Abstract
Cerebral lateralization has been suggested to convey a selective advantage to individuals by enhancing their cognitive abilities. Few, however, have explicitly compared the cognitive ability of animals with strongly contrasting laterality. Here, we examined the influence of laterality on learning performance in the crimson spotted rainbowfish, Melanotaenia duboulayi, using a classical conditioning paradigm. We also compared the learning ability of wild caught and captive-reared fish to examine the influence of rearing environment on cognitive performance. Laterality was established by observing which eye fish preferred to use while viewing their mirror image. Subjects were then conditioned to associate the appearance of a red light with a food reward over 7 days. Our results revealed that left-lateralized fish learned the conditioning task faster than right-lateralized. These results provide further evidence that cerebral lateralization can play important roles in cognitive function which likely have diverse fitness consequences for animals in their natural environments.
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References
Allen M (1983) Models of hemispheric specialization. Psychol Bull 93(1):73–104
Andrew RJ, Osorio D, Budaev S (2009) Light during embryonic development modulates patterns of lateralization strongly and similarly in both zebrafish and chick. Phil Trans R Soc Lon B 364:983–989
Bibost A-L, Brown C (2013) Laterality influences schooling position in rainbowfish, Mealnotaenia spp. PLoS ONE 8(11):e80907
Bibost A-L, Kydd E, Brown C (2013) The effect of sex and early environment on the lateralization of the rainbowfish Melanotaenia duboulayi. In: Csermely D, Regolin L (eds) Behavioral Lateralization in Vertebrates. Springer, Heidelberg, pp 9–24
Bisazza A, Dadda M (2005) Enhanced schooling performance in lateralized fishes. Proc R Soc Lon B 272:1677–1681
Bisazza A, Cantalupo C, Vallortigara G (1997) Lateral asymmetries during escape behavior in a species of teleost fish (Jenynsia lineata). Physiol Behav 61:31–35
Bisazza A, Cantalupo C, Capocchiano M, Vallortigara G (2000) Population lateralization and social behaviour: a study with 16 species of fish. Laterality 5:269–284
Broglio C, Rodriguez F, Salas C (2003) Spatial cognition and its neural basis in teleost fishes. Fish Fish 4:247–255
Brown C (2001) Familiarity with the test environment improves escape responses in the crimson spotted rainbowfish, Melanotaenia duboulayi. Anim Cogn 4(2):109–113
Brown C, Braithwaite VA (2005) Effects of predation pressure on the cognitive ability of the poeciliid Brachyraphis episcopi. Behav Ecol 16:482–497
Brown C, Day R (2002) The future of stock enhancements: bridging the gap between hatchery practice and conservation biology. Fish Fish 3:79–94
Brown C, Laland K (2001) Social learning and life skills training for hatchery reared fish. J Fish Biol 59:471–493
Brown C, Magat M (2011) The evolution of lateralized foot use in parrots: a phylogenetic approach. Behav Ecol 22:1201–1208
Brown C, Warburton K (1997) Predator recognition and anti-predator responses in the rainbowfish Melanotaenia eachamensis. Behav Ecol Sociobiol 41:61–68
Brown C, Davidson T, Laland K (2003) Environmental enrichment and prior experience of live prey improve foraging behaviour in hatchery-reared Atlantic salmon. J Fish Biol 63:187–196
Brown C, Gardner C, Braithwaite VA (2004) Population variation in lateralised eye use in the poeciliid Brachyraphis episcopi. Proc R Soc Lon B 271:S455–S457
Brown C, Western J, Braithwaite VA (2007) The influence of early experience on, and inheritance of, cerebral lateralization. Anim Behav 74:231–238
Brydges NM, Colegrave N, Heathcote RJP, Braithwaite VA (2008) Habitat stability and predation pressure affect temperament behaviours in populations of three-spined sticklebacks. J Anim Ecol 77:229–235
Castellano MA, Diaz-Palarea MD, Rodriguez M, Barroso J (1987) Lateralization in male rats and dopaminergic system: evidence of right-side population bias. Physiol Behav 40:607–612
Dadda M, Bisazza A (2006) Does brain asymmetry allow efficient performance of simultaneous tasks? Anim Behav 72:523–529
Dadda M, Bisazza A (2012) Prenatal light exposure affects development of behavioural lateralization in a livebearing fish. Behav Process 91:115–118
Dadda M, Zandonà E, Agrillo C, Bisazza A (2009) The costs of hemispheric specialization in a fish. Proc R Soc Lon B 276:4399–4407
Diamond MC, Johnson RE, Young D, Singh SS (1983) Age-related morphologic differences in the rat cerebral cortex and hippocampus: male-female; right–left. Exp Neurol 81:1–13
Goto K, Kurashima R, Gokan H, Inoue N, Ito I, Watanabe S (2010) Left–right asymmetry defect in the hippocampal circuitry impairs spatial learning and working memory in mice. PLoS ONE 5:e15468
Gotts SJ, Jo HJ, Wallace GL, Saad ZS, Cox RW, Martin A (2013) Two distinct forms of functional lateralization in the human brain. Proc Natl Acad Sci. doi:10.1073/pnas.1302581110
Griffiths SW (1996) Sex differences in the trade-off between feeding and mating in the guppy. J Fish Biol 48:891–898
Güntürkün O, Diekamp B, Manns M, Nottelmann F, Prior H, Schwarz A et al (2000) Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr Biol 10:1079–1081
Guttridge T, Brown C (2013) Learning and memory in the Port Jackson shark, Heterodontus portusjacksoni. Anim Cogn. doi:10.1007/s10071-013-0673-4
Huber R, van Staaden MJ, Kaufman LS, Liem KF (1997) Microhabitat use, trophic patterns, and the evolution of brain structure in African cichlids. Brain Behav Evol 50:167–182
Huntingford FA (2004) Implications of domestication and rearing conditions for the behaviour of cultivated fishes. J Fish Biol 65:122–142
Jacobs LF, Gaulin SJ, Sherry DF, Hoffman GE (1990) Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size. Proc Natl Acad Sci 87:6349–6352
Kanit L, Koylu EO, Erdogan O, Pogun S (2005) Effects of laterality and sex on cognitive strategy in a water maze place learning task and modification by nicotine and nitric oxide synthase inhibition in rats. Brain Res Bull 66:189–202
Kotrschal K, Van Staaden M, Huber R (1998) Fish brains: evolution and environmental relationships. Rev Fish Biol Fish 8:373–408
Kydd E, Brown C (2009) Loss of shoaling preference for familiar individuals in captive-reared crimson spotted rainbowfish Melanotaenia duboulayi. J Fish Biol 74:2187–2195
Mackney PA, Hughes RN (1995) Foraging behaviour and memory window in sticklebacks. Behaviour 132:1241–1253
Magat M, Brown C (2009) Laterality enhances cognition in Australian parrots. Proc R Soc Lon B 276:4155–4162
McGrew WC, Marchant LF (1999) Laterality of hand use pays off in foraging success for wild chimpanzees. Primates 40:509–513
Nilsson J, Kristiansen T, Fosseidengen J, Fernö A, van den Bos R (2008) Learning in cod (Gadus morhua): long trace interval retention. Anim Cogn 11:215–222
Pascual A, Huang K-L, Neveu J, Preat T (2004) Neuroanatomy: brain asymmetry and long-term memory. Nature 427:605–606
Reddon AR, Hurd PL (2008) Aggression, sex and individual differences in cerebral lateralization in a cichlid fish. Biol Lett 4:338–340
Rogers LJ (2000) Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 73:236–253
Rogers LJ (2002) Lateralization in vertebrates: its early evolution, general pattern, and development. Adv Study Behav 31:107–161
Rogers LJ, Andrew RJ (2002) Comparative vertebrate lateralization. Cambridge University Press, Cambridge, UK
Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. Proc R Soc Lon B 271:S420–S422
Salvanes AGV, Moberg O, Ebbesson LOE, Nilsen TO, Jensen KH, Braithwaite VA (2013) Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proc R Soc Lon B. doi:10.1098/rspb.2013.1331
Sandoz J-C, Menzel R (2001) Side-specificity of olfactory learning in the honeybee: generalization between odors and sides. Learn Mem 8:286–294
Sovrano VA, Dadda M, Bisazza A (2005) Lateralized fish perform better than nonlateralized fish in spatial reorientation tasks. Behav Brain Res 163:122–127
Tabibnia G, Cooke BM, Breedlove SM (1999) Sex difference and laterality in the volume of mouse dentate gyrus granule cell layer. Brain Res 827:41–45
Tappin AR (2010) Rainbowfish: their care and keeping in captivity. Art publications. http://peter.unmack.net/tappin/Rainbowfishes.2011.pdf
Vallortigara G (2000) Comparative neuropsychology of the dual brain: a stroll through animals’ left and right perceptual worlds. Brain Lang 73:189–219
Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–633
Acknowledgments
We wish to thank Samuel Brown and Brianne Messer for their assistance in the experimental observation. We also thank Mariella Herberstein and Darrell Kemp for helpful comments on the manuscript. This project was funded by the Australian Research Council.
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Bibost, AL., Brown, C. Laterality influences cognitive performance in rainbowfish Melanotaenia duboulayi . Anim Cogn 17, 1045–1051 (2014). https://doi.org/10.1007/s10071-014-0734-3
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DOI: https://doi.org/10.1007/s10071-014-0734-3