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Parallel neural systems for classical conditioning: Support from computational modeling

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Abstract

Classical conditioning has been explained by two main types of theories that postulate different learning mechanisms. Rescorla and Wagner (1972) put forth a theory in which conditioning is based on the ability of the US to drive learning through error correction. Alternatively, Mackintosh (1973) put forth a theory in which the ability of the CS to be associated with the unconditioned stimulus is modulated. We have proposed a reconciliation of these two mechanisms as working in parallel within different neural systems: a cerebellar system for US modulation and a hippocampal system for CS modulation. We developed a computational model of cerebellar function in eyeblink conditioning based on the error correction mechanism of the Rescorla-Wagner rule in which learningrelated activity from the cerebellum inhibits the inferior olive, which is the US input pathway to the cerebellum (Gluck et al., 1994). We developed a computational model of the hippocampal region that forms altered representations of conditioned stimuli based on their behavioral outcomes (Gluck & Myers, 1993; Myers et al., 1995). Overall, computational modeling and empirical findings support the idea that, at least in the case of eyeblink conditioning, there may be two different neural systems: the cerebellum which mediates US-based error correction and hippocampus which alters representations of CSs.

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References

  • Allen, M.T., Chelius, L. & Gluck, M.A. (1998) Selective entorhinal ibotenic lesions disrupt the learned irrelevance pre-exposure effect in the classically conditioned rabbit eyeblink response paradigm conditioningSociety for Neuroscience Abstracts. 24.

  • Allen, M.T., Myers, C.E. & Gluck, M.A. (under review) Entorhinal lesions, but not hippocampal lesions, disrupt learned irrelevance in rabbit eyeblink conditioning.Psychobiology.

  • Andersson, G., & Hesslow, G. (1987). Inferior olive excitability after high frequency climbing fibre activation in the cat.Experimental Brain Research. 67(3):523–32.

    Google Scholar 

  • Andersson, G., Garwicz, M., & Hesslow G. (1988). Evidence for a GABA-mediated cerebellar inhibition of the inferior olive in the cat.Experimental Brain Research.72(3):450–6.

    Article  Google Scholar 

  • Baruch I., Hemsley, D.R., & Gray, J.A. (1988). Differential performance of acute and chronic schizophrenics in a latent inhibition task.Journal of Nervous & Mental Disease.176:598–606.

    Article  Google Scholar 

  • Berger, T. & Orr, W. (1983). Hippocampectomy selective disrupts discrimination reversal learning of the rabbit nictitating membrane response.Behavioral Brain Research. 8:49–68.

    Article  Google Scholar 

  • Clark, R.E. and D.G. Lavond (1993). Reversible lesions of the red nucleus during acquisition and retention of a classically conditioned behavior in rabbit.Behavioral Neuroscience. 107:264–270.

    Article  PubMed  Google Scholar 

  • Clark, R.E., A.A. Zhang, & Lavond, D.G. (1992). Reversible lesions of the cerebellar interpositus nucleus during acquisition and retention of a classically conditioned behavior.Behavioral Neuroscience. 106:879–888.

    Article  PubMed  Google Scholar 

  • Donegan, N.H., M.R. Foy, & Thompson, R.F. (1985). Neuronal responses of the rabbit cerebellar cortex during performance of the classically conditioned eyelid response.Neuroscience Abstracts 11:245–8.

    Google Scholar 

  • Donegan, N.H., M.A. Gluck, & Thompson, R.F. (1989). Integrating behavioral and biological models of conditioning.Psychology of Learning and Motivation, Academic Press. 3:109–156.

  • Donegan, N.H. & Wagner, A.R. (1987). Conditioned diminution and facilitation of the UR: A sometimes opponent-process interpretation. Gormezano, I (Ed.); Prokasy, W.F. (Ed); (1987).Classical conditioning (3rd ed.). Hillsdale, NJ, USA: Lawrence Erlbaum Associates, Inc: Foy, M.R. and R.F. Thompson (1986). “Single unit analysis of Parkinje cell discharge in classically conditioned and untrained rabbits.”Neuroscience Abstracts 12:518.

    Google Scholar 

  • Gluck, M.A., & Bower, G.H. (1988). From conditioning to category learning: an adaptive network model.Journal of Experimental psychology: General. 117:227–247.

    Article  Google Scholar 

  • Gluck, M.A., E.S. Reifsnider, & Thompson, R.F. (1990). Adaptive signal processing and the cerebellum: Models of classical conditioning and VOR adaptation.Neuroscience and Connectionist Theory. M. A. Gluck and D.E. Rumelhart. Hillsdale, NJ, Lawrence Erlbaum: 131–185.

    Google Scholar 

  • Gluck, M. and C. Myers (1993). Hippocampal mediation of stimulus representation: A computational theory.Hippocampus. 3:491–516.

    Article  PubMed  Google Scholar 

  • Gluck, M., C. Myers, & Thompson, R.F. (1994). A computational model of the cerebellum and motor-reflex conditioning.An Introduction to Neural and Electronic Networks. Zornetzer, Davis, Lau and McKenna. New York: Academic Press: 91–98.

    Google Scholar 

  • Gormezano, I., E.J. Kehoe, & Marshall, B.S. (1983). “Twenty years of classical conditioning research with the rabbit.”Progress in Psychobiology and Physiological Psychology. 10:197–275.

    Google Scholar 

  • Han, J.S., Gallager, M. & Holland, P.C. (1995). Hippocampal lesions disrupt increments but not decrements in stimulus processing.Journal of Neuroscience. 15:7323–7329.

    PubMed  Google Scholar 

  • Hebb, D.O. (1949)The organization of behavior; a neuropsychological theory. New York: Wiley. Hesslow, G., & Ivarsson, M. (1996). Inhibition of the inferior olive during conditioned responses in the decerebrate ferret.Experimental Brain Research. 110:36–46.

    Google Scholar 

  • Holland, P. (1997). Brain mechanisms for changes in processing of conditioned stimuli in Pavlovian conditioning: Implications for behavior theory.Animal Learning and Behavior. 25(4):373–399.

    Article  Google Scholar 

  • Honey, R., & Good, M. (1993). Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning.Behavioral Neuroscience, 107(1),23–33.

    Article  PubMed  Google Scholar 

  • Hull, C. (1943).Principles of Behavior. New York: Appleton-Century-Crofts.

    Google Scholar 

  • Ito, M. (1984).The Cerebellum and Neural Control. New York: Raven Press.

    Google Scholar 

  • Jones, S.H., Hemsley, D.R., & Gray, J.A. (1991). Contextual effects on choice reaction time and accuracy in acute and chronic schizophrenics. Impairment in selective attention or in the influence of prior learning?.British Journal of Psychiatry. 159:415–21.

    Article  PubMed  Google Scholar 

  • Kamin, L. (1969). Predictability, surprise, attention and conditioning.Punishment and Aversive Behavior. B. Campbell and R. Church. New York: Appleton-Century-Crofts: 279–296.

    Google Scholar 

  • Kehoe, E. (1981). Stimulus selection and combination in classical conditioning with the rabbit.Classical Conditioning. I. Gormezano, W. Prokasy and R. Thompson. Hillsdale, NJ; Erlbaum:

    Google Scholar 

  • Kim, J., D. Krupa, & Thompson, R.F. (1998). Inhibitory cerebello-olivary projections and blocking effect in classical conditioning.Science. 279:570–573.

    Article  PubMed  Google Scholar 

  • Kim, J.J., & Thompson, R.F. (1997). Cerebellar circuits and synaptic, mechanisms involved in classical eyeblink conditioning.Trends in Neuroscience, 20:177–181.

    Article  Google Scholar 

  • Krupa, D.J., J.K. Thompson, & Thompson R.F. (1993). Localization of a memory trace in the mammalian brain.Science. 260:989–99.

    Article  PubMed  Google Scholar 

  • Krupa, D.J. and R.F. Thompson (1995). Inactivation of the superior cerebellar peduncle blocks expression but not acquisition of the rabbit's classically conditioned eyeblink response.Proceedings of the National Academy of Science. 92:5097–5101.

    Article  Google Scholar 

  • Lavond, D.G., J.E. Steinmetz, Yokaitis, M.H., & Thompson, R.F. (1987). Reacquisition of classical conditioning after removal of cerebellar cortex.Experimental Brain Research. 67:569–593.

    Article  Google Scholar 

  • Lubow, R. (1973). Latent Inhibition.Psychological Bulletin. 79:398–407.

    Article  PubMed  Google Scholar 

  • Mackintosh, N. (1973). Stimulus selection: Learning to ignore stimuli that predict no change in reinforcement. In R. Hinde & J. Stevenson-Hinde (Eds.),Constraints on Learning: Limitations and Predispositions (pp. 75–96). New York: Academic Press.

    Google Scholar 

  • Mackintosh, N.J. (1975). A theory of attention: Variations in the associability of stimuli with reinforcement.Psychological Review. 82(4):276–298.

    Article  Google Scholar 

  • Marchant, H. and J. Moore (1973). Blocking of the rabbit's conditioned nictitating membrane response in Kamin's two-stage paradigm.Journal of Experimental Psychology 101(1):155–158.

    Article  PubMed  Google Scholar 

  • Martin, I. and A. Levey (1991). Blocking observed in human eyelid conditioning.Quarterly Journal of Experimental Psychology B: Comparative and Physiological Psychology. 43(3):233–256.

    Google Scholar 

  • McCormick, D. and R. Thompson (1982). Locus coeruleus lesions and resistance to extinction of a classically conditioned response: Involvement of the neocortex and hippcoampus.Brain Research. 245(2):239–249.

    Article  PubMed  Google Scholar 

  • Myers, E.C., Gluck, M.A., & Granger, R. (1995). Dissociation of hippocampal and entorhinal function in associativelearning: A computational approach.Psychobiology. 23:116–138.

    Google Scholar 

  • Nelson, B., & Mugnoini, E. (1987). GABAergic innervation of the inferior olivary complex and experimental evidence for its origin.In P. Strata (Ed.),The olivocerebellar system in motor control. New York: Springer-Verlag.

    Google Scholar 

  • Pearce, J. and G. Hall (1980). A model for Pavlovian learning: Variations in the effectiveness of conditioned but not of unconditioned stimuli.Psychological Review. 87:532–552.

    Article  PubMed  Google Scholar 

  • Penick, S., & Solomon, P. (1991). Hippocampus, context, and conditioningBehavioral Neuroscience. 105(5):611–617.

    Article  PubMed  Google Scholar 

  • Perret, S.P., Ruiz, B.P., & Mauk, M.D. (1993). Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses.Journal of Neuroscience. 13(4):1708–1718.

    Google Scholar 

  • Port, R.L., & Patterson, M.M. (1984). Fimbrial lesions and sensory preconditioning.Behavioral Neuroscience. 98:584–589.

    Article  PubMed  Google Scholar 

  • Ramirez, O.A., A.F. Nordholm, & Thompson, R.F. (1997). The conditoned eyeblink response: A role for the GABA-B receptor.Pharmacology, biochemistry and Behavior. 58:127–132.

    Article  Google Scholar 

  • Rescorla, R. (1968). “Probability of shock in the presence and absence of CS in fear conditioning.”Journal of Comparative and Physiological Psychology. 66(1):1–5.

    Article  PubMed  Google Scholar 

  • Rescorla, R. and A. Wagner (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and non-reinforcement.Classical Conditioning II: Current Research and Theory, A. Black and W. Prokasy. New York: Appleton-Century-Crofts: 64–99.

    Google Scholar 

  • Schmajuk, N.A., & DiCarlo, J.J. (1991). A neural network approach to hippocampal function in classical conditioning.Behavioral Neuroscience, 105(1):82–110. Schmaltz, L. and J. Theios (1972). “Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus).”Journal of Comparative and Physiological Psychology. 79:328–333.

    Article  PubMed  Google Scholar 

  • Schmaltz, L.W., & Theios, J. (1972). Acquisition and extinction of a classically conditioned response in Hippocampectomized rabbits (oryctolagus cuniculus).Journal of Comparative and Physiological Psychology. 79:328–333.

    Article  PubMed  Google Scholar 

  • Sears, L. and J. Steinmetz (1990). Acquisition of classically conditioned-related activity in the hippocampus is affected by lesions of the cerebellar interpositus nucleus.Behavioral Neuroscience. 104(5):681–692.

    Article  PubMed  Google Scholar 

  • Shohamy, D., Allen, M.T., & Gluck, M.A. (2000). Dissociating entorhinal and hippocampal function in latent inhibition.Behavioral Neuroscience. 114:867–874.

    Article  PubMed  Google Scholar 

  • Solomon, P.R., Crider, A., Winkelman, J.W., Turi, A., Kamer, R.M., & Kaplan L.J. (1981). Disrupted latent inhibition in the rat with chronic amphetamine or haloperidol-induced supersensitivity: relationship to schizophrenic attention disorder.Biological Psychiatry. 16(6):519–37.

    PubMed  Google Scholar 

  • Solomon, P. and J. Moore (1975). Latent inhibition and stimulus generalization of the classically conditioned nictiating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation.Journal of Comparative and Physiological Psychology. 89:1192–1203.

    Article  PubMed  Google Scholar 

  • Solomon, P. (1977). Role of the hippocampus in blocking and conditioned inhibition of the rabbit's nictiating membrane.Journal of Comparative and Physiological Psychology. 91(2):407–417.

    Article  PubMed  Google Scholar 

  • Spence, K.W. (1956).Behavior Theory and Conditioning. New Haven, CT: Yale University Press

    Book  Google Scholar 

  • Steinmetz, J.E., Lavond, D.G., & Thompson, R.F. (1989). Classical conditoning in rabbits using pontine nucleus stimulation as a conditioned stimulus and inferior olive stimulation as an unconditioned stimulus.Synapse. 3:225–233.

    Article  PubMed  Google Scholar 

  • Steinmetz, J.E., Logue, S.F., & Steinmetz, S.S. (1992). Rabbit classically conditioned eyelid responses do not reappear after interpositus lesion and extensive post-lesion training.Behavioral Brain Research. 541:103–114.

    Article  Google Scholar 

  • Steinmetz, J.E., Rosen, D.J., Chapman, P.F., Lavond, D.G., & Thompson, R.F. (1986). “Classical conditioning of the rabbit eyelid response with a mossy fiber stimulation CS. I.Behavioral Neuroscience. 100:878–887

    Article  PubMed  Google Scholar 

  • Steinmetz, J.E., & Sengelaub, D.R. (1992). Possible conditioned stimulus pathway for classical eyelid conditioning in rabbits: a anatomical evidence for direct projections from the pontine nuclei to the cerebellar interpositus nucleus.Behavioral & Neural Biology. 57:103–115.

    Article  Google Scholar 

  • Steinmetz, J.E., & Thompson, R.F. (1991). Brain substrates of aversive classical conditioning. In J.M. IV (Eds.), Neurobiology of learning emotion and affect (pp. 97–120). New York: Raven Press Ltd.

    Google Scholar 

  • Tracey, J., Thompson, J.K., Krupa, D.J., & Thompson, R.F. (1998). Evidence of plasticity in the pontocerebellar CS pathway during classical conditioning of the eyeblink response in the rabbit.Behavioral Neuroscience. 112:267–285. Wagner, A. R. (1981). SOP: A model of automatic memory processing in animal behavior. In N. E. Spear & R. R. Miller (Eds.),Information processing in animals: Memory mechanism (pp. 5–47). Hillsdale, NJ: Erlbaum.

    Article  Google Scholar 

  • Wagner, A.R. (1981). SOP: A model of automatic memory processing in animal behavior.,Information Processing in Animals: Memory Mechanisms. N. Spear and R. Miller. Hillsdale, NJ, Erlbaum: 5–47.

    Google Scholar 

  • Wagner, A.R., & Brandon, S.E. (1989). Evolution of a structured connectionist model of Pavlovian conditioning (AESOP). In S.B. Klein and R.R. Mowrer (Eds.),Contemporary Learning Theories. Hillsdale, NJ: Erlbaum.

    Google Scholar 

  • Wagner, A.R. & Rescorla, R. (1972). Inhibition in Pavlovian conditioning: Application of a theory.Inhibition and Learning. Weiner I. Lubow RE. Feldon J. 1984 Abolition of the expression but not the acquisition of latent inhibition by chronic amphetamine in rats.Psychopharmacology. 83(2):194–9.

    Google Scholar 

  • Weiss, C., McCurdy, M.L., Houk, J.C., & Gibson, A.R. (1985). Anatomy and physiology of dorsal column afferents to forelimb dorsal accessory olive.Society for Neuroscience Abstracts, 11, 182.

    Google Scholar 

  • Woodruff-Pak, D., D. Lavond, Logan, C.G., Steinmetz, J.E., & Thompson, R.F. (1993). Cerebellar cortical lesions and reacquisition in classical conditioning of the nictitating membrane response in rabbits.Brain Research. 608(1):67–77.

    Article  PubMed  Google Scholar 

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  1. Center for Molecular & Behavioral Neuroscience, Rutgers University, the State University of New Jersey, 197 University Ave., 07102, Newark, NJ

    M. Todd Allen, Catherine E. Myers & Mark A. Gluck

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  1. M. Todd Allen
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  2. Catherine E. Myers
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Correspondence to M. Todd Allen.

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Allen, M.T., Myers, C.E. & Gluck, M.A. Parallel neural systems for classical conditioning: Support from computational modeling. Integr. psych. behav. 36, 36–61 (2001). https://doi.org/10.1007/BF02733946

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