Summary
The odor and taste processing systems of the terrestrial mollusc Limax maximus have been shown capable of a number of complex computations. Most of the complex higher-order features of Limax learning have been demonstrated using differential aversive conditioning. The present experiments probe the appetitive learning ability of Limax. In the first experiment a differential appetitive classical conditioning procedure was used. An aversive CS+ odor was paired with an attractive taste while a CS− odor was explicitly unpaired with the attractive taste. This appetitive conditioning procedure dramatically increased the preference for the CS+ odor. Further experiments determined the time course of acquisition, the effect of an extinction procedure and long-term retention of the appetitive conditioning. Now that Limax has been shown capable of appetitive conditioning, the neural network simulation of Limax learning, called LIMAX, can be examined for its ability to display appetitive conditioning.
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Abbreviations
- AA :
-
amyl acetate
- CS :
-
conditioned stimulus
- ISI :
-
interstimulus interval
- ITI :
-
intertrial interval
- MCH :
-
methylcyclohexanol
- US :
-
unconditioned stimulus
References
Alexander J Jr, Audesirk TE, Audesirk GJ (1984) One-trial reward learning in the snail Lymnaea stagnalis. J Neurobiol 15:67–72
Alkon DL (1974) Associative training of Hermissenda. J Gen Physiol 64:70–84
Audesirk TE, Alexander J Jr, Audesirk GJ, Moyer CM (1982) Rapid, nonaversive conditioning in a freshwater gastropod. I. Effects of age and motivation. Behav Neur Biol 36:379–390
Carew TJ, Walters ET, Kandel ER (1981) Classical conditioning in a simple withdrawal reflex in Aplysia californica. J Neurosci 1:1426–1437
Cook A, Radford DJ (1988) The comparative ecology of four sympatric limacid slug species in northern Ireland. Malacologia 28:131–146
Cook DG, Carew TJ (1986) Operant conditioning of head-waving in Aplysia. Proc Natl Acad Sci USA 83:1120–1124
Croll RP, Chase R (1977) A long-term memory for food odors in the land snail, Achatina fulica. Behav Biol 19:261–268
Croll RP, Chase R (1980) Plasticity of olfactory orientation to foods in the snail Achatina fulica. J Comp Physiol 136:267–277
Crow TJ (1988) Cellular and molecular analysis of associative learning and memory in Hermissenda. Trends Neurosci 11:136–142
Crow TJ, Alkon DL (1978) Retention of an associative behavioral change in Hermissenda. Science 201:1239–1241
Delaney K, Gelperin A (1986) Post-ingestive food-aversion learning to amino acid deficient diets by the terrestrial slug Limax maximus. J Comp Physiol A 159:281–295
Domjan M, Burkhardt B (1982) The principles of learning and behavior. Brooks/Cole, Monterey, CA
Farley J, Alkon DL (1980) Neural organization predicts stimulus specificity for a retained associative behavioral change. Science 210:1373–1375
Farley J, Alkon DL (1982) Associative neural and behavioral change in Hermissenda: Consequences of nervous system orientation for light and pairing-specificity. J Neurophysiol 48:785–807
Gelperin A (1975) Rapid food-aversion learning by a terrestrial mollusk. Science 189:567–570
Gelperin A, Hopfield JJ, Tank DW (1984) The logic of Limax learning. In: Selverston AI (ed) Model neural networks and behavior. Plenum Press, New York, pp 237–261
Gelperin A, Tank DW, Tesauro J (1988) Olfactory processing and associative learning: Cellular and modeling studies. In: Byrne JH, Berry W (eds) Neural models of plasticity. Academic Press, Orlando
Gormezano I (1975) Yoked comparison of classical and instrumental conditioning of the eyelid response; and an addendum on ‘voluntary responders’. In: Prokasy WF (ed) Classical conditioning: a symposium. New York, Appleton-Century-Crofts
Gould JL (1986) The biology of learning. Annu Rev Psychol 37:163–192
Gouyon PH, Fort Ph, Caraux G (1983) Selection of seedlings of Thymus vulgaris by grazing slugs. J Ecology 71:299–306
Hawkins RD, Carew TJ, Kandel ER (1986) Effects of interstimulus interval and contingency on classical conditioning of the Aplysia siphon withdrawal reflex. J Neurosci 6:1695–1701
Hollis KL (1984) Cause and function of animal learning processes. In: Marler P, Terrace HS (eds) The biology of learning. Springer, Berlin Heidelberg New York, pp 357–371
Hopfield JF, Gelperin A (1989) Differential conditioning to a compound stimulus and its components in the terrestrial mollusc Limax maximus. Behavioral Neurosci 103:329–333
Kemenes G, Benjamin PR (1989) Appetitive learning in snails shows characteristics of conditioning in vertebrates. Brain Res 489:163–166
Mackintosh NJ (1983) Conditioning and associative learning. Oxford Univ Press, New York
Mpitsos GJ, Cohan CS (1986a) Discriminative behavior and Pavlovian conditioning in the mollusc Pleurobranchaea. J Neurobiol 17:469–486
Mpitsos GJ, Cohan CS (1986b) Differential Pavlovian conditioning in the mollusc Pleurobranchaea. J Neurobiol 17:487–497
Mpitsos GJ, Collins SD (1975) Learning: Rapid aversive conditioning in the gastropod mollusc Pleurobranchaea. Science 108:954–957
Mpitsos GJ, Davis WJ (1973) Learning: Classical and avoidance conditioning in the mollusk Pleurobranchaea. Science 180:317–320
Reingold SC, Gelperin A (1980) Feeding motor program in Limax. II. Modulation by sensory inputs in intact animals and isolated central nervous system. J Exp Biol 85:1–19
Rescorla RA (1988) Behavioral studies of Pavlovian conditioning. Annu Rev Neurosci 11:329–352
Revusky SH, Garcia J (1971) Learned associations over long delays. In: Bower GH (ed) The psychology of learning and motivation. Raven Press, New York, pp 1–84
Sahley CL (1984) Behavior theory and invertebrate learning. In: Marler P, Terrace HS (eds) The biology of learning. Springer, Berlin Heidelberg New York, pp 181–196
Sahley CL (1990) The behavioral analysis of associative learning in the terrestrial mollusc, Limax maximus: The importance of interevent relationships.In: Hanson S, Olson C (eds) Connectionist modeling and brain function: The developing interface. MIT Press, Cambridge, MA, pp 36–73
Sahley CL, Gelperin A, Rudy J (1981a) One-trial associative learning modifies food odor preferences of a terrestrial mollusc. Proc Natl Acad Sci USA 78:640–642
Sahley CL, Rudy JW, Gelperin A (1981b) An analysis of associative learning in a terrestrial mollusc: Higher-order conditioning, blocking and a transient US pre-exposure effect. J Comp Physiol 144:1–8
Sahley CL, Rudy JW, Gelperin A (1984) Associative learning in a mollusc: A comparative analysis. In: Alkon DL, Farley J (eds) Primary neural substrates of learning and behavioral change. Cambridge Univ Press, New York, pp 243–258
Sahley CL, Hardison P, Hsuan A, Gelperin A (1982) Appetitively reinforced odor-conditioning modulates feeding in Limax maximus. Soc Neurosci Abstr 8:823
Schneiderman N (1966) Interstimulus interval function of the nictitating membrane response of the rabbit under delay versus trace conditioning. J Comp Physiol Psychol 62:397–402
Seligman MEP (1970) On the generality of the laws of learning. Psychol Rev 77:406–418
Staddon JER, Ettinger Rh (1989) Learning. An introduction to the principles of adaptive behavior. Harcourt Brace Jovanovich, New York
Susswein AJ, Schwarz M, Feldman E (1986) Learned changes of feeding behavior in Aplysia in response to edible and inedible foods. J Neurosci 6:1513–1527
Whelan RJ (1982) Response of slugs to unacceptable food items. J Appl Ecol 19:79–87
Winer BJ (1971) Statistical principles in experimental design. McGraw Hill, New York
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Sahley, C.L., Martin, K.A. & Gelperin, A. Analysis of associative learning in the terrestrial mollusc Limax maximus. II. Appetitive learning. J Comp Physiol A 167, 339–345 (1990). https://doi.org/10.1007/BF00192569
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DOI: https://doi.org/10.1007/BF00192569