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Neuroscience of Pavlovian Conditioning: A Brief Review

Published online by Cambridge University Press:  10 April 2014

Luis Aguado
Luis Aguado*
Affiliation:
Complutense University of Madrid
*
Correspondence concerning this article should be addressed to Luis Aguado, Departamento de Psicología Básica I, Facultad de Psicología, Campus de Somosaguas, 28223 – Madrid (Spain). E-mail: psbas17@sis.ucm.es
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Abstract

Current knowledge on the neuronal substrates of Pavlovian conditioning in animals and man is briefly reviewed. First, work on conditioning in aplysia, that has showed amplified pre-synaptic facilitation as the basic mechanism of associative learning, is summarized. Then, two exemplars of associative learning in vertebrates, fear conditioning in rodents and eyelid conditioning in rabbits, are described and research into its neuronal substrates discussed. Research showing the role of the amygdala in fear conditioning and of the cerebellum in eyelid conditioning is reviewed, both at the circuit and cellular plasticity levels. Special attention is given to the parallelism suggested by this research between the neuronal mechanisms of conditioning and the principles of formal learning theory. Finally, recent evidence showing a similar role of the amygdala and of the cerebellum in human Pavlovian conditioning is discussed.

El artículo revisa brevemente los conocimientos actuales acerca de los substratos neuronales del condicionamiento pavloviano en los animales y en el hombre. En primer lugar, se resume la investigación sobre condicionamiento en aplysias, que ha demostrado la importancia de la facilitación sináptica amplificada como mecanismo básico del aprendizaje asociativo. A continuación, se describen dos ejemplos de aprendizaje asociativo en vertebrados, el condicionamiento del miedo en roedores y el condicionamiento del parpadeo en conejos, con referencias a la investigación sobre sus substratos neuronales. Se revisa la investigación que muestra el papel de la amígdala en el condicionamiento del miedo y del cerebelo en el condicionamiento del parpadeo, al nivel tanto de circuitos como de la plasticidad celular. Se presta especial atención a los paralelismos que esta área de investigación sugiere entre los mecanismos neuronales del condicionamiento y los principios de las teorías formales del aprendizaje. Por último, se comentan diversas pruebas recientes que demuestran un papel semejante de la amígdala y del cerebelo en el condicionamiento pavloviano humano.

Keywords

Pavlovian conditioningneural mechanismslearning theoriescondicionamiento pavlovianomecanismos neuralesteorias del aprendizaje
Type
Research Article
Information
The Spanish Journal of Psychology , Volume 6 , Issue 2: Special Issue: A Century of Pavlovian Theory: The Madrid Lecture (Pavlov, 1903) , November 2003 , pp. 155 - 167
Copyright
Copyright © Cambridge University Press 2003

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References

Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 372, 669–672.CrossRefGoogle Scholar
Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1995). Fear and the human amygdala. Journal of Neuroscience, 15, 5879–5892.CrossRefGoogle ScholarPubMed
Alkon, D. (1987). Memory traces in the brain. Cambridge, UK: Cambridge University Press.Google Scholar
Allen, M., Myers, C., & Gluck, M. (2001). Parallel neural systems for classical conditioning: Support from computational modelling. Integrative Physiological and Behavioral Science, 36, 1, 36–61.CrossRefGoogle Scholar
Antonov, I., Antonova, I., Kandel, E., & Hawkins, R. (2001). The contribution of activity-depedent synaptic plasticity to classical conditioning in aplysia. Journal of Neuroscience, 21, 16, 6413–6422.CrossRefGoogle Scholar
Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, Ch., & Damasio, A., (1995). Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science, 269, 1115–1118.CrossRefGoogle Scholar
Bliss, T., & Collingridge, G. (1993). A synaptic model of memory: Long-term potentiation in the hippocampus. Nature, 361, 31–49.CrossRefGoogle ScholarPubMed
Bouton, M. (1993). Context, time and memory retrieval in the interference paradigms of Pavlovian conditioning. Psychological Bulletin, 114, 80–99.CrossRefGoogle Scholar
Büchel, C., Morris, J., Dolan, R., & Friston, K. (1998). Brain systems mediating aversive conditioning: An event-related fMRI study. Neuron, 20, 947–957.CrossRefGoogle ScholarPubMed
Cahill, L., Weinberger, N., Rozendaal, B., & McGaugh, J. (1999). Is the amygdala a locus of “conditioned fear”? Some questions and caveats. Neuron, 23, 227–228.CrossRefGoogle ScholarPubMed
Castellucci, V., & Kandel, E. (1974). A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. Proceedings of the Natural Academy of Sciences, USA, 71, 5004–5008.CrossRefGoogle ScholarPubMed
Castellucci, V., & Kandel, E. (1976). Presynaptic facilitation as a mechanism for behavioral sensitization in Aplysia. Science, 194, 1176–1178.CrossRefGoogle ScholarPubMed
Chen, C., & Thompson, R.F. (1995). Temporal specificity of long-term depression in parallel fiber-Purkinje synapses in rat cerebellar slice. Learning & Memory, 2, 185–198.CrossRefGoogle ScholarPubMed
Clark, G. (1984). A cellular mechanism for the temporal specificity of classical conditioning of the siphon withdrawal response in Aplysia. Society of Neuroscience Abstracts, 10, 268.Google Scholar
Clark, R., Manns, J., & Squire, L. (2002). Classical conditioning, awareness, and brain systems. Trends in Cognitive Sciences, 6, 12, 524–531.CrossRefGoogle ScholarPubMed
Clark, R., & Squire, L. (1998). Classical conditioning and brain systems: A key role for awareness. Science, 280, 77–81.CrossRefGoogle Scholar
Daum, L., Channon, S., & Canavan, A. (1989). Classical conditioning in patients with severe memory problems. Journal of Neurology, Neurosurgery & Psychiatry, 52, 47–51.CrossRefGoogle ScholarPubMed
Diamond, D., & Weinberger, N. (1986). Classical conditioning rapidly induces specific changes in frequency receptive fields of single neurons in secondary and ventral ectosylvian auditory cortical fields. Brain Research, 372, 357–360.CrossRefGoogle ScholarPubMed
Dickinson, A. (1980). Contemporary animal learning theory. Cambridge, UK: Cambridge University Press.Google Scholar
Donegan, N., Foy, M., & Thompson, R.F. (1985). Neuronal responses of the rabbit cerebellar cortex during performance of the classically conditioned eyelid response. Neuroscience Abstracts, 11, 245–248.Google Scholar
Dudai, Y. (1989). The neurobiology of memory. Oxford: Oxford University Press.Google Scholar
Dudai, Y. (1988). Neurogenetic dissection of learning and shortterm memory in drosophila. Annual Review of Neuroscience, 11, 537–563.CrossRefGoogle ScholarPubMed
Edeline, J., Pham, P., & Weinberger, N. (1993). Rapid development of learning-induced receptive field plasticity in the auditory cortex. Behavioral Neuroscience, 107, 539–551.CrossRefGoogle ScholarPubMed
Edeline, J., & Weinberger, N. (1992). Associative retuning in the thalamic source of input to the amygdala and auditory cortex: receptive field plasticity in the medial division of the medial geniculate body. Behavioral Neuroscience, 106, 81–105.CrossRefGoogle Scholar
Fanselow, M. (1994). Neural organization of the defensive behavior system responsible for fear. Psychonomic Bulletin & Review, 1, 429–438.CrossRefGoogle ScholarPubMed
Fanselow, M., & Kim., J. (1994). Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist, D,L-2-amino-phosphonovaleric acid, to the basolateral amygdala. Behavioral Neuroscience, 108, 210–212.CrossRefGoogle Scholar
Freeman, J., & Nicholson, D. (1999). Neuronal activity in the cerebellar interpositus and lateral pontine nuclei during inhibitory classical conditioning of the eyeblink response. Brain Research, 833, 225–233.CrossRefGoogle ScholarPubMed
Gabriel, M. (1988). An extended laboratory for behavioral neuroscience: A review of Classical Conditioning (3rd ed.). Psychobiology, 16, 1, 79–81.Google Scholar
Gabrieli, J., McGlinchey-Berroth, R., Carrillo, M., & Gluck, M. (1995). Intact delay-eyeblink classical conditioning in amnesia. Behavioral Neuroscience, 109, 819–827.CrossRefGoogle ScholarPubMed
Gluck, M., & Granger, R. (1993). Computational models of the neural bases of learning and memory. Annual Review of Neuroscience, 16, 667–706.CrossRefGoogle ScholarPubMed
Gluck, M., & Thompson, R.F. (1987). Modelling the neural substrates of associative learning and memory: A computational approach. Psychological Review, 94, 176–191.CrossRefGoogle ScholarPubMed
Gormezano, I., Kehoe, J., & Marshall, B. (1983). Twenty years of classical conditioning research with the rabbit. Progress in Psychobiology and Physiological Psychology, 10, 197–275.Google Scholar
Hansen, Ch., Linden, D., & D'Angelo, E. (2001). Beyond parallel fiber LTD: The diversity of synaptic and non-synaptic plasticity in the cerebellum. Nature Neuroscience, 4, 467–475.CrossRefGoogle Scholar
Hawkins, R., Abrams, T., Carew, T., & Kandel, E. (1983). A cellular mechanism of classical conditioning in Aplysia: Activity-dependent amplification of presynaptic facilitation. Science, 219, 400–405.CrossRefGoogle ScholarPubMed
Hawkins, R., & Kandel, E. (1984). Is there a cell-biological alphabet for simple forms of learning? Psychological Review, 91, 375–391.CrossRefGoogle Scholar
Hawkins, R., Kandel, E., & Siegelbaum, S. (1993). Learning to modulate transmitter release: Themes and variations in synaptic plasticity. Annual Review of Neuroscience, 16, 625–665.CrossRefGoogle ScholarPubMed
Hebb, D.O. (1949). The organization of behavior. NewYork: Wiley.Google Scholar
Kamin, L. (1969). Predictability, surprise, attention and conditioning. In Church, R.M. (Ed.), Punishment and aversive behavior (pp. 279–296). New York: Appleton.Google Scholar
Kim, J., Krupa, D., & Thompson, R. (1998). Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. Science, 279, 570–573.CrossRefGoogle ScholarPubMed
Knuttinen, M., Power, J.M., Prewston, A., & Disterhoft, J. (2001). Awareness in classical differential eyelid conditioning in young and aged humans. Behavioral Neuroscience, 115, 747–757.CrossRefGoogle Scholar
LaBar, K., Gatenby, J., Gore, J., LeDoux, J., & Phelps, E. (1995). Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study. Neuron, 20, 937–945CrossRefGoogle Scholar
Lavond, D., & Steinmetz, J. (1989). Acquisition of classical conditioning without the cerebellar cortex. Behavioural and Brain Research, 33, 113–164.CrossRefGoogle ScholarPubMed
LeDoux, J. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 255–284.CrossRefGoogle ScholarPubMed
LeDoux, J., Farb, C., & Romanski, L. (1991). Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex. Neuroscience Letters, 134, 139.CrossRefGoogle Scholar
LeDoux, J., Sakaguchi, A., & Reis, D. (1984). Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned by acoustic stimuli. Journal of Neuroscience, 4, 683–698.CrossRefGoogle ScholarPubMed
Lee, H., & Kim, J. (1998). Amygdalar NMDA receptors are critical for new learning in previously fear-conditioned rats. Journal of Neuroscience, 18, 8444–8454.CrossRefGoogle ScholarPubMed
Lin, X.Y., & Glanzman, D.L. (1997). Effect of interstimulus interval on pairing-induced LTP of Aplysia sensorimotor synapses in cell culture. Journal of Neurophysiology, 77, 667–674.CrossRefGoogle ScholarPubMed
Manns, J. (2000). Standard delay eyeblink classical conditioning is independent of awareness. Journal of Experimental Psychology: Animal Behavior Processes, 28, 32–37.Google Scholar
Maren, S. (2001). Neurobiology of Pavlovian fear conditioning. Annual Review of Neuroscience, 24, 897–931.CrossRefGoogle ScholarPubMed
Maren, S., Poremba, A., & Gabriel, M. (1991). Basolateral amygdaloid multi-unit neuronal correlates of discriminative avoidance learning in rabbits. Brain-Research, 549, 311–316.CrossRefGoogle ScholarPubMed
Martin, K., Casadio, Y., Zhu, J., Rose, M., Chen, C., Bailey, C., & Kandel, E. (1997). Synapse-specific, long-term faciliation of Aplysia sensory to motor synapses: A function for local protein synthesis in memory storage. Cell, 91, 927–938.CrossRefGoogle Scholar
McCormick, D., & Thompson, R. (1984a). Cerebellum: essential involvement in the classically conditioned eyelid response. Science, 223, 296–299.CrossRefGoogle ScholarPubMed
McCormick, D., & Thompson, R. (1984b). Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane response. Journal of Neuroscience, 4, 2811–2822.CrossRefGoogle Scholar
McGlinchey-Berroth, R. (1997). Impaired trace eyeblink conditioning in bilateral, medial-temporal lobe amnesia. Behavioral Neuroscience, 111, 873–882.CrossRefGoogle ScholarPubMed
Medina, J., & Mauk, M. (2000). Computer simulation of cerebellar information processing. Nature Neuroscience, 3, 1205–1211.CrossRefGoogle ScholarPubMed
Medina, J., García, K., & Mauk, M. (2001). A mechanism for savings in the cerebellum. Journal of Neuroscience, 21, 11, 4081–4089.CrossRefGoogle ScholarPubMed
Medina, J., Repa, J., Mauk, M., & LeDoux, J. (2002). Parallels between cerebellum- and amygdala-dependent conditioning. Nature Reviews Neuroscience, 3, 122–131.CrossRefGoogle ScholarPubMed
Morris, J., Büchel, C., & Dolan, R.J. (2001). Parallel responses in amygdala subregions and sensory cortex during implicit fear conditioning. Neuroimage, 13, 1044–1052.CrossRefGoogle ScholarPubMed
Morris, J., Ohman, A., & Dolan, R. (1998). Conscious and unconscious emotional learning in the human amygdala. Nature, 393, 467–470.CrossRefGoogle ScholarPubMed
Morris, J., Ohman, A., & Dolan, R. (1999). A subcortical pathway to the right amygdala mediating ‘unseen’ fear. Proceedings of the National Academy of Science, 96, 1680–1685.CrossRefGoogle Scholar
Murphy, G., & Glanzman, D. (1997). Mediation of classical conditioning in aplysia californica by long-term potentiation of sensorimotor synapses. Science, 278, 467–471.CrossRefGoogle ScholarPubMed
Ohman, A., & Soares, J. (1998). Emotional conditioning to masked stimuli: Expectancies for aversive outcomes following nonrecognized fear-relevant stimuli. Journal of Experimental Psychology: General, 127, 69–82.CrossRefGoogle ScholarPubMed
Ohyama, T., & Mauk, M. (2001). Latent acquisition of timed responses in cerebellar cortex. Journal of Neuroscience, 21, 682–690.CrossRefGoogle ScholarPubMed
Perret, S., Ruiz, B., & Mauk, M. (1993). Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. Journal of Neuroscience, 13, 1708–1718.CrossRefGoogle Scholar
Phelps, E., O'Connor, K., Gatenby, Ch., Gore, J., Grillon, Ch., & Davis, M. (2001). Activation of the left amygdala to a cognitive representation of fear. Nature Neuroscience, 4, 437–441.CrossRefGoogle ScholarPubMed
Quirk, G., Armony, J., & LeDoux, J. (1997). Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron, 19, 613–624.CrossRefGoogle ScholarPubMed
Quirk, G., Repa, C., & LeDoux, J. (1995). Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: Parallel recordings in the freely behaving rat. Neuron, 15, 1029–1039.CrossRefGoogle ScholarPubMed
Repa, J. (2001). Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nature Neuroscience, 4, 724–731.CrossRefGoogle Scholar
Repa, J., Muller, J., Aspergis, J., Desrochers, T., Zhou, Y., & LeDoux, J. (2001). Two differente lateral amygdala cell populations contribute to the initiation and storage of memory. Nature Neuroscience, 4, 724–731.CrossRefGoogle Scholar
Rescorla, R.A. (1988). Behavioral studies of Pavlovian conditioning. Annual Review of Neuroscience, 11, 329–352.CrossRefGoogle ScholarPubMed
Rescorla, R. A., & Wagner, A.R. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and non-reinforcement. In Black, A. & Prokasy, W. (Eds.), Classical Conditioning II: Current Research and Theory (64–99). New York: Appleton.Google Scholar
Romanski, L., LeDoux, J., Cugnet, M., & Bordi, F. (1993). Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behavioral Neuroscience, 107, 444–450.CrossRefGoogle ScholarPubMed
Sahley, C. (1984). Associative learning in a mollusk: A comparative analyses. In Alkon, D. & Farley, J. (Eds.), Primary neural substrates of learning and behavior change (pp. 243–258). Cambridge: Cambridge University Press.Google Scholar
Schafe, G., & LeDoux, J. (2000). Memory consolidation of auditory Pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. Journal of Neuroscience, 20, 1–5.CrossRefGoogle ScholarPubMed
Schultz, W., Apicella, P., & Ljunberg, T. (1993). Responses of monkey dopamine neurons to reward and conditioned stimuli during succesive steps of learning a delayed response task. Journal of Neuroscience, 13, 900–913.CrossRefGoogle Scholar
Schultz, W., Dayan, P., & Montague, P. (1997). A neural substrate of prediction and reward. Science, 275, 1593–1599.CrossRefGoogle ScholarPubMed
Schultz, W., & Dickinson, A. (2000). Neuronal coding of prediction errors. Annual Review of Neuroscience, 23, 473–500.CrossRefGoogle ScholarPubMed
Sears, L., & Steinmetz, J. (1991). Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain-Research, 545, 114–122.CrossRefGoogle ScholarPubMed
Solomon, P., Vander Schaff, E., Thompson, R.F., & Weisz, D. (1986). Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behavioral Neuroscience, 100, 729–744.CrossRefGoogle ScholarPubMed
Steinmetz, J., Lavond, D., & Thomspon, R. (1989). Classical conditioning in rabbits using pontine nucleus stimulation as an unconditioned stimulus. Synapse, 3, 225–233.CrossRefGoogle ScholarPubMed
Steinmetz, J., & Sengelaub, D. (1992). Possible conditioned stimulus pathway for classical eyelid conditioning in rabbits. I. Anatomical evidence for direct projections from the pontine nuclei to the cerebellar interpositus nucleus. Behavioral and Neural Biology, 57, 103–115.CrossRefGoogle Scholar
Waelti, P., Dickinson, A., & Schultz, W. (2001). Dopamine responses comply with basic assumptions of formal learning theory. Nature, 412, 43–48.CrossRefGoogle ScholarPubMed
Walters, E.T. (1989). Transformation of siphon responses during conditioning of Aplysia suggest a model of primitive stimulus-response association. Proceedings of the National Academy of Sciences, USA, 86, 7616–7619.CrossRefGoogle Scholar
Weinberger, N. (1993). Learning-induced changes of auditory receptive fields. Current Opinion in Neurobiology, 3, 570–577.CrossRefGoogle ScholarPubMed
Weinberger, N. (1998). Phyisiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiology of Learning and Memory, 70, 226–251.CrossRefGoogle Scholar
Weiss, C. (1999). Hippocampal lesions prevent trace eyelid conditioning in the freely moving rat. Behavioral & Brain Research, 99, 123–132.CrossRefGoogle Scholar
Whalen, P., Shin, L., McInerney, S., Fischer, H., Wriht, C., & Rauch, S. (2001). A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion, 1, 70–83.CrossRefGoogle ScholarPubMed
Wiensky, A., Schafe, G., & LeDoux, J. (1999). Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. Journal of Neuroscience, 19, RC48, 1–5.Google Scholar
Wieskrantz, L., & Warrington, E. (1979). Conditioning in amnesic patients. Neuropsychologia, 17, 187–194.CrossRefGoogle Scholar
Zajonc, R. (1980). Feeling and thinking: Preferences need no inferences. American Psychologist, 35, 151–175.CrossRefGoogle Scholar