Animal Cognition

, Volume 19, Issue 5, pp 1027–1030 | Cite as

Serotonin blockade delays learning performance in a cooperative fish

  • Marta C. Soares
  • José R. Paula
  • Redouan Bshary
Short Communication


Animals use learning and memorizing to gather information that will help them to make ecologically relevant decisions. Neuro-modulatory adjustments enable them to make associations between stimuli and appropriate behavior. A key candidate for the modulation of cooperative behavior is serotonin. Previous research has shown that modulation of the serotonergic system spontaneously affects the behavior of the cleaner wrasse Labroides dimidiatus during interactions with so-called ‘client’ reef fish. Here, we asked whether shifts in serotonin function affect the cleaners’ associative learning abilities when faced with the task to distinguish two artificial clients that differ in their value as a food source. We found that the administration of serotonin 1A receptor antagonist significantly slowed learning speed in comparison with saline treated fish. As reduced serotonergic signaling typically enhances fear, we discuss the possibility that serotonin may affect how cleaners appraise, acquire information and respond to client-derived stimuli via manipulation of the perception of danger.


Serotonin Learning Cooperation Serotonin 1A receptor WAY 100.635 



We thank the Oceanário de Lisboa staff for logistical support, Mariana Ramos, Andreia Teixeira for assistance during experimental trails. We also thank Sónia Cardoso for designing Fig. 1.


MSC was supported by Fundação para a Ciência e Tecnologia (PTDC/MAR/105276/2008) and RB by Swiss Science Foundation 31003AB grant. MSC is currently supported by SFRH/BPD/109433/2015.

Compliance with ethical standards

Human and animal rights statement

Animal procedures used in this study have been approved by the Portuguese Veterinary Office (#0420/000/000/2009).


  1. Beulig A, Fowler J (2008) Fish on Prozac: effect of serotonin reuptake inhibitors on cognition in goldfish. Behav Neurosci 122(2):426–432CrossRefPubMedGoogle Scholar
  2. Bshary R (2001) The cleaner fish market. In: Noë R, Van Hooff JARAM, Hammerstein P (eds) Economics in nature. Cambridge University Press, Cambridge, pp 146–172Google Scholar
  3. Bshary R, Schäfer D (2002) Choosy reef fish select cleaner fish that provide high-quality service. Anim Behav 63:557–564CrossRefGoogle Scholar
  4. Clarke HF, Dalley JW, Crofts HS, Robbins TW, Roberts AC (2004) Cognitive inflexibility after prefrontal serotonin depletion. Science 304:878–880CrossRefPubMedGoogle Scholar
  5. Davis M (1992) The amygdala: neurobiological aspects of emotion. In: Aggleton JP (ed) Memory, and mental dysfunction. Wiley, NewYork, pp 255–306Google Scholar
  6. Gallagher M, Hollandt PC (1994) The amygdala complex: multiple roles in associative learning and attention. Proc Natl Acad Sci USA 91:11771–11776CrossRefPubMedPubMedCentralGoogle Scholar
  7. Höglund E, Balm PHM, Winberg S (2002) Stimulatory and inhibitory effects of 5- HT1A receptors on adrenocorticotropic hormone and cortisol secretion in a teleost fish, the arctic charr (Salvelinus alpinus). Neurosci Lett 324:193–196CrossRefPubMedGoogle Scholar
  8. Hughes CR, Tran L, Keele NB (2012) 5-HT2A receptor activation normalizes exaggerated fear behavior in p-chlorophenylalanine (PCPA)-treated rats. J Behav Brain Sci 2:454–462CrossRefGoogle Scholar
  9. Oliveira RF (2009) Social behavior in context: hormonal modulation of behavioral plasticity and social competence. Integr Comp Biol 49:423–440CrossRefPubMedGoogle Scholar
  10. Oliveira RF (2013) Mind the fish: zebrafish as a model in cognitive social neuroscience. Front Neural Circuits 7:e131Google Scholar
  11. Paula JR, Messias JP, Grutter AS, Bshary R, Soares MC (2015) The role of serotonin in the modulation of cooperative behaviour. Behav Ecol 26(4):1005–1012CrossRefGoogle Scholar
  12. Rogers RD, Blackshaw AJ, Middleton HC, Matthews K, Deakin JFW, Sahakian BJ, Robbins TW (1999) Tryptophan depletion impairs stimulus-reward learning while methylphenidate disrupts attentional control in healthy young adults: implications for the monoaminergic basis of impulsive behaviour. Psychopharmacology 146:482–491CrossRefPubMedGoogle Scholar
  13. Salas C, Broglio C, Durán E, Gómez A, Ocaňa FM, Jiménez-Moya F, Rodríguez F (2006) Neuropsychology of learning and memory in teleost fish. Zebrafish 3:157–171CrossRefPubMedGoogle Scholar
  14. Soares M, Cardoso S, Grutter AS, Bshary R (2014) Cortisol mediates cleaner wrasse switch from cooperation to cheating and tactical deception. Horm Behav 66:346–350CrossRefPubMedGoogle Scholar
  15. Tran L, Lasher BK, Young KA, Keele NB (2013) Depletion of serotonin in the basolateral amygdala elevates glutamate receptors and facilitates fear-potentiated startle. Transl Psychiatry 3:e298CrossRefPubMedPubMedCentralGoogle Scholar
  16. Winberg S, Nilsson A, Hylland P, Söderstöm V, Nilsson GE (1997) Serotonin as a regulator of hypothalamic–pituitary–interrenal activity in teleost fish. Neurosci Lett 230:113–116CrossRefPubMedGoogle Scholar
  17. Wood RM, Rilling JK, Sanfey AG, Bhagwagar Z, Rogers RD (2006) Effects of tryptophan depletion on the performance of an iterated Prisoner’s Dilemma game in healthy adults. Neuropsychopharmacology 31:1075–1084CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Marta C. Soares
    • 1
  • José R. Paula
    • 2
  • Redouan Bshary
    • 3
  1. 1.CIBIO, Centro de Investigação em Biodiversidade e Recursos GenéticosUniversidade do PortoVairãoPortugal
  2. 2.MARE - Marine and Environmental Sciences Centre, Laboratório Marítimo da GuiaFaculdade de Ciências da Universidade de LisboaCascaisPortugal
  3. 3.Institut de Biologie, Eco-EthologieUniversité de NeuchâtelNeuchâtelSwitzerland

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