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.
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Abbreviations
- CS :
-
conditioned stimulus
- US :
-
unconditioned stimulus
- S :
-
stimulus
- SOC :
-
second-order conditioning
- PU :
-
paired-unpaired
- UP :
-
unpaired-paired
References
Alkon D (1981) Membrane depolarization accumulates during acquisition of an associative behavioral change. Science 210:1375–1376
Amiro TW, Bitterman ME (1980) Second-order conditioning in goldfish. J Exp Psychol [Anim Behav] 6:41–48
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 171–200
Carew TJ, Walters ET, Kandel ER (1980) Defensive classical conditioning inAplysia: Functionally distinct motor systems show different neurophysiological correlates. Soc Neurosci Abstr 6:590
Carew TJ, Walters ET, Kandel ER (1981) Associative learning inAplysia: Cellular correlates supporting a conditioned fear hypothesis. Science 211:501–503
Chang JJ, Gelperin A (1980) Rapid taste-aversion learning by an isolated molluscan CNS. Proc Natl Acad Sci USA 77:6204–6206
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] 4:237–249
Cheatle MD, Rudy JW (1979) Ontogeny of second-order odoraversion conditioning in neonatal rats. J Exp Psychol [Anim Behav] 5:142–151
Couvillon PA, Bitterman ME (1980) Some phenomena of associative learning in honey bees. J Comp Physiol Psychol 94:878–85
Croll R, Chase R (1980) Plasticity of olfactory orientation to foods in the snailAchatina fulica. J Comp Physiol 136:267–277
Crow TJ, Alkon DL (1978) Retention of an associative behavioral change inHermissenda. Science 201:1239–1241
Davis WJ (1976) Plasticity in the invertebrates. In: Rosenzweig MR, Bennett EL (eds) Neural mechanisms of learning and memory. MIT Press, Cambridge, MA, pp 430–462
Davis WJ, Gillette R (1978) Neural correlates of behavioral plasticity in command neurons ofPleurobranchaea. Science 199:801–804
Dickinson A, Mackintosh NJ (1979) Classical conditioning in animals. Annu Rev Psychol 29:287–312
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] 3:310–321
Farley J, Alkon D (1980) Neural organization predicts stimulus specificity for a retained associative behavioral change. Science 210:1373–1375
Gelperin A (1980) Synaptic modulation by identified serotonin neurons. In: Jacobs B, Gelperin A (eds) Serotonin neurotransmission and behavior. MIT Press, Cambridge (in press)
Gillan DJ, Domjan M (1977) Taste aversion conditioning with expected versus unexpected drug treatment. J Exp Psychol [Anim Behav] 3:297–309
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 43:669–685
Granzow B, Kater SB (1977) Identified higher-order neurons controlling the feeding motor program ofHelisoma. Neuroscience 2:1049–1063
Holland PC (1977) Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. J Exp Psychol [Anim Behav] 3:77–104
Holland PC, Rescorla RA (1975) Second-order conditioning with food unconditioned stimulus. J Comp Physiol Psychol 88:459–467
Kamin LJ (1969) Predictability, surprise, attention, and conditioning. In: Church R, Campbell BA (eds) Punishment and aversive behavior. Appleton-Century-Crofts, New York, pp 279–296
Kandel E (1976) Cellular basis of behavior. Freeman, San Francisco, pp 29–65
Kaneko CRS, Merickel M, Kater SB (1978) Centrally programmed feeding inHelisoma: Identification and characteristics of an electrically coupled premotor neuron network. Brain Res 146:1–21
Marchant HG, Moore JW (1973) Blocking of the rabbit's conditioned nictitating membrane response in Kamin's two-stage paradigm. J Exp Psychol 101:155–158
Mpitsos GJ, Collins SD, McClellan AD (1978) Learning: A model system for physiological studies. Science 199:497–502
Pavlov IP (1927) Conditioned reflexes. Oxford University Press, London, pp 33–35
Randich A, LoLordo VM (1979) Associative and nonassociative theories of the UCS pre-exposure phenomenon: Implications for Pavlovian conditioning. Psychol Bull 86:523–548
Rashotte ME, Griffin RW, Sisk CL (1977) Second-order conditioning of the pigeon's key peck. Anim Learn Behav 5:25–38
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 85:1–19
Rescorla RA (1967) Pavlovian conditioning and its proper control procedures. Psychol Rev 74:71–80
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 7–33
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 7–35
Rizley RC, Rescorla RA (1972) Associations in second-order conditioning and sensory preconditioning. J Comp Physiol Psychol 81:1–11
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 85:149–168
Rose RM, Benjamin PR (1980b) Interneuronal control of feeding in the pond snailLymnaea stagnalis: II. The interneuronal mechanism generating feeding cycles. J Exp Biol 85:169–186
Saal W Vom, Jenkins HM (1970) Blocking the development of stimulus control. Learn Motiv 1:52–62
Sahley CL, Gelperin A, Rudy JW (1981) One-trial associative learning in a terrestrial mollusc. Proc Natl Acad Sci USA 78:640–642
Tennant WA, Bitterman ME (1975) Blocking and overshadowing in two species of fish. J Exp Psychol [Anim Behav] 104:22–29
Terry WS (1976) Effects of priming unconditioned stimulus representation in short-term memory on Pavlovian conditioning. J Exp Psychol [Anim Behav] 2:354–369
Walters ET, Carew TJ, Kandel ER (1979) Classical conditioning inAplysia californica. Proc Natl Acad Sci USA 76:6675–6679
Walters ET, Carew TJ, Kandel ER (1981) Associative learning inAplysia. Evidence for conditioned fear in an invertebrate. Science 211:504–506
Willows AOD (1980) Physiological basis of feeding behavior inTritonia II. Neuronal mechanisms. J Neurophysiol 44:849–961
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We thank D. Hogan and A. Nonneman for their critical comments and discussions of the manuscript. We also thank L. Cholewiak for help in collecting some of the data. This work was supported by NIH postdoctoral fellowship 5 F32 NS06221-02 to C.S. and NSF Grant BNS 8005822 and NIH Grant NSMH 15698 to A.G.
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Sahley, C., Rudy, J.W. & Gelperin, A. An analysis of associative learning in a terrestrial mollusc. J. Comp. Physiol. 144, 1–8 (1981). https://doi.org/10.1007/BF00612791
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DOI: https://doi.org/10.1007/BF00612791