Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T07:42:38.607Z Has data issue: false hasContentIssue false

7 - A Fish Memory Tale

Memory and Recall in Fish and Sharks

from Part II - Memory and Recall

Published online by Cambridge University Press:  01 July 2021

By
Catarina Vila Pouca ,
Louise Tosetto  and
Culum Brown
Edited by
Allison B. Kaufman ,
Josep Call  and
James C. Kaufman
Allison B. Kaufman
Affiliation:
University of Connecticut
Josep Call
Affiliation:
University of St Andrews, Scotland
James C. Kaufman
Affiliation:
University of Connecticut
Get access

Summary

Fishes offer fantastic systems in which to study the evolutionary drivers of cognition because they comprise more than 30,000 species occupying a diverse range of habitats. Many researchers have taken advantage of this diversity to examine the ecological correlates of brain morphology and learning, but memory abilities per se are still fairly understudied compared to terrestrial vertebrates. Here, we review studies that have examined memory retention in fish, sharks, and rays and summarize the mechanisms of regulation of memory in these groups. Mechanisms of memory regulation are similar to those of terrestrial vertebrates, and it is clear that they can retain information from several days, months, and even years. We also address the potential for episodic-like memory in fish, which appears to be on par with evidence from other nonhuman vertebrates, further suggesting the process of memory retention is conserved across all vertebrates. In the last section of this review, we discuss avenues of memory research in which fish have been given little attention and highlight areas of future investigation.

Keywords

teleostselasmobranchsmemory retentionlong-term memoryepisodic-like memory
Type
Chapter
Information
The Cambridge Handbook of Animal Cognition , pp. 140 - 173
Publisher: Cambridge University Press
Print publication year: 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abe, T. & Kudo, H. (2018). Molecular characterization and gene expression of syntaxin-1 and VAMP2 in the olfactory organ and brain during both seaward and homeward migrations of chum salmon, Oncorhynchus keta. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. doi: https://doi.org/10.1016/j.cbpa.2018.09.008Google Scholar
Agranoff, B. W., Davis, R. E., & Brink, J. J. (1965). Memory fixation in the goldfish. Proceedings of the National Academy of Sciences, 54(3), 788–793. doi: 10.1073/pnas.54.3.788Google Scholar
Agranoff, B. W., Davis, R. E., & Brink, J. J. (1966). Chemical studies on memory fixation in goldfish. Brain Research, 1(3), 303–309. doi: https://doi.org/10.1016/0006-8993(66)90095-3Google Scholar
Aronson, L. R. (1951). Orientation and jumping behavior in the gobiid fish, Bathygobius soporator. American Museum Noviates, 1486, 22.Google Scholar
Aronson, L. R. (1971). Further studies on orientation and jumping behaviour in the Gobiid fish, Bathygobius soporator. Annals of the New York Academy of Sciences, 188(1), 378–392. doi: 10.1111/j.1749-6632.1971.tb13110.xCrossRefGoogle ScholarPubMed
Bailey, C. H., Bartsch, D., & Kandel, E. R. (1996). Toward a molecular definition of long-term memory storage. Proceedings of the National Academy of Sciences, 93(24), 13445–13452.Google Scholar
Bass, N. C., Mourier, J., Knott, N. A., Day, J., Guttridge, T., & Brown, C. (2017). Long-term migration patterns and bisexual philopatry in a benthic shark species. Marine and Freshwater Research, 68(8), 1414–1421.Google Scholar
Berejikian, B. A., Smith, R. J. F., Tezak, E. P., Schroder, S. L., & Knudsen, C. M. (1999). Chemical alarm signals and complex hatchery rearing habitats affect antipredator behavior and survival of chinook salmon (Oncorhynchus tshawytscha) juveniles. Canadian Journal of Fisheries and Aquatic Sciences, 56(5), 830–838.Google Scholar
Bertucci, F., Jacob, H., Mignucci, A., Gache, C., Roux, N., Besson, M., … Lecchini, D. (2018). Decreased retention of olfactory predator recognition in juvenile surgeon fish exposed to pesticide. Chemosphere, 208, 469–475. doi: https://doi.org/10.1016/j.chemosphere.2018.06.017Google Scholar
Bett, N., Hinch, S., Kaukinen, K., Li, S., & Miller, K. (2018). Olfactory gene expression in migrating adult sockeye salmon Oncorhynchus nerka. Journal of Fish Biology, 92(6), 2029–2038.CrossRefGoogle ScholarPubMed
Beukema, J. J. (1969). Angling experiments with carp (Cyprinus carpio L.). Netherlands Journal of Zoology, 20(1), 11. doi: 10.1163/002829670X00088Google Scholar
Blank, M., Guerim, L. D., Cordeiro, R. F., & Vianna, M. R. M. (2009). A one-trial inhibitory avoidance task to zebrafish: Rapid acquisition of an NMDA-dependent long-term memory. Neurobiology of Learning and Memory, 92(4), 529–534. doi: https://doi.org/10.1016/j.nlm.2009.07.001Google Scholar
Braida, D., Ponzoni, L., Martucci, R., Sparatore, F., Gotti, C., & Sala, M. (2014). Role of neuronal nicotinic acetylcholine receptors (nAChRs) on learning and memory in zebrafish. Psychopharmacology, 231(9), 1975–1985. doi: 10.1007/s00213-013-3340-1Google Scholar
Broglio, C., Gómez, A., Durán, E., Salas, C., & Rodríguez, F. (2011). Brain and Cognition in Teleost Fish. In Brown, C., Laland, K., & Krause, J. (Eds.), Fish Cognition and Behavior (2nd ed., pp. 325–358). Oxford: Wiley-Blackwell.Google Scholar
Brown, C. (2001). Familiarity with the test environment improves escape responses in the crimson spotted rainbowfish, Melanotaenia duboulayi. Animal Cognition, 4(2), 109–113. doi: 10.1007/s100710100105CrossRefGoogle Scholar
Brown, C. & Warburton, K. (1999). Differences in timidity and escape responses between predator‐naive and predator‐sympatric rainbowfish populations. Ethology, 105(6), 491–502.Google Scholar
Brown, C., Markula, A., & Laland, K. (2003). Social learning of prey location in hatchery-reared Atlantic salmon. Journal of Fish Biology, 63(3), 738–745. doi: 10.1046/j.1095-8649.2003.00186.xGoogle Scholar
Brown, C., Laland, K., & Krause, J. (2011). Fish Cognition and Behavior. Brown, C., Laland, K., & Krause, J. (Eds.) 2nd ed. Oxford: Blackwell Publishing.Google Scholar
Brown, G. E. & Smith, R. J. F. (1994). Fathead minnows use chemical cues to discriminate natural shoalmates from unfamiliar conspecifics. Journal of Chemical Ecology, 20(12), 3051–3061.Google Scholar
Brown, G. E. & Smith, R. J. F. (1998). Acquired predator recognition in juvenile rainbow trout (Oncorhynchus mykiss): Conditioning hatchery-reared fish to recognize chemical cues of a predator. Canadian Journal of Fisheries and Aquatic Sciences, 55(3), 611–617.Google Scholar
Brown, G. E., Ferrari, M. C., Malka, P. H., Oligny, M.-A., Romano, M., & Chivers, D. P. (2011). Growth rate and retention of learned predator cues by juvenile rainbow trout: Faster-growing fish forget sooner. Behavioral Ecology and Sociobiology, 65(6), 1267–1276.CrossRefGoogle Scholar
Bshary, R., Wickler, W., & Fricke, H. (2002). Fish cognition: A primate’s eye view. Animal Cognition, 5(1), 1–13. doi: 10.1007/s10071-001-0116-5Google Scholar
Bshary, R. & Brown, C. (2014). Fish cognition. Current Biology, 24(19), R947–R950. doi: https://doi.org/10.1016/j.cub.2014.08.043Google Scholar
Chivers, D. P. & Smith, R. J. F. (1994). Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish. Animal Behaviour, 48(3), 597–605.Google Scholar
Chivers, D. P., McCormick, M. I., Nilsson, G. E., Munday, P. L., Watson, S. A., Meekan, M. G., … Ferrari, M. C. O. (2014). Impaired learning of predators and lower prey survival under elevated CO2: A consequence of neurotransmitter interference. Global Change Biology, 20(2), 515–522. doi: 10.1111/gcb.12291Google Scholar
Chung, W.-S., Marshall, N. J., Watson, S.-A., Munday, P. L., & Nilsson, G. E. (2014). Ocean acidification slows retinal function in a damselfish through interference with GABA-A receptors. Journal of Experimental Biology, 217(3), 323–326.Google Scholar
Clark, E. (1959). Instrumental conditioning of lemon sharks. Science, 130(3369), 217–218.Google Scholar
Clayton, N. S., & Dickinson, A. (1998). Episodic-like memory during cache recovery by scrub jays. Nature, 395, 272. doi: 10.1038/26216Google Scholar
Clayton, N. S., Salwiczek, L. H., & Dickinson, A. (2007). Episodic memory. Current Biology, 17(6), R189–R191.Google Scholar
Cognato, G. d. P., Bortolotto, J. W., Blazina, A. R., Christoff, R. R., Lara, D. R., Vianna, M. R., & Bonan, C. D. (2012). Y-Maze memory task in zebrafish (Danio rerio): The role of glutamatergic and cholinergic systems on the acquisition and consolidation periods. Neurobiology of Learning and Memory, 98(4), 321–328. doi: https://doi.org/10.1016/j.nlm.2012.09.008Google Scholar
Colson, V., Cousture, M., Zanerato-Damasceno, D., Valotaire, C., Nguyen, T., Le Cam, A., & Bobe, J. (2018). Maternal temperature exposure triggers emotional and cognitive disorders and dysregulation of neurodevelopment genes in fish. PeerJ Preprints, 6, e26910v26911. doi: 10.7287/peerj.preprints.26910v1Google Scholar
Crick, F. (1984). Memory and molecular turnover. Nature, 312, 101. doi: 10.1038/312101a0Google Scholar
Croy, M. I. & Hughes, R. N. (1991). The role of learning and memory in the feeding behaviour of the fifteen-spined stickleback, Spinachia spinachia L. Animal Behaviour, 41(1), 149–159.Google Scholar
Crystal, J. D. (2010). Episodic-like memory in animals. Behavioural Brain Research, 215(2), 235–243. doi: https://doi.org/10.1016/j.bbr.2010.03.005CrossRefGoogle ScholarPubMed
Csányi, V., Csizmadia, G., & Miklosi, A. (1989). Long-term memory and recognition of another species in the paradise fish. Animal Behaviour, 37, 908–911.Google Scholar
Day, J. J. & Sweatt, J. D. (2010). DNA methylation and memory formation. Nature Neuroscience, 13(11), 1319.Google Scholar
Dere, E., Huston, J. P., & De Souza Silva, M. A. (2005). Episodic-like memory in mice: Simultaneous assessment of object, place and temporal order memory. Brain Research Protocols, 16(1), 10–19. doi: https://doi.org/10.1016/j.brainresprot.2005.08.001Google Scholar
Dixson, D. L., Munday, P. L., & Jones, G. P. (2010). Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecology Letters, 13(1), 68–75.Google Scholar
Dou, Y., He, S., Liang, X.-F., Cai, W., Wang, J., Shi, L., & Li, J. (2018). Memory function in feeding habit transformation of mandarin fish (Siniperca chuatsi). International Journal of Molecular Sciences, 19(4), 1254.Google Scholar
Dukes, J. P., Deaville, R., Bruford, M. W., Youngson, A. F., & Jordan, W. C. (2004). Odorant receptor gene expression changes during the parr-smolt transformation in Atlantic salmon. Molecular Ecology, 13(9), 2851–2857. doi: 10.1111/j.1365-294X.2004.02252.xGoogle Scholar
Dunlop, R., Millsopp, S., & Laming, P. (2006). Avoidance learning in goldfish (Carassius auratus) and trout (Oncorhynchus mykiss) and implications for pain perception. Applied Animal Behaviour Science, 97(2–4), 255–271.Google Scholar
Eaton, L., Edmonds, E. J., Henry, T. B., Snellgrove, D. L., & Sloman, K. A. (2015). Mild maternal stress disrupts associative learning and increases aggression in offspring. Hormones and Behavior, 71, 10–15. doi: https://doi.org/10.1016/j.yhbeh.2015.03.005Google Scholar
Ebbesson, L. & Braithwaite, V. (2012). Environmental effects on fish neural plasticity and cognition. Journal of Fish Biology, 81(7), 2151–2174.Google Scholar
Echevarria, D. J., Caramillo, E. M., & Gonzalez-Lima, F. (2016). Methylene blue facilitates memory retention in zebrafish in a dose-dependent manner. Zebrafish, 13(6), 489–494.Google Scholar
Eisenberg, M. & Dudai, Y. (2004). Reconsolidation of fresh, remote, and extinguished fear memory in medaka: Old fears don’t die. European Journal of Neuroscience, 20(12), 3397–3403. doi: 10.1111/j.1460-9568.2004.03818.xGoogle Scholar
El-Ghundi, M., O’Dowd, B. F., & George, S. R. (2007). Insights into the role of dopamine receptor systems in learning and memory. Reviews in the Neurosciences, 18, 37.Google Scholar
Fricke, H. (1973). Individual partner recognition in fish: Field studies on Amphiprion bicinctus. Naturwissenschaften, 60(4), 204–204.Google Scholar
Fukumori, K., Okuda, N., Yamaoka, K., & Yanagisawa, Y. (2010). Remarkable spatial memory in a migratory cardinalfish. Animal Cognition, 13(2), 385–389. doi: 10.1007/s10071-009-0285-1Google Scholar
Fuss, T., Bleckmann, H., & Schluessel, V. (2014). Visual discrimination abilities in the gray bamboo shark (Chiloscyllium griseum). Zoology, 117(2), 104–111. doi: https://doi.org/10.1016/j.zool.2013.10.009Google Scholar
Fuss, T. & Schluessel, V. (2015). Something worth remembering: Visual discrimination in sharks. Animal Cognition, 18(2), 463–471.Google Scholar
Fuss, T. & Schluessel, V. (2018). Immediate early gene expression related to learning and retention of a visual discrimination task in bamboo sharks (Chiloscyllium griseum). Brain Structure and Function. doi: 10.1007/s00429-018-1728-8Google Scholar
Gaikwad, S., Stewart, A., Hart, P., Wong, K., Piet, V., Cachat, J., & Kalueff, A. V. (2011). Acute stress disrupts performance of zebrafish in the cued and spatial memory tests: The utility of fish models to study stress–memory interplay. Behavioural Processes, 87(2), 224–230. doi: https://doi.org/10.1016/j.beproc.2011.04.004Google Scholar
Ghio, S. C, Boudreau Leblanc, A., Audet, C., & Aubin-Horth, N. (2016). Effects of maternal stress and cortisol exposure at the egg stage on learning, boldness and neophobia in brook trout. Behaviour, 153(13–14), 1639–1663. doi: https://doi.org/10.1163/1568539X-00003377Google Scholar
Gómez, Y., Vargas, J. P., Portavella, M., & López, J. C. (2006). Spatial learning and goldfish telencephalon NMDA receptors. Neurobiology of Learning and Memory, 85(3), 252–262. doi: https://doi.org/10.1016/j.nlm.2005.11.006Google Scholar
Gómez-Laplaza, L. M. & Morgan, E. (2005). Time–place learning in the cichlid angelfish, Pterophyllum scalare. Behavioural Processes, 70(2), 177–181.CrossRefGoogle ScholarPubMed
Gonzalez, R., Behrend, E. R., & Bitterman, M. (1967). Reversal learning and forgetting in bird and fish. Science, 158(3800), 519–521.Google Scholar
Griffiths, S. W. & Magurran, A. E. (1997). Familiarity in schooling fish: How long does it take to acquire? Animal Behaviour, 53(5), 945–949. doi: https://doi.org/10.1006/anbe.1996.0315Google Scholar
Grosenick, L., Clement, T. S., & Fernald, R. D. (2007). Fish can infer social rank by observation alone. Nature, 445(7126), 429.Google Scholar
Grossman, L., Stewart, A., Gaikwad, S., Utterback, E., Wu, N., DiLeo, J., … Kalueff, A. V. (2011). Effects of piracetam on behavior and memory in adult zebrafish. Brain Research Bulletin, 85(1), 58–63. https://doi.org/10.1016/j.brainresbull.2011.02.008Google Scholar
Guttridge, T. L. & Brown, C. (2014). Learning and memory in the Port Jackson shark, Heterodontus portusjacksoni. Animal Cognition, 17(2), 415–425. doi: 10.1007/s10071-013-0673-4Google Scholar
Guzowski, J. F., Setlow, B., Wagner, E. K., & McGaugh, J. L. (2001). Experience-dependent gene expression in the rat hippocampus after spatial learning: A comparison of the immediate-early genes Arc, c-fos, and zif268. Journal of Neuroscience, 21(14), 5089–5098.Google Scholar
Halder, R., Hennion, M., Vidal, R. O., Shomroni, O., Rahman, R.-U., Rajput, A., … Bonn, S. (2015). DNA methylation changes in plasticity genes accompany the formation and maintenance of memory. Nature Neuroscience, 19, 102. doi: 10.1038/nn.4194 https://www.nature.com/articles/nn.4194#supplementary-informationCrossRefGoogle ScholarPubMed
Hamilton, T. J., Myggland, A., Duperreault, E., May, Z., Gallup, J., Powell, R. A., … Digweed, S. M. (2016). Episodic-like memory in zebrafish. Animal Cognition, 19(6), 1071–1079.Google Scholar
Hamilton, T. J., Tresguerres, M., & Kline, D. I. (2017). Dopamine D1 receptor activation leads to object recognition memory in a coral reef fish. Biology Letters, 13(7). doi: 10.1098/rsbl.2017.0183CrossRefGoogle Scholar
Harooni, H. E., Naghdi, N., Sepehri, H., & Rohani, A. H. (2009). The role of hippocampal nitric oxide (NO) on learning and immediate, short- and long-term memory retrieval in inhibitory avoidance task in male adult rats. Behavioral Brain Research, 201(1), 166–172. doi: 10.1016/j.bbr.2009.02.011Google Scholar
Harvey‐Girard, E., Dunn, R. J., & Maler, L. (2007). Regulated expression of N‐methyl‐D‐aspartate receptors and associated proteins in teleost electrosensory system and telencephalon. Journal of Comparative Neurology, 505(6), 644–668.Google Scholar
Harvey-Girard, E., Tweedle, J., Ironstone, J., Cuddy, M., Ellis, W., & Maler, L. (2010). Long-term recognition memory of individual conspecifics is associated with telencephalic expression of Egr-1 in the electric fish Apteronotus leptorhynchus. Journal of Comparative Neurology, 518(14), 2666–2692. doi: 10.1002/cne.22358CrossRefGoogle ScholarPubMed
Hasler, A. D. & Scholz, A. T. (2012). Olfactory Imprinting and Homing in Salmon: Investigations into the Mechanism of the Imprinting Process (Vol. 14). Springer Science & Business Media. https://books.google.nl/books?id=EurwCAAAQBAJ&dq=Olfactory+imprinting+and+homing+in+salmon:+Investigations+into+the+mechanism+of+the+imprinting+process&source=gbs_navlinks_sGoogle Scholar
Hasselmo, M. E. (1999). Neuromodulation: Acetylcholine and memory consolidation. Trends in Cognitive Sciences, 3(9), 351–359. https://doi.org/10.1016/S1364-6613(99)01365-0Google Scholar
He, S., Liang, X.-F., Sun, J., Li, L., Yu, Y., Huang, W., … Tao, Y.-X. (2013). Insights into food preference in hybrid F1 of Siniperca chuatsi (♀) × Siniperca scherzeri (♂) mandarin fish through transcriptome analysis. BMC Genomics, 14(1), 601. doi: 10.1186/1471-2164-14-601Google Scholar
HedayatiRad, M., Nematollahi, M. A., Forsatkar, M. N., & Brown, C. (2017). Prozac impacts lateralization of aggression in male Siamese fighting fish. Ecotoxicology and Environmental Safety, 140, 84–88. https://doi.org/10.1016/j.ecoenv.2017.02.027Google Scholar
Hotta, T., Takeyama, T., Jordan, L. A., & Kohda, M. (2014). Duration of memory of dominance relationships in a group living cichlid. Naturwissenschaften, 101(9), 745–751.Google Scholar
Hughes, R. N. & Blight, C. M. (1999). Algorithmic behaviour and spatial memory are used by two intertidal fish species to solve the radial maze. Animal Behaviour, 58(3), 601–613. https://doi.org/10.1006/anbe.1999.1193Google Scholar
Jenkins, J. G. & Dallenbach, K. M. (1924). Obliviscence during sleep and waking. The American Journal of Psychology, 35(4), 605–612. doi: 10.2307/1414040Google Scholar
Johnston, T. D. (1982). Selective Costs and Benefits in the Evolution of Learning. In Rosenblatt, J. S., Hinde, R. A., Beer, C., & Busnel, M.-C. (Eds.), Advances in the Study of Behavior (Vol. 12, pp. 65–106). New York: Academic Press.Google Scholar
Johnstone, K. A., Lubieniecki, K. P., Koop, B. F., & Davidson, W. S. (2012). Identification of olfactory receptor genes in Atlantic salmon Salmo salar. Journal of Fish Biology, 81(2), 559–575. doi: 10.1111/j.1095-8649.2012.03368.xGoogle Scholar
Jozet-Alves, C., Bertin, M., & Clayton, N. S. (2013). Evidence of episodic-like memory in cuttlefish. Current Biology, 23(23), R1033–R1035. doi: https://doi.org/10.1016/j.cub.2013.10.021Google Scholar
Jun, J. J., Longtin, A., & Maler, L. (2016). Active sensing associated with spatial learning reveals memory-based attention in an electric fish. Journal of Neurophysiology, 115(5), 2577–2592.Google Scholar
Kart-Teke, E., De Souza Silva, M. A., Huston, J. P., & Dere, E. (2006). Wistar rats show episodic-like memory for unique experiences. Neurobiology of Learning and Memory, 85(2), 173–182. https://doi.org/10.1016/j.nlm.2005.10.002Google Scholar
Kendrick, K. M., Guevara-Guzman, R., Zorrilla, J., Hinton, M. R., Broad, K. D., Mimmack, M., & Ohkura, S. (1997). Formation of olfactory memories mediated by nitric oxide. Nature, 388(6643), 670–674. doi: 10.1038/41765Google Scholar
Kerr, B. & Feldman, M. W. (2003). Carving the cognitive niche: Optimal learning strategies in homogeneous and heterogeneous environments. Journal of Theoretical Biology, 220(2), 169–188.Google Scholar
Kim, N. N., Choi, Y. J., Lim, S.-G., Jeong, M., Jin, D.-H., & Choi, C. Y. (2015). Effect of salinity changes on olfactory memory-related genes and hormones in adult chum salmon Oncorhynchus keta. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 187, 40–47.Google Scholar
Kim, Y.-H., Lee, Y., Kim, D., Jung, M. W., & Lee, C.-J. (2010). Scopolamine-induced learning impairment reversed by physostigmine in zebrafish. Neuroscience Research, 67(2), 156–161. https://doi.org/10.1016/j.neures.2010.03.003Google Scholar
Kimber, J. A., Sims, D. W., Bellamy, P. H., & Gill, A. B. (2014). Elasmobranch cognitive ability: Using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark. Animal Cognition, 17(1), 55–65.Google Scholar
Kouwenberg, A.-L., Walsh, C. J., Morgan, B. E., & Martin, G. M. (2009). Episodic-like memory in crossbred Yucatan minipigs (Sus scrofa). Applied Animal Behaviour Science, 117(3), 165–172. https://doi.org/10.1016/j.applanim.2009.01.005Google Scholar
Küster, A. & Adler, N. (2014). Pharmaceuticals in the environment: Scientific evidence of risks and its regulation. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1656). doi: 10.1098/rstb.2013.0587 %J Philosophical Transactions of the Royal Society B: Biological SciencesGoogle Scholar
Laland, K. N. & Williams, K. (1998). Social transmission of maladaptive information in the guppy. Behavioral Ecology, 9(5), 493–499.CrossRefGoogle Scholar
Le Luyer, J., Laporte, M., Beacham, T. D., Kaukinen, K. H., Withler, R. E., Leong, J. S., … Bernatchez, L. (2017). Parallel epigenetic modifications induced by hatchery rearing in a Pacific salmon. Proceedings of the National Academy of Sciences, 114(49), 12964–12969. doi: 10.1073/pnas.1711229114 %J Proceedings of the National Academy of SciencesGoogle Scholar
Lee, Y., Lee, S., Park, J.-W., Hwang, J.-S., Kim, S.-M., Lyoo, I. K., … Han, I.-O. (2018). Hypoxia-induced neuroinflammation and learning–memory impairments in adult zebrafish are suppressed by glucosamine. Molecular Neurobiology, 55(11), 8738–8753. doi: 10.1007/s12035-018-1017-9Google Scholar
Levenson, J. M., O’Riordan, K. J., Brown, K. D., Trinh, M. A., Molfese, D. L., & Sweatt, J. D. (2004). Regulation of histone acetylation during memory formation in the hippocampus. Journal of Biological Chemistry, 279(39-issue of September 24), 40545–40559.Google Scholar
Levin, E. D. & Chen, E. (2004). Nicotinic involvement in memory function in zebrafish. Neurotoxicology and Teratology, 26(6), 731–735. https://doi.org/10.1016/j.ntt.2004.06.010Google Scholar
Luchiari, A. C., Chacon, D. M., & Oliveira, J. J. (2015). Dose-dependent effects of alcohol on seeking behavior and memory in the fish Betta splendens. Psychology & Neuroscience, 8(1), 143.Google Scholar
Mackney, P. & Hughes, R. (1995). Foraging behaviour and memory window in sticklebacks. Behaviour, 132(15), 1241–1253. doi: 10.1163/156853995X00559Google Scholar
Magurran, A. E. (1989). Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus). Ethology, 82(3), 216–223.Google Scholar
Martin, J. M., Bertram, M. G., Saaristo, M., Ecker, T. E., Hannington, S. L., Tanner, J. L., … Wong, B. B. M. (2019). Impact of the widespread pharmaceutical pollutant fluoxetine on behaviour and sperm traits in a freshwater fish. Science of the Total Environment, 650, 1771–1778. https://doi.org/10.1016/j.scitotenv.2018.09.294CrossRefGoogle Scholar
Martinez, J. L., Jensen, R. A., Vasquez, B. J., McGuinness, T., & McGaugh, J. L. (1978). Methylene blue alters retention of inhibitory avoidance responses. Physiological Psychology, 6(3), 387–390. doi: 10.3758/bf03326744Google Scholar
Mesquita, F. d. O. & Young, R. J. (2007). The behavioural responses of Nile tilapia (Oreochromis niloticus) to anti-predator training. Applied Animal Behaviour Science, 106(1), 144–154. https://doi.org/10.1016/j.applanim.2006.06.013Google Scholar
Messias, J. P. M., Santos, T. P., Pinto, M., & Soares, M. C. (2016). Stimulation of dopamine D1 receptor improves learning capacity in cooperating cleaner fish. Proceedings of the Royal Society B: Biological Sciences, 283(1823). doi: 10.1098/rspb.2015.2272Google Scholar
Meyer, C. G., Holland, K. N., & Papastamatiou, Y. P. (2005). Sharks can detect changes in the geomagnetic field. Journal of the Royal Society Interface, 2(2), 129–130. doi: 10.1098/rsif.2004.0021 %J Journal of The Royal Society InterfaceGoogle Scholar
Miklósi, Á., Haller, J., & Csányi, V. (1992). Different duration of memory for conspecific and heterospecific fish in the paradise fish (Macropodus opercularis L.). Ethology, 90(1), 29–36.Google Scholar
Miller, C. A. & Sweatt, J. D. (2007). Covalent modification of DNA regulates memory formation. Neuron, 53(6), 857–869. https://doi.org/10.1016/j.neuron.2007.02.022Google Scholar
Miller, C. A., Campbell, S. L., & Sweatt, J. D. (2008). DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiology of Learning and Memory, 89(4), 599–603. doi: 10.1016/j.nlm.2007.07.016Google Scholar
Mirza, R. S. & Chivers, D. P. (2000). Predator-recognition training enhances survival of brook trout: Evidence from laboratory and field-enclosure studies. Canadian Journal of Zoology, 78(12), 2198–2208.Google Scholar
Miyashita, T., Kubik, S., Lewandowski, G., & Guzowski, J. F. (2008). Networks of neurons, networks of genes: An integrated view of memory consolidation. Neurobiology of Learning and Memory, 89(3), 269–284. https://doi.org/10.1016/j.nlm.2007.08.012Google Scholar
Mourier, J., Brown, C., & Planes, S. (2017). Learning and robustness to catch-and-release fishing in a shark social network. Biology Letters, 13(3). doi: 10.1098/rsbl.2016.0824 %J Biology LettersGoogle Scholar
Muir, D., Simmons, D., Wang, X., Peart, T., Villella, M., Miller, J., & Sherry, J. (2017). Bioaccumulation of pharmaceuticals and personal care product chemicals in fish exposed to wastewater effluent in an urban wetland. Scientific Reports, 7(1), 16999. doi: 10.1038/s41598-017-15462-xGoogle Scholar
Naderi, M., Jamwal, A., Chivers, D. P., & Niyogi, S. (2016). Modulatory effects of dopamine receptors on associative learning performance in zebrafish (Danio rerio). Behavioural Brain Research, 303, 109–119. https://doi.org/10.1016/j.bbr.2016.01.034Google Scholar
Newton, K. C. & Kajiura, S. M. (2017). Magnetic field discrimination, learning, and memory in the yellow stingray (Urobatis jamaicensis). Animal Cognition, 20(4), 603–614. doi: 10.1007/s10071-017-1084-8Google Scholar
Nilsson, J., Kristiansen, T. S., Fosseidengen, J. E., Fernö, A., & van den Bos, R. (2008). Learning in cod (Gadus morhua): Long trace interval retention. Animal Cognition, 11(2), 215–222.Google Scholar
Oliveira, R. F. (2013). Mind the fish: Zebrafish as a model in cognitive social neuroscience. Frontiers in Neural Circuits, 7, 131.Google Scholar
Oulton, L. J., Taylor, M. P., Hose, G. C., & Brown, C. J. E. (2014). Sublethal toxicity of untreated and treated stormwater Zn concentrations on the foraging behaviour of Paratya australiensis (Decapoda: Atyidae). Ecotoxicology, 23(6), 1022–1029.CrossRefGoogle ScholarPubMed
Pastuzyn, E. D., Day, C. E., Kearns, R. B., Kyrke-Smith, M., Taibi, A. V., McCormick, J., … Shepherd, J. D. (2018). The neuronal gene Arc encodes a repurposed retrotransposon Gag protein that mediates intercellular RNA transfer. Cell, 172(1), 275–288.e218. https://doi.org/10.1016/j.cell.2017.12.024Google Scholar
de Perera, T. B. (2004). Spatial parameters encoded in the spatial map of the blind Mexican cave fish, Astyanax fasciatus. Animal Behaviour, 68(2), 291–295.Google Scholar
Pevzner, A., Miyashita, T., Schiffman, A. J., & Guzowski, J. F. (2012). Temporal dynamics of Arc gene induction in hippocampus: Relationship to context memory formation. Neurobiology of Learning and Memory, 97(3), 313–320. https://doi.org/10.1016/j.nlm.2012.02.004Google Scholar
Pinheiro-da-Silva, J., Tran, S., Silva, P. F., & Luchiari, A. C. (2017). Good night, sleep tight: The effects of sleep deprivation on spatial associative learning in zebrafish. Pharmacology Biochemistry and Behavior, 159, 36–47.CrossRefGoogle ScholarPubMed
Pinheiro-da-Silva, J., Tran, S., & Luchiari, A. C. (2018). Sleep deprivation impairs cognitive performance in zebrafish: A matter of fact? Behavioural Processes, 157, 656–663. https://doi.org/10.1016/j.beproc.2018.04.004Google Scholar
Poirier, R., Cheval, H., Mailhes, C., Garel, S., Charnay, P., Davis, S., & Laroche, S. (2008). Distinct functions of egr gene family members in cognitive processes. Frontiers in Neuroscience, 2, 2.Google Scholar
Pradel, G., Schachner, M., & Schmidt, R. (1999). Inhibition of memory consolidation by antibodies against cell adhesion molecules after active avoidance conditioning in zebrafish. Journal of Neurobiology, 39(2), 197–206.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Pyanov, A. I. (1993). Fish learning in response to trawl fishing. Paper presented at the ICES Marine Science Symposia.Google Scholar
Radford, A. N., Kerridge, E., & Simpson, S. D. (2014). Acoustic communication in a noisy world: Can fish compete with anthropogenic noise? Behavioral Ecology, 25(5), 1022–1030.Google Scholar
Rajan, K. E, Ganesh, A., Dharaneedharan, S., & Radhakrishnan, K. (2011). Spatial learning-induced egr-1 expression in telencephalon of gold fish Carassius auratus. Fish Physiology and Biochemistry, 37(1), 153–159. doi: 10.1007/s10695-010-9425-4Google Scholar
Rasch, B. & Born, J. (2013). About sleep’s role in memory. Physiological Reviews, 93(2), 681–766. doi: 10.1152/physrev.00032.2012Google Scholar
Rawashdeh, O., de Borsetti, N. H., Roman, G., & Cahill, G. M. (2007). Melatonin suppresses nighttime memory formation in zebrafish. Science, 318(5853), 1144–1146. doi: 10.1126/science.1148564Google Scholar
Réale, D., Garant, D., Humphries, M. M., Bergeron, P., Careau, V., & Montiglio, P.-O. (2010). Personality and the emergence of the pace-of-life syndrome concept at the population level. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 365(1560), 4051–4063.Google Scholar
Reebs, S. (1996). Time-place learning in golden shiners (Pisces: Cyprinidae). Behavioural Processes, 36(3), 253–262.Google Scholar
Reebs, S. G. (1999). Time–place learning based on food but not on predation risk in a fish, the inanga (Galaxias maculatus). Ethology, 105(4), 361–371.Google Scholar
Richetti, S. K., Blank, M., Capiotti, K. M., Piato, A. L., Bogo, M. R., Vianna, M. R., & Bonan, C. D. (2011). Quercetin and rutin prevent scopolamine-induced memory impairment in zebrafish. Behavioural Brain Research, 217(1), 10–15. https://doi.org/10.1016/j.bbr.2010.09.027Google Scholar
Rickard, N. S., Gibbs, M. E., & Ng, K. T. (1999). Inhibition of the endothelial isoform of nitric oxide synthase impairs long-term memory formation in the chick. Learning & Memory, 6(5), 458–466.Google Scholar
Routtenberg, A. (2001). It’s About Time. In Gold, P. E. & Greenough, W. T. (Eds.), Memory Consolidation: Essays in Honor of James L. McGaugh (pp. 17–34), Washington, DC: American Psychological Association Press.Google Scholar
Roy, T. & Bhat, A. (2016). Learning and memory in juvenile zebrafish: What makes the difference –population or rearing environment? Ethology, 122(4), 308–318.Google Scholar
Ruhl, T., Prinz, N., Oellers, N., Seidel, N. I., Jonas, A., Albayram, Ö., … von der Emde, G. (2014). Acute administration of THC impairs spatial but not associative memory function in zebrafish. Psychopharmacology, 231(19), 3829–3842. doi: 10.1007/s00213-014-3522-5Google Scholar
Sahar, S. & Sassone-Corsi, P. (2012). Circadian rhythms and memory formation: regulation by chromatin remodeling. Frontiers in Molecular Neuroscience, 5, 37. doi: 10.3389/fnmol.2012.00037Google Scholar
Salwiczek, L. H. & Bshary, R. (2011). Cleaner wrasses keep track of the ‘when’ and ‘what’ in a foraging task. Ethology, 117(11), 939–948. doi: 10.1111/j.1439-0310.2011.01959.xGoogle Scholar
Schluessel, V. (2015). Who would have thought that ‘Jaws’ also has brains? Cognitive functions in elasmobranchs. Animal Cognition, 18(1), 19–37.Google Scholar
Schluessel, V. & Bleckmann, H. (2005). Spatial memory and orientation strategies in the elasmobranch Potamotrygon motoro. Journal of Comparative Physiology A, 191(8), 695–706. doi: 10.1007/s00359-005-0625-9Google Scholar
Schluessel, V. & Bleckmann, H. (2012). Spatial learning and memory retention in the grey bamboo shark (Chiloscyllium griseum). Zoology, 115(6), 346–353. https://doi.org/10.1016/j.zool.2012.05.001Google Scholar
Schmidt, R. (1987). Changes in subcellular distribution of ependymins in goldfish brain induced by learning. Journal of Neurochemistry, 48(6), 1870–1878.Google Scholar
Schmidt, R. (1995). Cell-adhesion molecules in memory formation. Behavioral Brain Research, 66(1–2), 65–72.Google Scholar
Schübeler, D. (2015). Function and information content of DNA methylation. Nature, 517, 321. doi: 10.1038/nature14192Google Scholar
Schultz, W. (2010). Dopamine signals for reward value and risk: Basic and recent data. Behavioral and Brain Functions, 6(1), 1–9. doi: 10.1186/1744-9081-6-24Google Scholar
Shashoua, V. E. & Moore, M. E. (1978). Effect of antisera to β and γ goldfish brain proteins on the retention of a newly acquired behavior. Brain Research, 148(2), 441–449. https://doi.org/10.1016/0006-8993(78)90731-XGoogle Scholar
Sheriff, M. J. & Love, O. P. (2013). Determining the adaptive potential of maternal stress. Ecology Letters, 16(2), 271–280. doi: 10.1111/ele.12042Google Scholar
Shettleworth, S. J. (2010). Cognition, Evolution, and Behavior. Oxford: Oxford University Press.Google Scholar
Smarr, B. L., Jennings, K. J., Driscoll, J. R., & Kriegsfeld, L. J. (2014). A time to remember: The role of circadian clocks in learning and memory. Behavioral Neuroscience, 128(3), 283–303. doi: 10.1037/a0035963Google Scholar
Soares, M. C., Paula, J. R., & Bshary, R. (2016). Serotonin blockade delays learning performance in a cooperative fish. Animal Cognition, 19(5), 1027–1030. doi: 10.1007/s10071-016-0988-zGoogle Scholar
Stewart, A. M., Braubach, O., Spitsbergen, J., Gerlai, R., & Kalueff, A. V. (2014). Zebrafish models for translational neuroscience research: From tank to bedside. Trends in Neurosciences, 37(5), 264–278. https://doi.org/10.1016/j.tins.2014.02.011Google Scholar
Sytnyk, V., Leshchyns’ka, I., & Schachner, M. (2017). Neural cell adhesion molecules of the immunoglobulin superfamily regulate synapse formation, maintenance, and function. Trends in Neurosciences, 40(5), 295–308. https://doi.org/10.1016/j.tins.2017.03.003Google Scholar
Tarrant, R. M. (1964). Rate of extinction of a conditioned response in juvenile sockeye salmon. Transactions of the American Fisheries Society, 94(4), 3. https://doi.org/10.1577/1548-8659(1964)93[399:ROEOAC]2.0.CO;2Google Scholar
Templer, Victoria L. & Hampton, Robert R. (2013). Episodic memory in nonhuman animals. Current Biology, 23(17), R801–R806. https://doi.org/10.1016/j.cub.2013.07.016Google Scholar
Tlusty, M. F., Andrew, J., Baldwin, K., & Bradley, T. M. (2008). Acoustic conditioning for recall/recapture of escaped Atlantic salmon and rainbow trout. Aquaculture, 274(1), 57–64. https://doi.org/10.1016/j.aquaculture.2007.11.007Google Scholar
Tosetto, L., Williamson, J. E., & Brown, C. (2017). Trophic transfer of microplastics does not affect fish personality. Animal Behaviour, 123, 159–167.Google Scholar
Tulving, E. (1972). Episodic and Semantic Memory. In Tulving, E. & Donaldson, W. (Eds.), Organization of Memory (Vol. 1, pp. 381–403), New York: Academic Press.Google Scholar
Tulving, E. (2005). Episodic Memory and Autonoesis: Uniquely Human? In Terrace, H. S. & Metcalfe, J. (Eds.), The Missing Link in Cognition: Origins of Self-Reflective Consciousness (pp. 3–56). New York: Oxford University Press.Google Scholar
Utne, A. C. W. & Bacchi, B. (1997). The influence of visual and chemical stimuli from cod Gadus morhua on the distribution of two-spotted goby Gobiusculus flavescens (Fabricius). Sarsia, 82(2), 129–135.CrossRefGoogle Scholar
Utne-Palm, A. C. & Hart, P. J. B. (2000). The effects of familiarity on competitive interactions between threespined sticklebacks. Oikos, 91(2), 225–232. doi: 10.1034/j.1600-0706.2000.910203.xGoogle Scholar
Utne-Palm, A. C. (2001). Response of naive two-spotted gobies Gobiusculus flavescens to visual and chemical stimuli of their natural predator, cod Gadus morhua. Marine Ecology Progress Series, 218, 267–274.Google Scholar
Vila Pouca, C. & Brown, C. (2017). Contemporary topics in fish cognition and behaviour. Current Opinion in Behavioral Sciences, 16, 46–52.Google Scholar
Vila Pouca, C. & Brown, C. (2018). Food approach conditioning and discrimination learning using sound cues in benthic sharks. Animal Cognition, 21(4), 481–492. doi: 10.1007/s10071-018-1183-1Google Scholar
Vorster, A. P. & Born, J. (2015). Sleep and memory in mammals, birds and invertebrates. Neuroscience & Biobehavioral Reviews, 50, 103–119. https://doi.org/10.1016/j.neubiorev.2014.09.020Google Scholar
Warburton, K. (2003). Learning of foraging skills by fish. Fish and Fisheries, 4(3), 203–215. doi:10.1046/j.1467-2979.2003.00125.xGoogle Scholar
Warburton, K. & Thomson, C. (2006). Costs of learning: The dynamics of mixed-prey exploitation by silver perch, Bidyanus bidyanus (Mitchell, 1838). Animal Behaviour, 71(2), 361–370.Google Scholar
Ware, D. M. (1971). Predation by rainbow trout (Salmo gairdneri): The effect of experience. Journal of the Fisheries Research Board of Canada, 28(12), 1847–1852. doi:10.1139/f71-279Google Scholar
White, G. E. & Brown, C. (2014). A comparison of spatial learning and memory capabilities in intertidal gobies. Behavioral Ecology and Sociobiology, 68(9), 1393–1401.Google Scholar
Wilkens, H. (2010). Genes, modules and the evolution of cave fish. Heredity, 105(5), 413.Google Scholar
Williams, F. E., White, D., & Messer Jr, W. S. J. B. p. (2002). A simple spatial alternation task for assessing memory function in zebrafish. Behavioural Processes, 58(3), 125–132.Google Scholar
Wise, R. A. (2004). Dopamine, learning and motivation. Nature Reviews Neuroscience, 5, 483. doi: 10.1038/nrn1406Google Scholar
Xu, X., Boshoven, W., Lombardo, B., & Spranger, J. (1998). Comparison of the amnestic effects on NMDA receptor antagonist MK-801 and nitric oxide synthase inhibitors: L-NAME and L-NOARG in goldfish. Behavioral Neuroscience, 112(4), 892–899. doi: 10.1037/0735-7044.112.4.892Google Scholar
Xu, X., Russell, T., Bazner, J., & Hamilton, J. (2001). NMDA receptor antagonist AP5 and nitric oxide synthase inhibitor 7-NI affect different phases of learning and memory in goldfish. Brain Research, 889(1), 274–277. https://doi.org/10.1016/S0006-8993(00)03216-9Google Scholar
Yokogawa, T., Marin, W., Faraco, J., Pézeron, G., Appelbaum, L., Zhang, J., … Mignot, E. (2007). Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants. PLOS Biology, 5(10), e277. doi: 10.1371/journal.pbio.0050277Google Scholar
Zhang, W., Wu, J., Ward, , Matthew, D., Yang, S., Chuang, Y.-A., Xiao, M., … Worley, , Paul, F. (2015). Structural basis of Arc binding to synaptic proteins: Implications for cognitive disease. Neuron, 86(2), 490–500. https://doi.org/10.1016/j.neuron.2015.03.030Google Scholar
Zhdanova, I. V. (2011). Sleep and its regulation in zebrafish. Reviews in the Neurosciences, 22, 27.Google Scholar
Zhdanova, I. V., Yu, L., Lopez-Patino, M., Shang, E., Kishi, S., & Guelin, E. (2008). Aging of the circadian system in zebrafish and the effects of melatonin on sleep and cognitive performance. Brain Research Bulletin, 75(2), 433–441. https://doi.org/10.1016/j.brainresbull.2007.10.053Google Scholar
Zion, B., Barki, A., Grinshpon, J., Rosenfeld, L., & Karplus, I. (2011). Retention of acoustic conditioning in St Peter’s fish Sarotherodon galilaeus. Journal of Fish Biology, 78(3), 838–847. https://doi.org/10.1111/j.1095-8649.2010.02899.xGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×