Conjunctive representations, the hippocampus, and contextual fear conditioning

Springer Science and Business Media LLC - Tập 1 - Trang 66-82 - 2001
Jerry W. Rudy1, Randall C. O’Reilly1
1Department of Psychology, University of Colorado, Boulder

Tóm tắt

The context in which events occur can be represented as both (1) a set of independent features, the feature representation view, and (2) a set of features bound into a unitary representation, the conjunction representation view. It is assumed that extrahippocampal (e.g., neocortical) areas provide a basis for feature representations, but the hippocampal formation makes an essential contribution to the automatic storage of conjunctive representations. We develop this dual-representation view and explore its implications for hippocampal contributions to contextual fear conditioning processes. To this end, we discuss how our framework can resolve some of the conflicts in the recent literature relating the hippocampus to contextual fear conditioning. We also present new data supporting the role of a key mechanism afforded by conjunctive representations—pattern completion (the ability of a subset of a memory pattern to activate the complete memory)—in contextual fear conditioning. As is implied by this mechanism, we report that fear can be conditioned to the memory representation of a context that is not actually present at the time of shock. Moreover, this result is predicted by our computational model of cortical and hippocampal function. We suggest that pattern completion demonstrated in animals and by our model provides a mechanistic bridge to human declarative memory.

Tài liệu tham khảo

Alvarado, M. C., & Rudy, J.W. (1995). A comparison of kainic acid + colchichine and ibotenic acid induced hippocampal formation damage on four configural tasks. Behavioral Neuroscience, 109, 1052–1062. Anagnostaras, S. G., Maren, S., & Fanselow, M. S. (1999). Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: Within-subjects examination. Journal of Neuroscience, 19, 1106–1114. Baily, D. J., Sun, W., Kim, J. J., & Helmstetter, F. J. (1997). Inhibition of RNA synthesis in the amygdala and hippocampus selectively blocks acquisition of Pavlovian fear conditioning. Society for Neuroscience Abstracts, 23, 1609. Bellgowan, P. S. F., & Helmstetter, F. J. (1995). Effects of muscimol applied to the dorsal hippocampus on the acquisition and expression of cued versus contextual fear conditioning. Society for Neuroscience Abstracts, 21, 1219. Bevins, R. A., & Ayres, J. J. B. (1995). One-trial context fear conditioning as a function of the interstimulus interval. Animal Learning & Behavior, 23, 400–410. Bevins, R.A., Rauhut, A. S., McPhee, J. E., & Ayres, J. J. B. (2000). One-trial context fear conditioning with immediate shock: The roles of transport and contextual cues. Animal Learning & Behavior, 28, 162–171. Blanchard, R. J., Fukunaga, K.K., & Blanchard, D.C. (1976). Environmental control of defensive reactions to footshock. Bulletin of the Psychonomic Society, 8, 129–130. Davidson, T. L., McKernan, M. G., & Jarrard, L. W. (1993). Hippocampal lesions do not impair negative patterning: A challenge to configural association theory. Behavioral Neuroscience, 107, 227–234. Fanselow, M. S. (1986). Associative vs topographical accounts of the immediate shock freezing deficit in rats: Implications for the response selection rules governing species specific defensive reactions. Learning & Motivation, 17, 16–39. Fanselow, M. S. (1990). Factors governing one-trial contextual conditioning. Animal Learning & Behavior, 18, 264–270. Fanselow, M. S. (1999). Learning theory and neuropsychology: Configuring their disparate elements in the hippocampus. Journal of Experimental Psychology: Animal Behavior Processes, 25, 275–283. Fanselow, M. S. (2000). Contextual fear, gestalt memories, and the hippocampus. Behavioural Brain Research, 110, 73–81. Fanselow, M. S., DeCola, J. P., & Young, S. (1993). Mechanisms responsible for reduced contextual conditioning with massed unsignaled unconditional stimuli. Journal of Experimental Psychology: Animal Behavior Processes, 19, 121–137. Fanselow, M. S., & Rudy, J.W. (1998). Convergence of experimental and developmental approaches to animal learning and memory processes. In T. Carew, R. Menzel, & C. Shatz (Eds.), Mechanistic relationships between development and learning: Beyond metaphor (pp. 15–28). Chichester, U.K.: Wiley. Frankland, P. W., Cestari, V., Filipkowski, R. K., McDonald, R., & Silva, A. (1998). The dorsal hippocampus is essential for context discrimination, but not for contextual conditioning. Behavioral Neuroscience, 112, 863–874. Gallagher, M., & Holland, P. C. (1992). Preserved configural learning and spatial learning impairment in rats with hippocampal damage. Hippocampus, 2, 81–88. Gewirtz, J. C., McNish, K. A., & Davis, M. (2000). Is the hippocampus necessary for contextual fear conditioning? Behavioral & Brain Sciences, 110, 83–95. Gluck, M.A., & Myers, C. (1993). Hippocampal mediation of stimulus representation: A computational theory. Hippocampus, 3, 491–518. Good, M., & Bannerman, D. (1997). Differential effects of ibotenic acid lesions of the hippocampus and blockade of N-methyl-D-aspartate receptor-dependent long-term potentiation on contextual processing in rats. Behavioral Neuroscience, 111, 1171–1183. Good, M., & Honey, R. C. (1991). Conditioning and contextual retrieval in hippocampal rats. Behavioral Neuroscience, 105, 499–509. Gulliksen, H., & Wolfle, D. A. (1938). A theory of learning and transfer. Psychometrika, 3, 127–149. Honey, R.C., Watt, A., & Good, M. (1998). Hippocampal lesions disrupt associative mismatch process. Journal of Neuroscience, 18, 2226–2232. Kamin, L. J. (1968). “Attention-like” processes in classical conditioning. In M. R. Jones (Ed.), Miami symposium on the prediction of behavior: Aversive stimulation (pp. 9-33). Miami: University of Miami Press. Kiernan, M. J., & Westbrook, R. F. (1993). Effects of exposure to a to-be-shocked environment upon the rat’s freezing response: Evidence for facilitation, latent inhibition, and perceptual learning. Quarterly Journal of Psychology, 46B, 271–288. Kim, J. J., & Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science, 256, 675–676. Kim, J. J., Rison, R. A., & Fanselow, M. S. (1993). Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behavioral Neuroscience, 107, 1093–1098. Logue, S. F., Paylor, R., & Wehner, J. M. (1997). Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task. Behavioral Neuroscience, 111, 104–113. Maren, S., Aharonov, G., & Fanselow, M. S. (1997). Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning. Behavioural Brain Research, 88, 261–274. Maren, S., & Fanselow, M. S. (1998). Electrolytic lesions of the fimbria /fornix, dorsal hippocampus, or entorhinal cortex produce anterograde deficits in contextual fear conditioning in rats. Neurobiology of Learning & Memory, 67, 142–149. Marr, D. (1971). Simple memory: A theory for archicortex. Philosophical Transactions of the Royal Society of London: Series B, 262, 23–81. McNaughton, B. L., & Morris, R.G.M. (1987). Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends in Neurosciences, 10, 408–415. McNaughton, B. L., & Nadel, L. (1990). Hebb-Marr networks and the neurobiological representations of action in space. In M. A. Gluck & D. E. Rumelhart (Eds.), Neuroscience and connectionist theory (pp. 1–63). Hillsdale, NJ: Erlbaum. Morris, R.G.M., & Frey, U. (1997). Hippocampal synaptic plasticity: Role in spatial learning or automatic recording of attended experience. Philosophical Transactions of the Royal Society of London: Series B, 352, 1489–1503. Nadel, L., & Willner, J. (1980). Context and conditioning: A place for space. Physiology & Behavior, 8, 218–228. Nadel, L., Willner, J., & Kurz, E.M. (1985). Cognitive maps and environmental context. In P. Balsam & A. Tomie (Eds.), Context and learning (pp. 385–406). Hillsdale, NJ: Erlbaum. O’Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Oxford University Press. O’Reilly, R. C., & McClelland, J. L. (1994). Hippocampal conjunctive encoding, storage, and retrieval: Avoiding a trade off. Hippocampus, 4, 661–682. O’Reilly, R. C., & Rudy, J.W. (in press). Conjunctive representations in learning and memory: Principles of cortical and hippocampal function. Psychological Review. Pearce, J.W. (1987). A model for stimulus generalization in Pavlovian conditioning. Psychological Review, 94, 61–73. Pearce, J.W. (1994). Similarity and discrimination: A selective review and connectionist model. Psychology Review, 101, 587–607. Phillips, R. G., & LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience, 106, 274–285. Phillips, R. G., & LeDoux, J. E. (1994). Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learning & Memory, 1, 34–45. Pugh, C. R., Kuwagama, K., Fleshner, M., Watkins, L. R. Maier, S. F., & Rudy, J.W. (1998). Selective effects of peripheral lipopolysaccharide administration on contextual and auditory cue fear conditioning. Brain, Behavior, & Immunity, 12, 212–229. Pugh, C. R., Nguyen, K. T., Gonyea, J. L., Fleshner M., Watkins, L. R., Maier, S. F., & Rudy, J.W. (1999). Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behavioural Brain Research, 106, 109–118. Pugh, C. R., Tremblay, D., Fleshner, M., & Rudy, J. W. (1997). A selective role for corticosterone in fear conditioning. Behavioral Neuroscience, 111, 503–511. Rescorla, R.A. (1972). “Configural” conditioning in discrete-trial bar pressing. Journal of Comparative & Physiological Psychology, 79, 307–317. Rescorla, R.A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variation in the effectiveness of reinforcement and nonreinforcement. In A. H. Black & W. F. Prokasy (Eds.), Classical conditioning: II. Current research and theory (pp. 64–100). New York: Appleton-Century-Crofts. Richmond, M. A., Yee, B. K., Pouzet, B., Veenman, L., Rawlins, J. N. P., Felden, J., & Bannerman, D.M. (1999). Dissociating context and space within the hippocampus: Effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behavioral Neuroscience, 113, 1189–1203. Rudy, J.W. (1996). Post-conditioning isolation disrupts contextual fear conditioning: An experimental analysis. Behavioral Neuroscience, 110, 238–246. Rudy, J.W., Kuwagama, K., & Pugh, C. R. (1999). Isolation reduces contextual but not auditory-cue fear conditioning: A role for endogenous opioids. Behavioral Neuroscience, 113, 316–323. Rudy, J.W., & Morledge, P. (1994). Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function. Behavioral Neuroscience, 108, 1–8. Rudy, J. W., & O’Reilly, R. C. (1999). Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus. Behavioral Neuroscience, 113, 867–880. Rudy, J.W., & Pugh, C. R. (1998). Time of conditioning selectively influences contextual fear conditioning: Further support for a multiplememory systems view of fear conditioning. Journal of Experimental Psychology: Animal Behavior Processes, 24, 316–324. Rudy, J. W., & Sutherland, R. J. (1992). Configural and elemental associations and the memory coherence problem. Journal of Cognitive Neuroscience, 4, 208–216. Rudy, J. W., & Sutherland, R. J. (1994). The memory coherence problem, configural associations and the hippocampal system. In D. Schacter & E. Tulving (Eds.), Memory systems (pp. 119–147). Cambridge, MA: MIT Press. Rudy, J.W., & Sutherland, R. J. (1995). Configural association theory and the hippocampal formation: An appraisal and reconfiguration. Hippocampus, 5, 375–389. Rudy, J. W., & Wagner, A. R. (1975). Stimulus selection in associative learning. In W. K. Estes (Ed.), Handbook of learning and cognitive processes (Vol. 2, pp. 269–304). Hillsdale, NJ: Erlbaum. Saavedra, M.A. (1975). Pavlovian compound conditioning in the rabbit. Learning & Motivation, 6, 314–326. Save, E., Poucet, B., Foreman, N., & Buhot, N. (1992). Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to the parietal cortex or hippocampal formation. Behavioral Neuroscience, 106, 447–456. Schmajuk, N., & DiCarlo, J. (1992). Stimulus configuration, classical conditioning and hippocampal function. Psychological Review, 99, 268–305. Selden, N. R. W., Everitt, B. J., Jarrard, L. E., & Robbins, T. W. (1991). Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience, 42, 335–350. Spence, K.W. (1936). The nature of discrimination learning in animals. Psychological Review, 43, 427–449. Spence, K. W. (1937). The differential response in animals to stimuli varying within a single dimension. Psychological Review, 44, 430–444. Squire, L. R. (1992). Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review, 99, 195–231. Sutherland, R. J., & Rudy, J.W. (1989). Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia. Psychobiology, 17, 129–144. Tyler, T. J., & DiScenna, P. (1986). The hippocampus memory indexing theory. Behavioral Neuroscience, 100, 147–152. Wagner, A. F., Logan, F. A., Haberlandt, K., & Price, T. (1968). Stimulus selection in animal discrimination learning. Journal of Experimental Psychology, 76, 171–181. Westbrook, R. F., Good, A. J., & Kiernan, M. J. (1994). Effects of the interval between exposure to a novel environment and the occurrence of shock on the freezing response of rats. Quarterly Journal of Experimental Psychology, 47B, 427–436. Whisaw, I. Q., & Tomie, J. A. (1991). Acquisition and retention by hippocampal rats of simple, conditional, and configural tasks using tactile and olfactory cues: Implications for hippocampal function. Behavioral Neuroscience, 105, 787–797. Whitlow, J. W., Jr., & Wagner, A. R. (1972). Negative patterning in classical conditioning: Summation of response tendencies to isolable and configural components. Psychonomic Science, 27, 299–301. Wickelgren, W. A. (1979). Chunking and consolidation: A theoretical synthesis of semantic networks, configuring, S-R versus cognitive learning, normal forgetting, the amnesic syndrome, and the hippocampal arousal system. Psychological Review, 86, 44–60. Woodbury, C. B. (1943). The learning of stimulus patterns by dogs. Journal of Comparative & Physiological Psychology, 35, 29–40.