Journal of comparative physiology

, Volume 144, Issue 1, pp 1–8 | Cite as

An analysis of associative learning in a terrestrial mollusc

I. Higher-order conditioning, blocking and a transient US pre-exposure effect
  • Christie Sahley
  • Jerry W. Rudy
  • Alan Gelperin
Article

Summary

We have recently demonstrated that associative learning can play an important role in the regulation of food selection behavior ofLimax maximus, a terrestrial mollusc. The tendency ofLimax to approach a normally attractive odor generated by a food source such as carrot or potato can be markedly reduced if exposure to that odor is paired with exposure to a bitter taste (quinidine sulfate). We now report that variables known to influence associative learning by vertebrates (the operations of a second-order conditioning procedure, blocking and US-pre-exposure) similarly influence associative learning byLimax.

Abbreviations

CS

conditioned stimulus

US

unconditioned stimulus

S

stimulus

SOC

second-order conditioning

PU

paired-unpaired

UP

unpaired-paired

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alkon D (1981) Membrane depolarization accumulates during acquisition of an associative behavioral change. Science 210:1375–1376Google Scholar
  2. Amiro TW, Bitterman ME (1980) Second-order conditioning in goldfish. J Exp Psychol [Anim Behav] 6:41–48Google Scholar
  3. Benjamin PR, McCrohan CR, Rose RM (1981) Higher order interneurons which initiate and modulate feeding in the pond snailLymnaea stagnalis. In: Salánki J (ed) Invertebrate neurobiology: Mechanisms of integration. Pergamon Press, New York, pp 171–200Google Scholar
  4. Carew TJ, Walters ET, Kandel ER (1980) Defensive classical conditioning inAplysia: Functionally distinct motor systems show different neurophysiological correlates. Soc Neurosci Abstr 6:590Google Scholar
  5. Carew TJ, Walters ET, Kandel ER (1981) Associative learning inAplysia: Cellular correlates supporting a conditioned fear hypothesis. Science 211:501–503Google Scholar
  6. Chang JJ, Gelperin A (1980) Rapid taste-aversion learning by an isolated molluscan CNS. Proc Natl Acad Sci USA 77:6204–6206Google Scholar
  7. Cheatle MD, Rudy JW (1978) Analysis of second-order odoraversion conditioning in neonatal rats: Implications for Kamin's blocking effect. J Exp Psychol [Anim Behav] 4:237–249Google Scholar
  8. Cheatle MD, Rudy JW (1979) Ontogeny of second-order odoraversion conditioning in neonatal rats. J Exp Psychol [Anim Behav] 5:142–151Google Scholar
  9. Couvillon PA, Bitterman ME (1980) Some phenomena of associative learning in honey bees. J Comp Physiol Psychol 94:878–85Google Scholar
  10. Croll R, Chase R (1980) Plasticity of olfactory orientation to foods in the snailAchatina fulica. J Comp Physiol 136:267–277Google Scholar
  11. Crow TJ, Alkon DL (1978) Retention of an associative behavioral change inHermissenda. Science 201:1239–1241Google Scholar
  12. Davis WJ (1976) Plasticity in the invertebrates. In: Rosenzweig MR, Bennett EL (eds) Neural mechanisms of learning and memory. MIT Press, Cambridge, MA, pp 430–462Google Scholar
  13. Davis WJ, Gillette R (1978) Neural correlates of behavioral plasticity in command neurons ofPleurobranchaea. Science 199:801–804Google Scholar
  14. Dickinson A, Mackintosh NJ (1979) Classical conditioning in animals. Annu Rev Psychol 29:287–312Google Scholar
  15. Domjan M, Best MR (1977) Paradoxical effects of proximal unconditioned stimulus pre-exposure: Interference with a conditioning of a taste aversion. J Exp Psychol [Anim Behav] 3:310–321Google Scholar
  16. Farley J, Alkon D (1980) Neural organization predicts stimulus specificity for a retained associative behavioral change. Science 210:1373–1375Google Scholar
  17. Gelperin A (1980) Synaptic modulation by identified serotonin neurons. In: Jacobs B, Gelperin A (eds) Serotonin neurotransmission and behavior. MIT Press, Cambridge (in press)Google Scholar
  18. Gillan DJ, Domjan M (1977) Taste aversion conditioning with expected versus unexpected drug treatment. J Exp Psychol [Anim Behav] 3:297–309Google Scholar
  19. Gillette R, Gillette MI, Davis WJ (1980) Action-potential broadening and endogenously sustained bursting are substrates of command ability in a feeding neuron ofPleurobranchaea. J Neurophysiol 43:669–685Google Scholar
  20. Granzow B, Kater SB (1977) Identified higher-order neurons controlling the feeding motor program ofHelisoma. Neuroscience 2:1049–1063Google Scholar
  21. Holland PC (1977) Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. J Exp Psychol [Anim Behav] 3:77–104Google Scholar
  22. Holland PC, Rescorla RA (1975) Second-order conditioning with food unconditioned stimulus. J Comp Physiol Psychol 88:459–467Google Scholar
  23. Kamin LJ (1969) Predictability, surprise, attention, and conditioning. In: Church R, Campbell BA (eds) Punishment and aversive behavior. Appleton-Century-Crofts, New York, pp 279–296Google Scholar
  24. Kandel E (1976) Cellular basis of behavior. Freeman, San Francisco, pp 29–65Google Scholar
  25. Kaneko CRS, Merickel M, Kater SB (1978) Centrally programmed feeding inHelisoma: Identification and characteristics of an electrically coupled premotor neuron network. Brain Res 146:1–21Google Scholar
  26. Marchant HG, Moore JW (1973) Blocking of the rabbit's conditioned nictitating membrane response in Kamin's two-stage paradigm. J Exp Psychol 101:155–158Google Scholar
  27. Mpitsos GJ, Collins SD, McClellan AD (1978) Learning: A model system for physiological studies. Science 199:497–502Google Scholar
  28. Pavlov IP (1927) Conditioned reflexes. Oxford University Press, London, pp 33–35Google Scholar
  29. Randich A, LoLordo VM (1979) Associative and nonassociative theories of the UCS pre-exposure phenomenon: Implications for Pavlovian conditioning. Psychol Bull 86:523–548Google Scholar
  30. Rashotte ME, Griffin RW, Sisk CL (1977) Second-order conditioning of the pigeon's key peck. Anim Learn Behav 5:25–38Google Scholar
  31. Reingold S, Gelperin A (1980) Feeding motor program inLimax. II. Modulation by sensory inputs in intact animals and isolated central nervous systems. J Exp Biol 85:1–19Google Scholar
  32. Rescorla RA (1967) Pavlovian conditioning and its proper control procedures. Psychol Rev 74:71–80Google Scholar
  33. Rescorla RA (1973) Second-order conditioning: Implications for theories of learning. In: McGuigan FJ, Lamsden DB (eds) Contemporary approaches to conditioning and learning. Winston, Washington, DC, pp 7–33Google Scholar
  34. Rescorla RA (1975) Pavlovian excitatory and inhibitory conditioning. In: Estes WR (ed) Handbook of learning and cognitive processes, vol 2. Conditioning and behavior theory. Erlbaum, Hillsdale, NJ, pp 7–35Google Scholar
  35. Rizley RC, Rescorla RA (1972) Associations in second-order conditioning and sensory preconditioning. J Comp Physiol Psychol 81:1–11Google Scholar
  36. Rose RM, Benjamin PR (1980a) Interneuronal control of feeding in the pond snailLymnaea stagnalis: I. Initiation of feeding cycles by a single buccal interneurone. J Exp Biol 85:149–168Google Scholar
  37. Rose RM, Benjamin PR (1980b) Interneuronal control of feeding in the pond snailLymnaea stagnalis: II. The interneuronal mechanism generating feeding cycles. J Exp Biol 85:169–186Google Scholar
  38. Saal W Vom, Jenkins HM (1970) Blocking the development of stimulus control. Learn Motiv 1:52–62Google Scholar
  39. Sahley CL, Gelperin A, Rudy JW (1981) One-trial associative learning in a terrestrial mollusc. Proc Natl Acad Sci USA 78:640–642Google Scholar
  40. Tennant WA, Bitterman ME (1975) Blocking and overshadowing in two species of fish. J Exp Psychol [Anim Behav] 104:22–29Google Scholar
  41. Terry WS (1976) Effects of priming unconditioned stimulus representation in short-term memory on Pavlovian conditioning. J Exp Psychol [Anim Behav] 2:354–369Google Scholar
  42. Walters ET, Carew TJ, Kandel ER (1979) Classical conditioning inAplysia californica. Proc Natl Acad Sci USA 76:6675–6679Google Scholar
  43. Walters ET, Carew TJ, Kandel ER (1981) Associative learning inAplysia. Evidence for conditioned fear in an invertebrate. Science 211:504–506Google Scholar
  44. Willows AOD (1980) Physiological basis of feeding behavior inTritonia II. Neuronal mechanisms. J Neurophysiol 44:849–961Google Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • Christie Sahley
    • 1
  • Jerry W. Rudy
    • 2
  • Alan Gelperin
    • 1
  1. 1.Department of BiologyPrinceton UniversityPrincetonUSA
  2. 2.Department of PsychologyUniversity of ColoradoBoulderUSA

Personalised recommendations