleep curtailment in healthy young men is associated with decreased leptin levels, elevated ghrelin levels, and increased hunger and appetite. Ann Intern Med 141:846. doi:10.7326/0003-4819-141-11-200412070-00008
Stickgold R (2005) Sleep-dependent memory consolidation. Nature 437:1272–1278. doi:10.1038/nature04286
Stickgold R, Walker MP (2005) Memory consolidation and reconsolidation: what is the role of sleep? Trends Neurosci 28:408–415
Thomas M, Sing H, Belenky G et al (2000) Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 h of sleep deprivation on waking human regional brain activity. J Sleep Res 9:335–352. doi:10.1046/j.1365-2869.2000.00225.x
Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10:49–62
Van Cauter E (2005) Endocrine physiology. In: Principles and practice of sleep medicine. Elsevier, p 266–282
Watson BO, Buzsáki G (2015) Sleep, memory & brain rhythms. Daedalus 144:67–82. doi:10.1162/DAED_a_00318
Weger BD, Sahinbas M, Otto GW et al (2011) The light responsive transcriptome of the zebrafish: function and regulation. PLoS ONE 6:e17080. doi:10.1371/journal.pone.0017080
Yokogawa T, Marin W, Faraco J et al (2007) Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants. PLoS Biol 5:e277. doi:10.1371/journal.pbio.0050277
Yu L, Tucci V, Kishi S, Zhdanova IV (2006) Cognitive aging in zebrafish. PLoS One 1:e14. doi:10.1371/journal.pone.0000014
Zhdanova IV (2006) Sleep in zebrafish. Zebrafish 3:215–226. doi:10.1089/zeb.2006.3.215
Zhdanova IV (2011) Sleep and its regulation in zebrafish. Rev Neurosci 22:27–36
Zhdanova IV, Wang SY, Leclair OU, Danilova NP (2001) Melatonin promotes sleep-like state in zebrafish. Brain Res 903:263–268. doi:10.1016/S0006-8993(01)02444-1
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14
Acknowledgments
The authors would like to thank Mr. Freire and Mr. Fonseca for statistical support, Mr. and Mrs. Haghverdian for English revision, and Ms. Nascimento and Ms. Jordão for technical assistance. We are thankful to the anonymous reviewers, who provided helpful comments and constructive criticism. The authors declare no competing interests.
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Pinheiro-da-Silva, J., Silva, P.F., Nogueira, M.B. et al. Sleep deprivation effects on object discrimination task in zebrafish (Danio rerio). Anim Cogn 20, 159–169 (2017). https://doi.org/10.1007/s10071-016-1034-x
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DOI: https://doi.org/10.1007/s10071-016-1034-x