Variation in Emotion and Cognition Among Fishes

Abstract

Increasing public concern for the welfare of fish species that human beings use and exploit has highlighted the need for better understanding of the cognitive status of fish and of their ability to experience negative emotions such as pain and fear. Moreover, studying emotion and cognition in fish species broadens our scientific understanding of how emotion and cognition are represented in the central nervous system and what kind of role they play in the organization of behavior. For instance, on a macro neuro-architecture level the brains of fish species look dramatically different from those of mammals, while such a dramatic difference does not (always) occur at the level of emotion- and cognition-related behavior. Here, therefore, we discuss the evidence of emotion and cognition in fish species related to underlying neuro-architecture and the role that emotion and cognition play in the organization of behavior. To do so we use a framework encompassing a number of steps allowing a systematic approach to these issues. Emotion and cognition confer on human and non-human animals the capacity to compliment and/or override immediate reflexes to stimuli and so allow a large degree of flexibility in behavior. Systematic research on behavior that in mammals is indicative of emotion and cognition has been conducted in only a few fish species. The data thus far indicate that in these species brain-behavior relationships are not fundamentally different from those observed in mammals. Furthermore, data from other studies show evidence that behavior patterns related to emotion and cognition vary between fish species as well within fish species, related to sex and life history stage for example. From a welfare perspective, knowledge of such variability will potentially help us to design optimal living conditions for fish species kept by humans.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Arlinghaus, R., Cooke, S. J., Schwab, A., & Cowx, I. G. (2007). Fish welfare: A challenge of the feelings-based approach, with implications for recreational fishing. Fish and Fisheries, 8, 57–71.

    Article  Google Scholar 

  2. Ashley, P. J., Ringrose, S., Edwards, K. L., Wallington, E., McCrohan, C. R., & Sneddon, L. U. (2009). Effect of noxious stimulation upon antipredator responses and dominance status in rainbow trout. Animal Behaviour, 77, 403–410.

    Article  Google Scholar 

  3. Ashley, P. J., Sneddon, L. U., & McCrohan, C. R. (2006). Properties of corneal receptors in a teleost fish. Neuroscience Letters, 410, 165–168.

    Article  Google Scholar 

  4. Balleine, B. W., & Dickinson, A. (1998). Goal-directed instrumental action: Contingency and incentive learning and their cortical substrates. Neuropharmacology, 37, 407–419.

    Article  Google Scholar 

  5. Bechara, A., Damasio, H., Tranel, D., & Damasio, A. R. (1997). Deciding advantageously before knowing the advantageous strategy. Science, 275, 1293–1295.

    Article  Google Scholar 

  6. Benzie, V. L. (1967). Some aspects of the anti-predator responses of two species of stickleback. DPhil thesis, University of Oxford.

  7. Bermond, B. (1997). The myth of animal suffering. In M. Dol, S. Kasanmoentalib, S. Lijmbach, E. Rivas & R. van den Bos (Eds.), Animal consciousness and animal ethics; perspectives from the Netherlands (pp. 125–143). Assen: Van Gorcum, Animals in Philosophy and Science Vol. 1.

  8. Bermond, B. (2001). A neuropsychological and evolutionary approach to animal consciousness and animal suffering. Animal Welfare, 10, S47–S62.

    Google Scholar 

  9. Braithwaite, V. A., & Boulcott, P. (2007). Pain perception, aversion and fear in fish. Diseases of Aquatic Organisms, 75, 131–138.

    Article  Google Scholar 

  10. Braithwaite, V. A., & Girvan, J. R. (2003). Use of water flow to provide spatial information in a small-scale orientation task. Journal of Fish Biology, 63, 74–83.

    Article  Google Scholar 

  11. Brelin, D., Petersson, E., Dannewitz, J., Dahl, J., & Winberg, S. (2008). Frequency distribution of coping strategies in four populations of brown trout (Salmo trutta). Hormones and Behaviour, 53, 546–556.

    Article  Google Scholar 

  12. Brelin, D., Petersson, E., & Winberg, S. (2005). Divergent stress coping styles in juvenile brown trout (Salmo trutta). Annals of the New York Academy of Science, 1040, 239–245.

    Article  Google Scholar 

  13. Broglio, C., Gómez, A., Durán, E., Ocaña, F. M., Jiménez-Moya, F., & Rodríguez, S. C. (2005). Hallmarks of a common forebrain vertebrate plan: Specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish. Brain Research Bulletin, 66, 277–281.

    Article  Google Scholar 

  14. Broglio, C., Rodríguez, F., Gómez, A., Arias, J. L., & Salas, C. (2010). Selective involvement of the goldfish lateral pallium in spatial memory. Behaviorial Brain Research, 210, 191–201.

    Article  Google Scholar 

  15. Bshary, R., & Côté, I. M. (2008). New perspectives on marine cleaning mutualism. In C. Magnhagen, V. A. Braithwaite, E. Forsgren, & B. G. Kapoor (Eds.), Fish Behavior. New Hampshire: Science Publishers.

    Google Scholar 

  16. Cabanac, M. (1971). Physiological role of pleasure. Science, 173, 1103–1107.

    Article  Google Scholar 

  17. Cabanac, M. (1979). Sensory pleasure. Quarterly Review of Biology, 54, 1–29.

    Article  Google Scholar 

  18. Cabanac, M. (1992). Pleasure: The common currency. Journal of Theoretical Biology, 155, 173–200.

    Article  Google Scholar 

  19. Cabanac, M. (2008). The dialectics of pleasure. In M. L. Kringelbach & K. C. Berridge (Eds.), Pleasures of the brain. The neural basis of taste, smell and other rewards (pp. 113–124). Oxford: Oxford University Press.

    Google Scholar 

  20. Clark, R. E., & Squire, L. R. (1998). Classical conditioning and brain systems: The role of awareness. Science, 280, 77–81.

    Article  Google Scholar 

  21. Damasio, A. R. (1994). Descartes’ error. Emotion, reason and the human brain. New York: Avon Books.

    Google Scholar 

  22. Danisman, E., Bshary, R., & Bergmüller, R. (2010). Do cleaner fish learn to feed against their preference in a reverse reward contingency task? Animal Cognition, 13, 41–49.

    Article  Google Scholar 

  23. Dawkins, M. S. (2001). Who needs consciousness? Animal Welfare, 10, S19–S29.

    Google Scholar 

  24. de Veer Bos, M. W., & van den Bos, R. (1999). A critical review of methodology and interpretation of mirror self recognition research in nonhuman primates. Animal Behaviour, 58, 459–468.

    Article  Google Scholar 

  25. Dias-Ferreira, E., Sousa, J. C., Melo, I., Morgado, P., Mesquita, A. R., Cerqueira, J. J., et al. (2009). Chronic stress causes frontostriatal reorganization and affects decision-making. Science, 325, 621–625.

    Article  Google Scholar 

  26. Dickinson, A., & Balleine, B. (1994). Motivational control of goal-directed action. Animal Learning and Behaviour, 22, 1–18.

    Article  Google Scholar 

  27. Dickinson, A., & Balleine, B. (2008). The cognitive/motivational interface. In M. L. Kringelbach & K. C. Berridge (Eds.), Pleasures of the brain. The neural basis of taste, smell and other rewards (pp. 74–84). Oxford: Oxford University Press.

    Google Scholar 

  28. Dunlop, R., & Laming, P. (2005). Mechanoreceptive and nociceptive responses in the central nervous system of goldfish (Carassius auratus) and trout (Oncorhynchus mykiss). The Journal of Pain, 6, 561–568.

    Article  Google Scholar 

  29. Durán, E., Ocaña, F. M., Broglio, C., Rodríguez, F., & Salas, C. (2010). Lateral but not medial telencephalic pallium ablation impairs the use of goldfish spatial allocentric strategies in a ‘hole-board’ task. Behaviorial Brain Research, 214, 480–487.

    Article  Google Scholar 

  30. Gonzalez-Voyer, A., Winberg, S., & Kolm, N. (2009). Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative studies of cichlid fish. BMC Evolutionary Biology, 9, 238. doi:10.1186/1471-2148-9-238.

    Article  Google Scholar 

  31. Harvey, M. C., & Brown, G. E. (2004). Dine or dash? Ontogenetic shift in the response of yellow perch to conspecific alarm cues. Environmental Biology of Fishes, 70, 345–352.

    Article  Google Scholar 

  32. Healy, S. D., & Rowe, C. (2007). A critique of comparative studies of brain size. Proceedings of the Royal Society, London Series B, 274, 453–464.

    Article  Google Scholar 

  33. Hoogland, R. D., Morris, D., & Tinbergen, N. (1957). The spines of sticklebacks (Gasterosteus and Pygosteus) as means of defence against predators (Perca and Esox). Behaviour, 10, 205–237.

    Article  Google Scholar 

  34. Huntingford, F. A., Mesquita, F., & Kadri, S. (2012). Personality variation in cultures fish: Implications for production and welfare. In C. Carare & D. Maestripieri (Eds.), Animal personalities: Behavior, physiology and evolution. Chicago: Chicago University Press.

    Google Scholar 

  35. Huntingford, F. A., Wright, F. P. I., & Tierney, J. F. (1994). Adaptive variation in anti-predator behavior. In M. A. Bell & S. E. Foster (Eds.), The evolutionary biology of sticklebacks. Cambridge: Cambridge University Press.

    Google Scholar 

  36. Ito, H., & Yamamoto, N. (2009). Non-laminar cerebral cortex in teleost fishes? Biology Letters, 5, 117–121.

    Article  Google Scholar 

  37. Kolm, N., Gonzalez-Voyer, A., Brelin, D., & Winberg, S. (2009). Evidence for small-scale variation in the vertebrate brain: Mating strategy and sex affect brain size in wild brown trout (Salmo trutta). Journal of Evolutionary Biology, 22, 2524–2531.

    Article  Google Scholar 

  38. Kondoh, M. (2010). Linking learning approaches to trophic interactions: A brian size-based approach. Functional Ecology, 24, 35–43.

    Article  Google Scholar 

  39. Korte, S. M., Koolhaas, J. M., Wingfield, J. C., & McEwen, B. S. (2005). The Darwinian concept of stress: Benefits of allostasis and costs of allostatic load and the trade off in health and disease. Neuroscience and Biobehavioral Reviews, 29, 3–38.

    Article  Google Scholar 

  40. Kotrschal, K., Van Staaden, M. J., & Huber, R. (1998). Fish brains: Evolution and environmental relationships. Reviews in Fish Biology and Fisheries, 8, 272–408.

    Article  Google Scholar 

  41. Larson, E. T., Norris, D. O., & Summers, C. H. (2003). Monoamine changes associated with socially induced sex reversal in the saddleback wrasse. Neuroscience, 119, 251–263.

    Article  Google Scholar 

  42. Linsey, T. J., & Collin, S. P. (2006). Brain morphology in large pelagic fish: A comparison between sharks and teleosts. Journal of Fish Biology, 68, 532–554.

    Article  Google Scholar 

  43. Macphail, E. M. (1982). Brain and intelligence in vertebrates. Oxford: Clarendon Press.

    Google Scholar 

  44. Mason, G. J. (2010). Species differences in responses to captivity: Stress, welfare and the comparative method. Trends in Ecology & Evolution, 25, 713–721.

    Article  Google Scholar 

  45. Mendl, M., & Paul, E. S. (2004). Consciousness, emotion and animal welfare: Insights from cognitive science. Animal Welfare, 13, S17–S25.

    Google Scholar 

  46. Nilsson, J., Kristiansen, T. S., Fosseidengen, J. E., Ferno, A., & van den Bos, R. (2008). Learning in cod (Gadus morhua): Long trace interval retention. Animal Cognition, 11, 215–222.

    Article  Google Scholar 

  47. Nordgreen, J., Horsberg, T. E., Ranheim, B., & Chen, A. C. N. (2007). Somatosensory evoked potentials in the telencephalon of Atlantic salmon (Salmo salar) following galvanic stimulation of the tail. Journal of Comparative Physiology A, 193, 1235–1242.

    Article  Google Scholar 

  48. Nordgreen, J., Janczak, A. M., Hovland, A. L., Ranheim, B., & Horsberg, T. E. (2010). Trace classical conditioning in rainbow trout (Oncorhynchus mykiss): What do they learn? Animal Cognition, 13, 303–309.

    Article  Google Scholar 

  49. Panskepp, J. (2003). At the interface of the affective, behavioral, and cognitive neurosciences: Decoding the emotional feelings of the brain. Brain and Cognition, 52, 4–14.

    Article  Google Scholar 

  50. Panula, P., Chen, Y.-C., Priyadarshini, M., Kudo, H., Semenova, S. M., Sundvik, M., et al. (2010). The comparative neuroanatomy and neurochemistry of zebrafish CNS systems of relevance to human neuropsychiatric diseases. Neurobiology of Disease, 40, 46–57.

    Article  Google Scholar 

  51. Panula, P., Sallinen, V., Sundvik, M., Kolehmainen, J., Torkko, V., Tiittula, A., et al. (2006). Modulatory neurotransmitter systems and behavior: Towards zebrafish models of neurodegenerative diseases. Zebrafish, 3, 235–247.

    Article  Google Scholar 

  52. Pollen, A. A., Dobberfuhl, A. P., Scace, J., Igulu, M. M., Renn, S. C. P., Shumway, C. A., et al. (2007). Environmental complexity and social organisation sculpt the brain in Lake Tanganyikan cichlid fish. Brain, Behaviour and Evolution, 70, 21–39.

    Article  Google Scholar 

  53. Rodríguez, F., López, J. C., Vargas, J. P., Gómez, Y., Broglio, C., & Salas, C. (2002). Conservation of spatial memory function in the pallial forebrain of amniotes and ray-finned fishes. Journal of Neuroscience, 22, 2894–2903.

    Google Scholar 

  54. Rolls, E. (2007). Emotions explained. Oxford: Oxford University Press.

    Google Scholar 

  55. Romanes, G. J. (1883). Mental evolution in animals. London: Kegan Paul, Trench and Co.

    Google Scholar 

  56. Salas, C., Broglio, C., Durán, E., Gómez, A., Ocaña, F. M., Jiménez-Moya, F., et al. (2006). Neuropsychology of learning and memory in teleost fish. Zebrafish, 3, 157–171.

    Article  Google Scholar 

  57. Schwabe, L., Oitzl, M. S., Phlippsen, C., Richter, S., Bohringer, A., Wippich, W., et al. (2007). Stress modulates the use of spatial versus stimulus-response learning strategies in humans. Learning and Memory, 14, 109–116.

    Article  Google Scholar 

  58. Schwabe, L., & Wolf, O. T. (2009). Stress prompts habit behavior in humans. Journal of Neuroscience, 29, 7191–7198.

    Article  Google Scholar 

  59. Schwabe, L., Wolf, O. T., & Oitzl, M. S. (2010). Memory formation under stress: Quantity and quality. Neuroscience and Biobehavioral Reviews, 34, 584–591.

    Article  Google Scholar 

  60. Shettleworth, S. J. (1998). Cognition evolution and behaviour. New York: Oxford University Press.

    Google Scholar 

  61. Shumway, C. A. (2008). Habitat complexity brain and behavior. Brain, Behaviour and Evolution, 72, 123–134.

    Article  Google Scholar 

  62. Sneddon, L. U., Braithwaite, V. A., & Gentle, M. J. (2003a). Do fishes have nociceptors? Evidence for the evolution of a vertebrate sensory system. Proceeding of the Royal Society, London, Series B, 270, 1115–1121.

    Article  Google Scholar 

  63. Sneddon, L. U., Braithwaite, V. A., & Gentle, M. J. (2003b). Novel object test: Examining pain and fear in the rainbow trout. The Journal of Pain, 4, 431–440.

    Article  Google Scholar 

  64. Spruijt, B. M., van den Bos, R., & Pijlman, F. (2001). A concept of welfare based on how the brain evaluates its own activity: Anticipatory behavior as an indicator for this activity. Applied Animal Behaviour Science, 72, 145–171.

    Article  Google Scholar 

  65. Stienen, P. J., van Oostrom, H., van den Bos, R., de Groot, H. N. M., & Hellebrekers, L. J. (2006). Vertex-recorded, rather than primary somatosensory cortex-recorded, somatosensory-evoked potentials signal unpleasantness of noxious stimuli in the rat. Brain Research Bulletin, 70, 203–212.

    Article  Google Scholar 

  66. Tulley, J. J., & Huntingford, F. A. (1987). Paternal care and the development of adaptive variation in anti-predator responses in sticklebacks. Animal Behaviour, 35, 1570–1572.

    Article  Google Scholar 

  67. van den Bos, R. (1997). Reflections on the organisation of mind, brain and behavior. In M. Dol, S. Kasanmoentalib, S. Lijmbach, E. Rivas & R. van den Bos (Eds.), Animal consciousness and animal ethics; perspectives from the Netherlands (pp. 144–166). Assen: Van Gorcum, Animals in Philosophy and Science Vol. 1.

  68. van den Bos, R. (2000). General organizational principles of the brain as key to the study of animal consciousness. Psyche, 6, published on-line at http://psyche.cs.monash.edu.au/v6/psyche-6-05-vandenbos.html.

  69. van den Bos, R. (2001). The hierarchical organization of the brain as a key to the study of consciousness in human and non-human animals: Phylogenetic implications. Animal Welfare, 10, S246–S247.

    Google Scholar 

  70. van den Bos, R. (2004). Emotion and cognition. In M. Bekoff (Ed.), The handbook of animal behavior (pp. 554–557). Westport (CT): Greenwood Press.

    Google Scholar 

  71. van den Bos, R., & de Ridder, D. (2006). Evolved to satisfy our immediate needs: Self control and the rewarding properties of food. Appetite, 47, 24–29.

    Article  Google Scholar 

  72. van den Bos, R., Houx, B. B., & Spruijt, B. M. (2002). Cognition and emotion in concert in human and nonhuman animals. In M. Bekoff, C. Allen, & G. Burghardt (Eds.), The cognitive animal; empirical and theoretical perspectives on animal Cognition (pp. 97–103). Cambridge (MA): The MIT Press.

    Google Scholar 

  73. Vargas, J. P., López, J. C., & Portavella, M. (2009). What are the functions of fish brain pallium? Brain Research Bulletin, 79, 436–440.

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Victoria A. Braithwaite.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Braithwaite, V.A., Huntingford, F. & van den Bos, R. Variation in Emotion and Cognition Among Fishes. J Agric Environ Ethics 26, 7–23 (2013). https://doi.org/10.1007/s10806-011-9355-x

Download citation

Keywords

  • Cognition
  • Emotion
  • Welfare
  • Neuro-architecture
  • Complex behavior
  • Phylogeny