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The hippocampal system: Dissociating its functional components and recombining them in the service of declarative memory

Published online by Cambridge University Press:  04 February 2010

Howard Eichenbaum ,
Tim Otto  and
Neal J. Cohen
Howard Eichenbaum
Affiliation:
Department of Psychology, Boston University, Boston, MA 02215. hbe@bu.edu
Tim Otto
Affiliation:
Department of Psychology, Busch Campus, Rutgers University, New Brunswick, NJ 08903. totto@gandalf.rutg.edu
Neal J. Cohen
Affiliation:
Beckman Institute and Department of Psychology, University of Illinois at Urbana-Champaign, Urbana, IL 61801. njc@uiuc.edu
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Abstract

Continuing commentary raised several issues concerning our proposal that the hippocampus, parahippocampal region, and cortical association areas mediate different aspects of memory function. Recent relevant findings strengthen our argument that neocortical areas and the parahippocampal region maintain persistent encodings of specific single items and that the hippocampus mediates representations of the relations among these items. The reciprocally and closely interconnected structures that compose the hippocampal memory system work interactively to support flexible memory expression that is relevant to the natural behavior of animals and to conscious recollection in humans.

Type
Authors' Response
Information
Behavioral and Brain Sciences , Volume 19 , Issue 4 , December 1996 , pp. 772 - 776
Copyright
Copyright © Cambridge University Press 1996

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References

Aggleton, J. P. (1994) Commentary on Eichenbaum et al.'s “Two functional components of the hippocampal memory system.” Behavioral and Brain Sciences 17: 472–73. [DGM]CrossRefGoogle Scholar
Baars, B. J. (1988) A cognitive theory of conciousness. Cambridge University Press. [MM]Google Scholar
Bentin, S. (1994) Attention and memory. In: Attention and performance: 15. Conscious and nonconscious information processing, ed. Umiltà, C. & Moscovitch, M.. MIT/Bradford Press. [MM]Google Scholar
Bingman, V. P. (1994) Remembering spatial cognition as a hippocampal functional component. Behavioral and Brain Sciences 17:473–74. [WEC]CrossRefGoogle Scholar
Bunsey, M. & Eichenbaum, H. (1995) Selective damage to the hippocampal region blocks long-term retention of a natural and nonspatial stimulusstimulus association. Hippocampus 5:546–56. [HE]CrossRefGoogle Scholar
Bunsey, M. & Eichenbaum, H. (1996) Conservation of hippocampal memory function in rats and humans. Nature 37:255–57. [HE]CrossRefGoogle Scholar
Carroll, L. (1865–1872/1992) Through the looking-glass, unabridged ed. Wordsworth Editions. [WEC]Google Scholar
Clayton, N. S. & Krebs, J. R. (1995) Memory in food-storing birds: From behaviour to brain. Current Opinion in Neurobiology 5:149–54. [WEC]CrossRefGoogle Scholar
Cohen, N. J. & Eichenbaum, H. (1993) Memory, amnesia, and the hippocampal system. MIT Press. [HE]Google Scholar
Colombo, M. & Cross, C. G. (1994) Responses of inferior temporal cortex and hippocampal neurons during delayed matching to sample in monkeys (Macaca fascicularis). Behavioral Neuroscience 108:443–55. [MC]CrossRefGoogle ScholarPubMed
Cowey, A. & Stoerig, P. (1992) A structural model of autobiographical memory. In: The neuropsychology of consciousness, ed. Milner, A. D. & Rugg, M. D.. Academic Press. [MM]Google Scholar
Cowey, A. & Stoerig, P. (1994) Blindsight in monkeys. Nature 373:247–49. [MM]CrossRefGoogle Scholar
Crusio, W. E., Genthner-Grimm, G. & Schwegler, H. (1986) A quantitativegenetic quantitativegenetic analysis of hippocampal variation in the mouse. Journal of Neurogcnetics 3:203–14. [WEC]CrossRefGoogle ScholarPubMed
Crusio, W. E., Schwegler, H. & Brust, I. (1993) Covariations between hippocampal mossy fibres and working and reference memory in spatial and non-spatial radial maze tasks in mice. European Journal of Neuroscience 5:1413–20. [WEC]CrossRefGoogle ScholarPubMed
Eichenbaum, H. (1996) Is the rodent hippocampus just for ‘place’? Current Opinion in Neurobiology 6:187–75. [HE]CrossRefGoogle ScholarPubMed
Eichenbaum, H. & Bunsey, M. (1995) On the binding of associations in memory: Clues from studies on the role of the hippocampal region in paired associate learning. Current Directions in Psychological Science 4:19–23. [HE]CrossRefGoogle Scholar
Eichenbaum, H., Otto, T. & Cohen, N. J. (1994a) Two functional components of the hippocampal memory system. Behavioral and Brain Sciences 17:449–72. [MC, WEC, MM, DCM]CrossRefGoogle Scholar
Eichenbaum, H., Otto, T. & Cohen, N. J. (1994r) The hippocampal memory system and its functional components: Further explication and clarification [authors response to commentary]. Behavioral and Brain Science 17:500–17. [MC, WEC, DGM]CrossRefGoogle Scholar
Furedy, J. J. & Riley, D. M. (1987) Human Pavlovian autonomic: conditioning and the cognitive paradigm. In: Cognitive processes and Pavlovian conditioning in humans, ed. Davey, G.Wiley [FT]Google Scholar
Fuster, J. M. & Jervey, J. P. (1981) Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. Science 212:952–55. [MC]CrossRefGoogle ScholarPubMed
Fuster, J. M. & Jervey, J. P. (1982) Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task. Journal of Nettroscience 2:361–75. [MC]Google Scholar
Galef, B. G. (1990) An adaptionist perspective on social learning, social feeding, and social foraging in Norway rats. In: Contemporary issues in comparative psychology, ed. Dewsbury, D. A.. Sinauer. [HE]Google Scholar
Gallistel, C. R. (1980) The organization of action: A netv stjstfiesis. Erlbaum. [FT]Google Scholar
Gallup, G. G. Jr, (1985) Do minds exist in species other than our own? Neuroscience and Biobehavioral Reviews 9:631–41. [MM]CrossRefGoogle ScholarPubMed
Goldman-Rakic, P. S. (1988) Topography of cognition: Parallel distributed networks in primate association cortex. Annual Reviews of Neuroscience 11:137–56. [HE]CrossRefGoogle ScholarPubMed
Gray, J. A. (1982) Multiple book review of The neurobiology of anxiety: An enquiry into the functions of the septo-hippocampal system. Behavioral and Brain Sciences 5:469–534. [FT]CrossRefGoogle Scholar
Hampson, R. E. & Deadwyler, S. A. (1994) Hippocampal representations of DMS/DNMS in the rat. Behavioral and Brain Sciences 17:480–82. [MC]CrossRefGoogle Scholar
Hirsh, R. (1974) The hippocampus and contextual retrieval of information from memory: A theory. Behavioural Biology 12:421–44. [FT]CrossRefGoogle ScholarPubMed
Jarrard, L. E. (1993) Review: On the role sof the hippocampus in learning and memory in the nit. Behavioral ami Neural Biology 60:9–26. [HE]CrossRefGoogle Scholar
Jung, M. W., Wiener, S. I. & McNaughton, B. L. (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. Journal of Neuroscience 14:7347–56. [MC]CrossRefGoogle ScholarPubMed
Lipp, H. P., Schwegler, H., Crusio, W. E., Wolfer, D., Leisinger-Trigona, M.-C., Heiinrich, B. & Driscoll, P. (1989) Using genetically-defined rodent strains for the identification of hippocampal traits relevant for two-way avoidance learning: A non-invasive approach. Experientia 45:845–59. [WEC]CrossRefGoogle ScholarPubMed
McDonald, R. J. & White, N. M. (1995) Information acquired by the hippocampus interferes with acquisition of the amygdala-based conditonedcue preference in the rat. Hippocampus 5:189–97. [HE]CrossRefGoogle ScholarPubMed
McNaughton, N. (1994) The hippocampus: Relational processor or antiprocessor? Behavioral and Brain Sciences 17:487–88. [FT]CrossRefGoogle Scholar
Meunier, M., Bachevalier, J., Mishkin, M. & Murray, E. A. (1993) Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. Journal of Neuroscience 13:5418–32. [DGM]CrossRefGoogle ScholarPubMed
Morris, M., Camid, P., Rawlins, J. N. P. & O'Keefe, J. (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681–83. [DCM]CrossRefGoogle ScholarPubMed
Moscovitch, M. (1989) Confabulation and the frontal system: Strategic vs. associative retrieval in neuropsychological theories of memory. In: Varieties of memory and consciousness: Essays in honor of Endel Tulving, ed. Roediger, H. L. III & Crail, F. I. M.. Erlbaum. [MM]Google Scholar
Moscovitch, M. (1992a) Memory and working-with-inemory: A component process model based on modules and central systems. Journal of Cognitive Neuroscience 4:257–67. [MM]CrossRefGoogle ScholarPubMed
Moscovitch, M. (1992b) A neuropsychological model of memory and consciousness. In: The neuropsychology of memory, 2d ed., ed. Squire, L. R. & Butters, N.. Guilford Press. [MM]Google Scholar
Moscovitch, M. (1994a) Models of conscousness and memory. In: The cognitive neurosdences, ed. Gazzaniga, M. S.. MIT/Bradford Press. [MM]Google Scholar
Moscovitch, M. (1994b) Memory and working-with-memory: Evaluation of a component process model and comparisons with other models. In: Menumj systems 1994, ed. Schacter, D. & Tulving, E.. MIT/Bradford Press. [MM]Google Scholar
Moscovitch, M. (1995) Recovered conciousness: A hypothesis concerning modularity and episodic memory. Journal ofClincal and Experimental Neuropsychology 17:276–90. [MM]CrossRefGoogle Scholar
Moscovitch, M., Goshen-Gottstein, Y. & Vriezen, E. (1994) Memory without conscious recollection: A tutorial review from a neuropsychological perspective. In: Attention and performance: 15. Conscious and nonconscious information processing, ed.Umiltà, C. & Moscovitch, . MIT/Bradford Press. [MM]Google Scholar
Moscovitch, M. & Umiltà, C. (1990) Modularity and neuropsychology: Implications for the organization of attention and memdory in normal and hrain-damaged people. In: Modular processes in dementia, ed. Schwartz, M. E.. MIT Bradford Press. [MM]Google Scholar
Moscovitch, M. & Umiltà, C. (1991) Conscious and nonconscious aspects of memory: A neuropsychological framework of modules and central systems. In: Perspectives on cognitive neuroscience, ed. Lister, R. G. & Weingartner, H. J.. Oxford University Press. [MM]Google Scholar
Moscovitch, M., Vriezen, E. & Goshen-Gottstein, Y. (1993) Implicit tests of memory in patients with focal lesions and degenerative brain disorders. In: Handbook of neuropsychology, vol. 8, ed. Spinnler, H. & Boiler, F.. Elsevier. [MM]Google Scholar
Moser, E., Moser, M. B. & Andersen, P. (1993) Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. Journal of Neuroscience 13:3916–25. [MC]CrossRefGoogle ScholarPubMed
Mumby, D. C. & Pinel, J. P. J. (1994) Rhinal cortex lesions and object recognition in rats. Behavioral Neuroscience 108:11–18. [DGM]CrossRefGoogle ScholarPubMed
Mumby, D. C., Wood, E. R. & Pinel, J. P. J. (1992) Object recognition memory in rats is only mildly impaired by lesions of the hippocampus and amygdala. Psychobiology 20:18–27. [DGM]CrossRefGoogle Scholar
Nachson, I. (1995) On the modularity of face recognition: The riddle of domain specificity. Journal of Clinical and Experimental Neuropsychology 17:256–75. [MM]CrossRefGoogle ScholarPubMed
Nadel, L. (1991) The hippocampus and space revisited. Hippocampus 1:221–29. [WEC]CrossRefGoogle ScholarPubMed
Nadel, L. (1994) Hippocampus, space, and relations. Behavioral and Brain Sciences 17:490–91. [WEC]CrossRefGoogle Scholar
O'Boyle, V. J., Murray, E. A. & Mishkin, M. (1993) Effects of excitotoxic amygdalo-hippocampal lesions on visual recognition in rhesus monkeys. Society for Neuroscience Abstracts 19:438. [DGM]Google Scholar
O'Keefe, J. (1985) Is consciousness the gateway to the hippocampal cognitive map? A speculative essay on the neural basis of mind. In: Brain and mind, ed. Oakley, . Methuen. [MM]Google Scholar
O'Keefe, J. & Nadel, L. (1978) The hippocampus as a cognitive map. Clarendon. [MM]Google Scholar
O'Keefe, J. (1979) Précis of O'Keefe and Nadel's The hippocampus as a cognitive map. Behavioral and Brain Sciences 2:487–533. [WEC, FT]CrossRefGoogle Scholar
Olton, D. S., Becker, J. T. & Handelmann, G. E. (1979) Hippocampus, space and memory. Behavioral and Brain Sciences 2:313–65. [WEC, FT]CrossRefGoogle Scholar
Ono, T., Ramura, R. & Nakamura, K. (1991) The hippocampus and space: Are there “place neurons” in the monkey hippocampus? Hippocampus 1:253–57. [HE]CrossRefGoogle ScholarPubMed
Phillips, R. & LeDoux, J. E. (1995) Lesions of the fornix but not the entorhinal or perirhinal cortex interfere with contextual conditioning. Journal of Neuroscience 15:5308–15. [HE]CrossRefGoogle Scholar
Rawlins, J. N. P. (1985) Associations across time: The hippocampus as a temporary memory store. Behavioral and Brain Sciences 8:479–96. [FT]CrossRefGoogle Scholar
Riches, I. P., Wilson, F. A. W. & Brown, M. W. (1991) The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gynis and inferior temporal cortex of the primate. Journal of Neuroscience 11:1763–79. [MC]CrossRefGoogle ScholarPubMed
Roediger, H. L. III & McDermott, K. B. (1993) Implicit memory in normal human subjects. In: Handbook of neuropsychology, ed. Boller, F. & Grafman, J.. Elsevier. [MM]Google Scholar
Rolls, E. T. (1991) Functions of the primate hippocampus in spatial and nonspatial memory. Hippocampus 1:258–61. [HE]CrossRefGoogle ScholarPubMed
Rothblat, L. A. & Kramer, L. F. (1991) Object recognition memory in the rat: The role of the hippocampus. Behavioral Brain Research 42:25–32. [DGM]CrossRefGoogle ScholarPubMed
Rozin, P. (1976) The evaluation of intelligence and access to the cognitive unconscious. In: Progress in psychobiology and physiological psychology, ed. Sprague, J. & Epstein, A.. Academic Press. [MM]Google Scholar
Salzmann, E., Vidyasagar, T. R. & Creuzfeldt, O. D. (1993) Functional comparison of neuronal properties in the primate posterior hippocampus and parahippocampus (area TF/TH) during different behavioral paradigms involving memory and selective attention. Behavioral Brain Research 53:133–49. [MC]CrossRefGoogle ScholarPubMed
Schacter, D. (1989) Priming and multiple memory systems. In: Varieties of memories and consciousness: Essays in honor of Endel Tulving, ed. Roediger, H. L. III & Craik, F. I. M.. Erlbaum. [MM]Google Scholar
Schacter, D. L., McAndrews, M. P. & Moscovitch, M. (1988) Access to conciousness: Dissociations between implicit and explicit knowledge in neuropsycholgocial systems. In: Thimght without language, ed. Weiskrantz, L.. Oxford University Press. [MM]Google Scholar
Schoenbaum, G. & Eichenbaum, H. (1994) Information coding in the rodent prefrontal cortex: I. Single neuron activity in the orbitofrontal cortex compared with that in the periform cortex. Journal of Neurophysiology 74:733–50. [HE]CrossRefGoogle Scholar
Shettleworth, S. J. (1993) Varieties of learning and memory in animals. Journal of Experimental Psychology: Animal Behavior Processes 19:5–14. [WEC]Google ScholarPubMed
Squire, (1994) Commentary on Eichenbaum et al.'s “Two functional components of the hippocampal memory system.” Behavioral and Brain Sciences 17. [DGM]Google Scholar
Stuss, D. (1991) Self, awareness, and the frontal lobe: A neuropsychological perspective. In: The self: Interdisciplinary approaches, ed. Strauss, J. & Goethals, G. R.. Springer-Verlag. [MM]CrossRefGoogle Scholar
Sutherland, R. J., Whishaw, I. Q. & Kolb, B. (1983) A behavioral analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat. Behavioral Brain Research 7:133–53. [DGM]CrossRefGoogle ScholarPubMed
Suzuki, W. A. & Amaral, D. G. (1994a) Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents. Journal of Comparative Neurology 350:497–533. [MC]CrossRefGoogle ScholarPubMed
Suzuki, W. A. & Amaral, D. G. (1994b) Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. Journal of Neurosdence 14:1856–77. [MC]Google ScholarPubMed
Toates, F. (1994a) Hierarchies of control: Changing weightings of levels. In: Perceptual control theory, ed. Rodrigues, M. A. & Lee, M. H.. University of Wales, Aberystwyth. [FT]Google Scholar
Toates, F. (1994b) What is cognitive and what is not cognitive? In: From animals to animats 3, ed. Cliff, D., Husbands, P., Meyer, J. A. & Wilson, W. W.. MIT Press. [FT]Google Scholar
Toates, F. (1996) Cognition and evolution: An organization of action perspective. Beliavimiral Processes 35:239–50. [FT]CrossRefGoogle Scholar
Tulving, E. & Markowitsch, H. J. (1994) What do animal models of memory model? Behavioral and Brain Sciences 17: 498–99. [MM]CrossRefGoogle Scholar
van Daal, J. H. H. M., Jenks, B. G., Crusio, W. E., Lemmens, W. A. J. G. & van Abeelen, J. H. F. (1991) A genetic-correlational study of hippocampal neurochemical variation and variation in exploratory activities of mice. Behavioral Brain Research 43:6572. [WEC]CrossRefGoogle ScholarPubMed
Vidyasagar, T. R., Salzmann, E. & Creutzfeldt, O. D. (1991) Unit activity in the hippocampus and the parahippocampal temporobasal association cortex related to memory and complex behaviour in the awake monkey. Brain Research 544:269–78. [MC]CrossRefGoogle ScholarPubMed
Watanabe, T. & Niki, H. (1985) Hippocampal unit activity and delayed response in the monkey. Brain Research 325:241–54. [MC]CrossRefGoogle ScholarPubMed
Weiskrantz, L. (1986) Blindsight: A case study and implications. Oxford University Press. [MM]Google Scholar
Weiskrantz, L. (1988) Some contributions of neuropsychology of vision and memory to the problems of consciousness. In: Consciousness in contemporary science, ed. Marcel, A. J. & Bisiach, E.. Clarendon Press. [MM]Google Scholar
Wiig, K. A. & Bilkey, D. K. (1994a) Subtotal perirhinal cortex lesions increase exploratory behavior in the rat without producing deficits in the Morris water maze. Psychobiology 22:195–202. [DGM]CrossRefGoogle Scholar
Wiig, K. A. & Bilkey, D. K. (1994b) The effects of perirhinal cortical lesions on spatial reference memory in the rat. Behavioral Brain Research 63:101–9. [DGM]CrossRefGoogle ScholarPubMed
Wilson, F. A. W., Riches, I. P. & Brown, M. W. (1990) Hippocampus and medial temporal cortex: Neuronal activity related to behavioral responses during the performance of memory task by primates. Behavioral Brain Research 40:7–28. [MC]CrossRefGoogle ScholarPubMed
Witter, M. P. (1993) Organization of the entorhinal-hippocampal system: A review of current anatomical data. Hippocampus 3:33–44. [MC]CrossRefGoogle ScholarPubMed
Young, A. W. (1994) Conscious and nonconscious recognition of familiar faces. In: Attention and performance 15: Conscious and nonconscious information processing, ed. Umilta, C. & Moscovitch, M.. MIT/Bradford Press.Google Scholar
Young, B. J., Otto, T., Fox, G. D. & Eichenbaum, H. (1995) Neuronal activity in the parahippocampal region of rats performing a delayed non-match to sample task. Society for Neuroscience Abstracts 21:943. [HE]Google Scholar
Zola-Morgan, S. & Squire, L. R. (1993) Neuroanatomy of memory. Annual Review of Neuroscience 16:547–563. [MC]CrossRefGoogle ScholarPubMed