Skip to main content
Log in

Trace classical conditioning in rainbow trout (Oncorhynchus mykiss): what do they learn?

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

There are two main memory systems: declarative and procedural memory. Knowledge of these two systems in fish is scarce, and controlled laboratory studies are needed. Trace classical conditioning is an experimentally tractable model of declarative memory. We tested whether rainbow trout (Oncorhynchus mykiss) can learn by trace conditioning and form stimulus–stimulus, as opposed to stimulus–response, associations. We predicted that rainbow trout trained by trace conditioning would show appetitive behaviour (conditioned response; CR) towards the conditioned stimulus (CS; light), and that the CR would be sensitive to devaluation of the unconditioned stimulus (US; food). The learning group (L, N = 14) was trained on a CS + US contingency schedule with a trace interval of 3.4 s. The control group (CtrL, N = 4) was kept on a completely random schedule. The fish that learnt were further trained as either an experimental (L, N = 6) or a memory control (CtrM, N = 3) group. The L group had the US devalued. The CtrM group received only food. No fish in the CtrL group, but nine fish from the L group conditioned to the light. When tested, five L fish changed their CRs after US devaluation, indicating learning by stimulus–stimulus association of the light with the food. CtrM fish retained their original CRs. To the best of our knowledge, this experiment is the first to show that rainbow trout can learn by trace classical conditioning. The results indicate that the fish learnt by ‘facts-learning’ rather than by reflex acquisition in this study.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bitterman ME (1975) Comparative analysis of learning. Science 188:699–709

    Article  PubMed  CAS  Google Scholar 

  • Bokkers EAM, Koene P, Rodenburg TB, Zimmerman PH, Spruijt BM (2004) Working for food under conditions of varying motivation in broilers. Anim Behav 68:105–113

    Article  Google Scholar 

  • Breuning SE, Wolach AH (1977) Successive negative contrast effects with goldfish (Carassius auratus). Psychol Rec 3:565–575

    Google Scholar 

  • Christian KM, Thompson RF (2003) Neural substrates of eyeblink conditioning: acquisition and retention. Learn Mem 10:427–455

    Article  PubMed  Google Scholar 

  • Clark RE, Squire LR (1998) Classical conditioning and brain systems: the role of awareness. Science 280:77–81

    Article  CAS  PubMed  Google Scholar 

  • Clark RE, Squire LR (1999) Human eyeblink classical conditioning: Effects of manipulating awareness of the stimulus contingencies. Psychol Sci 10:14–18

    Article  Google Scholar 

  • Clark RE, Manns JR, Squire LR (2002) Classical conditioning, awareness and brain systems. Trends Cogn Sci 6:524–531

    Article  PubMed  Google Scholar 

  • Clayton NS, Dickinson A (1999) Memory for the content of caches by scrub jays (Aphelocoma coerulescens). J Exp Psychol Anim Behav Process 25:82–91

    Article  CAS  PubMed  Google Scholar 

  • Couvillon PA, Bitterman ME (1985) Effect of experience with a preferred food on consummatory responding for a less preferred food in goldfish. Anim Learn Behav 13:433–438

    Google Scholar 

  • Cozzutti C, Vallortigara G (2001) Hemispheric memories for the content and position of food caches in the domestic chick. Behav Neurosci 115:305–313

    Article  CAS  PubMed  Google Scholar 

  • Dörr S, Neumeyer C (2000) Color constancy in goldfish: the limits. J Comp Physiol A 186:885–896

    Article  PubMed  Google Scholar 

  • 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 97:255–271

    Article  Google Scholar 

  • Emery NJ (2006) Cognitive ornithology: the evolution of avian intelligence. Phil Trans R Soc Lond B 361:23–43

    Article  Google Scholar 

  • Forkman B (2000) Domestic hens have declarative representations. Anim Cogn 3:135–137

    Article  Google Scholar 

  • Gomez Garcia A, Álvarez E, Durán E, Ocaña FM, Broglio C, Jiménez-Moya F, Salas C, Rodriguez F (2004) Delay vs trace conditioning following pallium ablation in goldfish. FENS Abstr 2:A042.10

    Google Scholar 

  • Holland PC, Straub JJ (1979) Differential effects of two ways of devaluing the unconditioned stimulus after pavlovian appetitive conditioning. J Exp Psychol Anim Behav Process 5:65–78

    Article  CAS  PubMed  Google Scholar 

  • Kandel ER, Kupfermann I, Iversen S (2000) Learning and memory. In: Kandel ER, Schwartz JH, Jessel TM (eds) Principles of neural science, 4th edn. McGraw-Hill, New York, pp 1227–1246

    Google Scholar 

  • Mackintosh NJ (1983) Conditioning and associative learning. Clarendon Press, Oxford

    Google Scholar 

  • Mackintosh NJ (1988) Approaches to the study of animal intelligence. Br J Psychol 79:509–525

    Google Scholar 

  • Macphail EM (1987) The comparative psychology of intelligence. Behav Brain Sci 10:645–695

    Article  Google Scholar 

  • Macphail EM (1998) The evolution of consciousness. Oxford University Press, Oxford

    Google Scholar 

  • Manteifel YB, Karelina MA (1996) Conditioned food aversion in the goldfish, Carassius auratus. Comp Biochem Physiol A Physiol 115:31–35

    Article  Google Scholar 

  • Martin P, Bateson P (1993) Measuring behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Moreira PSA, Pulman KGT, Pottinger TG (2004) Extinction of a conditioned response in rainbow trout selected for high or low responsiveness to stress. Horm Behav 46:450–457

    Article  CAS  PubMed  Google Scholar 

  • Nilsson J, Kristiansen TS, Fosseidengen JE, Ferno A, van den Bos R (2008) Learning in cod (Gadus morhua): long trace interval retention. Anim Cogn 11:215–222

    Article  PubMed  Google Scholar 

  • Olsson IAS, Keeling LJ, Mcadie TM (2002) The push-door for measuring motivation in hens: an adaptation and a critical discussion of the method. Anim Welf 11:1–10

    CAS  Google Scholar 

  • 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 57:397–399

    Article  CAS  PubMed  Google Scholar 

  • 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 80:49–56

    Article  CAS  PubMed  Google Scholar 

  • Portavella M, Torres B, Salas C (2004) Avoidance response in goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 24:2335–2342

    Article  CAS  PubMed  Google Scholar 

  • Rescorla RA (1967) Pavlovian conditioning and its proper control procedures. Psychol Rev 74:71–80

    Article  CAS  PubMed  Google Scholar 

  • Shettleworth SJ (1998) Cognition, evolution and behavior. Oxford University Press, New York

    Google Scholar 

  • Sovrano VA, Bisazza A, Vallortigara G (2002) Modularity and spatial reorientation in a simple mind: encoding of geometric and nongeometric properties of a spatial environment by fish. Cognition 85:B51–B59

    Article  PubMed  Google Scholar 

  • Sovrano VA, Bisazza A, Vallortigara G (2005) Animals’ use of landmarks and metric information to reorient: effects of the size of the experimental space. Cognition 97:121–133

    Article  PubMed  Google Scholar 

  • Sovrano VA, Bisazza A, Vallortigara G (2007) How fish do geometry in large and in small spaces. Anim Cogn 10:47–54

    Article  PubMed  Google Scholar 

  • Squire LR (2004) Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 82:171–177

    Article  PubMed  Google Scholar 

  • Tulving E (1985) Memory and consciousness. Can Psychol 26:1–12

    Google Scholar 

  • Yue S, Moccia RD, Duncan IJH (2004) Investigating fear in domestic rainbow trout, Oncorhynchus mykiss, using an avoidance learning task. Appl Anim Behav Sci 87:343–354

    Article  Google Scholar 

  • Yue S, Duncan IJH, Moccia RD (2008) Investigating fear in rainbow trout (Oncorhynchus mykiss) using the conditioned-suppression paradigm. J Appl Anim Welf Sci 11:14–27

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to thank Victoria Braithwaite for advising us on the experimental set-up. We are grateful to three anonymous referees for comments on the manuscript. This experiment was financially supported by the Norwegian Research Council, Grant no. 159667/S40, and the Norwegian School of Veterinary Science. It complies with the Norwegian regulation on animal experimentation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Janicke Nordgreen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

S1: The video clip shows a fish from the CtrL group tested in the learning test. The fish is positioned in the tank to the right, in the left corner of the close zone. It remains there, unresponsive throughout the test. (MPG 2992 kb)

S2: The video clip shows a fish from the L group tested in the learning test. The fish is positioned in the tank to the left. When the CS is turned off, the fish swims towards the feeder and enters the close zone. (MPG 4238 kb)

S3: The video clip shows the same fish from the L group as in S2, tested in the devaluation test. The fish no longer approaches the feeder in the close zone, but remains unresponsive at the border between the far and close zone. (MPG 4420 kb)

S4: The video clip shows a CtrM fish tested in the devaluation test. The fish is positioned in the tank to the right, in the close zone under the feeder. When the CS is turned off, the fish shows increased activity under the feeder directed towards the feeder. (MPG 3162 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nordgreen, J., Janczak, A.M., Hovland, A.L. et al. Trace classical conditioning in rainbow trout (Oncorhynchus mykiss): what do they learn?. Anim Cogn 13, 303–309 (2010). https://doi.org/10.1007/s10071-009-0267-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-009-0267-3

Keywords

Navigation