Journal of Comparative Physiology A

, Volume 199, Issue 10, pp 843–856 | Cite as

Avoidance conditioning in bamboo sharks (Chiloscyllium griseum and C. punctatum): behavioral and neuroanatomical aspects

  • Susanne Schwarze
  • Horst Bleckmann
  • Vera SchluesselEmail author
Original Paper


Animals face different threats; to survive, they have to anticipate how to react or how to avoid these. It has already been shown in teleosts that selected regions in the telencephalon, i.e., the medial pallium, are involved in avoidance learning strategies. No such study exists for any chondrichthyan. In nature, an avoidance reaction may vary, ranging from a ‘freeze’ reaction to a startling response and quick escape. This study investigated whether elasmobranchs (Chiloscyllium griseum and C. punctatum) can be conditioned in an aversive classical conditioning paradigm. Upon successful conditioning, the dorsal, medial and lateral pallium were removed (group 1) and performance tested again. In a second group, the same operation was performed prior to training. While conditioning was successful in individuals of both groups, no escape responses were observed. Post-operative performance was assessed and compared between individual and groups to reveal if the neural substrates governing avoidance behavior or tasks learned in a classical conditioning paradigm are located within the telencephalon, as has been shown for teleosts such as goldfish.


Elasmobranch Fish Cognition Learning Fear conditioning 



We would like to thank M. Hofmann for technical support and helpful comments on the experimental setup. The research reported herein was performed under the guidelines established by the current German animal protection law (Landesamt für Natur, Umwelt und Verbraucherschutz NRW, 8.87-


  1. Agranoff BW, Davis RE, Brink JJ (1965) Memory fixation in the goldfish. Proc Natl Acad Sci USA 54:788–793PubMedCrossRefGoogle Scholar
  2. Agranoff BW, Davis RE, Brink JJ (1966) Chemical studies on memory fixation in goldfish. Brain Res 1:303–309PubMedCrossRefGoogle Scholar
  3. Akirav I, Maroun M (2007) The role of the medial prefrontal cortex–amygdala circuit in stress effects on the extinction of fear. Neural Plast 2007:1–11CrossRefGoogle Scholar
  4. Aronson LR, Herberman R (1960) Persistence of a conditioned response in the cichlid fish, Tilapia macrocephala, after forebrain and cerebellar ablations. Anat Rec 138:332Google Scholar
  5. Behrend ER, Bitterman ME (1963) Sidman avoidance in the fish. J Exp Anal Behav 6:47–52PubMedCrossRefGoogle Scholar
  6. Bindra D, Anchel H (1963) Immobility as an avoidance response, and its disruption by drugs. J Exp Anal Behav 6:213–218PubMedCrossRefGoogle Scholar
  7. Bolles R, Popp R (1964) ###Parameters affecting the acquisition of Sidman avoidance1. J Exp Anal Behav 7:315–321PubMedCrossRefGoogle Scholar
  8. Bovet D, Bovet-Nitti F, Oliverio A (1968) Memory and consolidation mechanisms in avoidance learning of inbred mice. Brain Res 10:168–182PubMedCrossRefGoogle Scholar
  9. Bradford MR (1995) Comparative aspects of forebrain organization in the ray-finned fishes: touchstones or not? Brain Behav Evol 46:259–274CrossRefGoogle Scholar
  10. Broglio C, Gómez A, Durán E, Ocaña FM, Jiménez-Moya F, Rodríguez F, Salas C (2005) Hallmarks of a common forebrain vertebrate plan: specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish. Brain Res Bull 66:277–281PubMedCrossRefGoogle Scholar
  11. Carpenter RE, Summers CH (2009) Learning strategies during fear conditioning. Neurobiol Learn Mem 91:415–423PubMedCrossRefGoogle Scholar
  12. Compagno LJV, Dando M, Fowler S (2005) A field guide to the sharks of the world. Collins, London, pp 65–326Google Scholar
  13. Chandroo K, Duncan IJ, Moccia R (2004) Can fish suffer?: Perspectives on sentience, pain, fear and stress. Appl Anim Behav Sci 86:225–250CrossRefGoogle Scholar
  14. Davis M (1992) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15:353–375PubMedCrossRefGoogle Scholar
  15. Dunlop R, Millsopp S, Laming P (2006) Avoidance learning in goldfish (Carassius auratus) and trout (Oncorhynchus mykiss) and implications for pain perception. Appl Anim Behav Sci 97:255–271CrossRefGoogle Scholar
  16. Ebbesson SO (1972) New insights into the organization of the shark brain. Comp Biochem Physiol 42:121–129CrossRefGoogle Scholar
  17. Ferrari EAM, Faleiros L, Cerutti SM, Oliveira AM (1999) The functional value of sound and exploratory behaviour in detelencephalated pigeons. Behav Brain Res 101:93–103PubMedCrossRefGoogle Scholar
  18. Ferreira TL, Moreira KM, Ikeda DC et al (2003) Effects of dorsal striatum lesions in tone fear conditioning and contextual fear conditioning. Brain Res 987:17–24PubMedCrossRefGoogle Scholar
  19. Flood NC, Overmier JB, Savage GE (1976) Teleost telencephalon and learning: an interpretive review of data and hypotheses. Physiol Behav 16:783–788PubMedCrossRefGoogle Scholar
  20. Freund G, Walker DW (1971) The effect of aging on acquisition and retention of shuttle box avoidance in mice. Life Sci 10:1343–1349CrossRefGoogle Scholar
  21. Gamaro GD, Michalowski MB, Catelli DH et al (1999) Effect of repeated restraint stress on memory in different tasks. Braz J Med Biol Res 32:341–347PubMedCrossRefGoogle Scholar
  22. Graeber RC, Ebbesson SO (1972) Visual discrimination learning in normal and tectal-ablated nurse sharks (Ginglymostoma cirratum). Comp Biochem Physiol 42:131–139CrossRefGoogle Scholar
  23. Graeber RC, Ebbesson SO, Jane JA (1973) Visual discrimination in sharks without optic tectum. Science 180:413–415PubMedCrossRefGoogle Scholar
  24. Hofmann MH (2001) The role of the fish telencephalon in sensory information processing. In: Kapoor BG, Hara TJ (eds) Sensory biology of jawed fishes: new insights. Oxford & IBH Publishing Co. Pvt. Ltd., New Delhi, pp 255–274Google Scholar
  25. Horner JL, Longo N, Bitterman ME (1961) A shuttle box for fish and a control circuit of general applicability. Am J Psychol 74:114–120PubMedCrossRefGoogle Scholar
  26. Hunt HF, Brady JV (1951) Some effects of electro-convulsive shock on a conditioned emotional response (“anxiety”). J Comp Physiol 44:88–98Google Scholar
  27. Jackson RL, Alexander J, Maier SF (1980) Learned helplessness, inactivity, and associative deficits: effects of inescapable shock on response choice escape learning. J Exp Psychol Anim Behav Proc 6:1–20CrossRefGoogle Scholar
  28. Kalmijn AJ (1988) Detection of weak electric fields. In: Atema J, Fay RR, Popper RN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 151–186CrossRefGoogle Scholar
  29. Kaplan BYH, Aronson LR (1967) Effect of forebrain ablation on the performance of a conditioned avoidance response in the teleost fish, Tilapia H. macrocephala. Anim Behav 15:438–448PubMedCrossRefGoogle Scholar
  30. Kelly JC, Nelson DR (1975) Hearing thresholds of the horn shark, Heterodontus francisci. J Acoust Soc Am 58:905–909PubMedCrossRefGoogle Scholar
  31. Maren S (2001) Neurobiology of pavlovian fear conditioning. Annu Rev Neurosci 224:897–931CrossRefGoogle Scholar
  32. Maren S, Fanselow MS (1997) Electrolytic lesions of the fimbria/fornix, dorsal hippocampus, or entorhinal cortex produce anterograde deficits in contextual fear conditioning in rats. Neurobiol Learn Mem 67:142–149PubMedCrossRefGoogle Scholar
  33. Maren S, Holt WG (2000) The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behav Brain Res 110:97–108PubMedCrossRefGoogle Scholar
  34. Maren S, Holt WG (2004) Hippocampus and Pavlovian fear conditioning in rats: muscimol infusions into the ventral, but not dorsal, hippocampus impair the acquisition of conditional freezing to an auditory conditional stimulus. Behav Neurosci 118:97–110PubMedCrossRefGoogle Scholar
  35. Martí-Nicolovius M, Portell-Cortés I, Morgado-Bernal I (1988) Improvement of shuttle-box avoidance following post-training treatment in paradoxical sleep deprivation platforms in rats. Physiol Behav 43:93–98PubMedCrossRefGoogle Scholar
  36. Mineka S (1979) The role of fear in theories of avoidance learning, flooding, and extinction. Psychol Bull 86:985–1010CrossRefGoogle Scholar
  37. Morgan MA, Romanski LM, LeDoux JE (1993) Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett 163:109–113PubMedCrossRefGoogle Scholar
  38. Nelson DR (1967) Hearing thresholds, frequency discrimination, and acoustic orientation in the lemon shark, Negaprion brevirostris (POEY). Bull Mar Sci 17:714–768Google Scholar
  39. Nieuwenhuys R (2009) The forebrain of actinopterygians revisited. Brain Behav Evol 73:229–252PubMedCrossRefGoogle Scholar
  40. Northcutt RG (1981) Evolution of the telencephalon in nonmammals. Annu Rev Neurosci 4:301–350PubMedCrossRefGoogle Scholar
  41. Northcutt RG (2008) Forebrain evolution in bony fishes. Brain Res Bull 75:191–205PubMedCrossRefGoogle Scholar
  42. O’Connell CP, Abel DC, Gruber SH et al (2011) Response of juvenile lemon sharks, Negaprion brevirostris, to a magnetic barrier simulating a beach net. Ocean Coast Manage 54:225–230CrossRefGoogle Scholar
  43. Otto T, Cousens G, Rajewski K (1997) Odor-guided fear conditioning in rats: 1. Acquisition, retention, and latent inhibition. Behav Neurosci 111:1257–1264PubMedCrossRefGoogle Scholar
  44. Otto T, Cousens G, Herzog C (2000) Behavioral and neuropsychological foundations of olfactory fear conditioning. Behav Brain Res 110:119–128PubMedCrossRefGoogle Scholar
  45. Overmier JB, Papini MR (1986) Factors modulating the effects of teleost telencephalon ablation on retention, relearning, and extinction of instrumental avoidance behavior. Behav Neurosci 100:190–199PubMedCrossRefGoogle Scholar
  46. Overmier JB, Starkman N (1974) Transfer of control of avoidance behavior in normal and telencephalon ablated goldfish (Carassius auratus). Physiol Behav 12:605–608PubMedCrossRefGoogle Scholar
  47. Owen EH, Logue SF, Rasmussen DL, Wehner JM (1997) Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses. Neuroscience 80:1087–1099PubMedCrossRefGoogle Scholar
  48. Pavlov IP (1928) Lectures on conditioned reflexes: twenty five years of objective study of the higher nervous activity (behaviour) of animals, pp 103–204Google Scholar
  49. Portavella M, Vargas JP (2005) Emotional and spatial learning in goldfish is dependent on different telencephalic pallial systems. Eur J Neurosci 21:2800–2806PubMedCrossRefGoogle Scholar
  50. Portavella M, Depaulis A, Vergnes M (1993) 22–28 kHz ultrasonic vocalizations associated with defensive reactions in male rats do not result from fear or aversion. Psychopharmacology 111:190–194PubMedCrossRefGoogle Scholar
  51. Portavella M, Vargas JP, Torres B, Salas C (2002) The effects of telencephalic pallial lesions on spatial, temporal, and emotional learning in goldfish. Brain Res Bull 57:397–399PubMedCrossRefGoogle Scholar
  52. Portavella M, Salas C, Vargas JP, Papini MR (2003) Involvement of the telencephalon in spaced-trial avoidance learning in the goldfish (Carassius auratus). Physiol Behav 80:49–56PubMedCrossRefGoogle Scholar
  53. Portavella M, Torres B, Salas C (2004a) Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 24:2335–2342PubMedCrossRefGoogle Scholar
  54. Portavella M, Torres B, Salas C, Papini MR (2004b) Lesions of the medial pallium, but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish (Carassius auratus). Neurosci Lett 362:75–78PubMedCrossRefGoogle Scholar
  55. Richter-Levin G (2004) The amygdala, the hippocampus, and emotional modulation of memory. Neuroscientist 10:31–39PubMedCrossRefGoogle Scholar
  56. Rodríguez F, López JC, Vargas JP, Gómez Y et al (2002) Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J Neurosci 22:2894–2903PubMedGoogle Scholar
  57. Rodríguez F, Durán E, Gómez A et al (2005) Cognitive and emotional functions of the teleost fish cerebellum. Brain Res Bull 66:365–370PubMedCrossRefGoogle Scholar
  58. Rooney DJ, Laming PR (1988) Effects of telencephalic ablation on habituation of arousal responses, within and between daily training sessions in goldfish. Behav Neurol Biol 49:83–96CrossRefGoogle Scholar
  59. Sagvolden T (1975) Acquisition of two-way active avoidance following septal lesions in the rat: effect of intensity of discontinuous shock. Behav Biol 14:59–74PubMedCrossRefGoogle Scholar
  60. Salas C, Broglio C, Durán E et al (2006) Neuropsychology of learning and memory in teleost fish. Zebrafish 3:157–171PubMedCrossRefGoogle Scholar
  61. Sanders MJ, Wiltgen BJ, Fanselow MS (2003) The place of the hippocampus in fear conditioning. Eur J Pharmacol 463:217–223PubMedCrossRefGoogle Scholar
  62. Scobie S (1970) The response–shock–shock–shock interval and unsignalled avoidance in goldfish. J Exp Anal Behav 2:219–224CrossRefGoogle Scholar
  63. Seligman MEP (1972) Learned helplessness. Annu Rev Med 23:407–412PubMedCrossRefGoogle Scholar
  64. Seligman MEP, Maier SF, Geer JH (1968) Alleviation of learned helplessness in the dog. J Abnorm Psychol 73:256–262PubMedCrossRefGoogle Scholar
  65. Shashoua VE, Hesse GW (1989) Classical conditioning leads to changes in extracellular concentrations of ependymin in goldfish brain. Brain Res 484:333–339PubMedCrossRefGoogle Scholar
  66. Springer AD, Schoel WM, Klinger PD, Agranoff BW (1975) Anterograde and retrograde effects of electroconvulsive shock and of puromycin on memory formation in the goldfish. Behav Biol 13:467–481PubMedCrossRefGoogle Scholar
  67. Squire L (2004) Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 82:171–177PubMedCrossRefGoogle Scholar
  68. Thorndike EL (1898) Animal intelligence: an experimental study of the associative processes in animals. Psychol Rev Monogr Suppl 2:1–109Google Scholar
  69. Tricas TC, New JG (1998) Sensitivity and response dynamics of elasmobranch electrosensory primary afferent neurons to near threshold fields. J Comp Physiol A 182:89–101PubMedCrossRefGoogle Scholar
  70. Vargas JP, López JC, Portavella M (2009) What are the functions of fish brain pallium? Brain Res Bull 79:436–440PubMedCrossRefGoogle Scholar
  71. Wilensky AE, Schafe GE, LeDoux JE (1999) Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. J Neurosci 19:1–5Google Scholar
  72. Yoshida M, Okamura I, Uematsu K (2004) Involvement of the cerebellum in classical fear conditioning in goldfish. Behav Brain Res 153:143–148PubMedCrossRefGoogle Scholar
  73. Yue S, Moccia RD, Duncan IJH (2004) Investigating fear in domestic rainbow trout, (Oncorhynchus mykiss), using an avoidance learning task. Appl Anim Behav Sci 87:343–354CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Susanne Schwarze
    • 1
  • Horst Bleckmann
    • 1
  • Vera Schluessel
    • 1
    Email author
  1. 1.Institute of ZoologyRheinische-Friedrichs-Wilhelm UniversitätBonnGermany

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