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Recollection-like memory retrieval in rats is dependent on the hippocampus


Recognition memory may be supported by two independent types of retrieval, conscious recollection of a specific experience and a sense of familiarity gained from previous exposure to particular stimuli1,2. In humans, signal detection techniques have been used to distinguish recollection and familiarity, respectively, in asymmetrical and curvilinear components of their receiver operating characteristic (ROC) curves, standard curves that represent item recognition across different levels of confidence or bias. To determine whether animals also employ multiple processes in recognition memory and to explore the anatomical basis of this distinction, we adapted these techniques to examine odour recognition memory in rats. Their ROC curve had asymmetrical and curvilinear components, indicating the existence of both recollection and familiarity in rats. Furthermore, following selective damage to the hippocampus the ROC curve became entirely symmetrical and remained curvilinear, supporting the view that the hippocampus specifically mediates the capacity for recollection.

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Figure 1: ROCs for recognition performance in humans and rats.
Figure 2: Lesions of the hippocampus reconstructed on coronal sections of the rat brain.
Figure 3: Odour recognition task.


  1. Yonelinas, A. P. The nature of recollection and familiarity: a review of 30 years of research. J. Mem. Lang. 46, 441–517 (2002)

    Article  Google Scholar 

  2. Sherman, S. J., Atri, A., Hasselmo, M. E., Stern, C. E. & Howard, M. W. Scopolamine impairs human recognition memory: data and modeling. Behav. Neurosci. 117, 526–539 (2003)

    Article  CAS  Google Scholar 

  3. Yonelinas, A. P. et al. Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nature Neurosci. 5, 1236–1241 (2002)

    Article  CAS  Google Scholar 

  4. Davachi, L. & Wagner, A. D. Hippocampal contributions to episodic encoding: insights from relational and item-based learning. J. Neurophysiol. 88, 982–990 (2002)

    Article  Google Scholar 

  5. Ranganath, C., Johnson, M. K. & D'Esposito, M. Prefrontal activity associated with working memory and episodic long-term memory. Neuropsychologia 41, 378–389 (2003)

    Article  Google Scholar 

  6. Manns, J. R., Hopkins, R. O., Reed, J. M., Kitchener, E. G. & Squire, L. R. Recognition memory and the human hippocampus. Neuron 37, 171–180 (2003)

    Article  CAS  Google Scholar 

  7. Stark, C. E. & Squire, L. R. Functional magnetic resonance imaging (fMRI) activity in the hippocampal region during recognition memory. J. Neurosci. 20, 7776–7781 (2000)

    Article  CAS  Google Scholar 

  8. Eichenbaum, H., Otto, T. & Cohen, N. J. Two functional components of the hippocampal memory system. Behav. Brain Sci. 17, 449–472, 472–518 (1994)

    Article  Google Scholar 

  9. Brown, M. W. & Aggleton, J. P. Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nature Rev. Neurosci. 2, 51–61 (2001)

    Article  CAS  Google Scholar 

  10. Beason-Held, L. L., Rosene, D. L., Killiany, R. J. & Moss, M. B. Hippocampal formation lesions produce memory impairment in the rhesus monkey. Hippocampus 9, 562–574 (1999)

    Article  CAS  Google Scholar 

  11. Zola, S. M. et al. Impaired recognition memory in monkeys after damage limited to the hippocampal region. J. Neurosci. 20, 451–463 (2000)

    Article  CAS  Google Scholar 

  12. Nemanic, S., Alvarado, M. C. & Bachevalier, J. The hippocampal/parahippocampal regions and recognition memory: insights from visual paired comparison versus object-delayed nonmatching in monkeys. J. Neurosci. 24, 2013–2026 (2004)

    Article  CAS  Google Scholar 

  13. Mumby, D. G. Perspectives on object recognition memory following hippocampal damage: lessons from studies on rats. Behav. Brain Res. 127, 159–181 (2001)

    Article  CAS  Google Scholar 

  14. Dudchenko, P. A., Wood, E. R. & Eichenbaum, H. Neurotoxic hippocampal lesions have no effect on odor span and little effect on odor recognition memory but produce significant impairments on spatial span, recognition, and alternation. J. Neurosci. 20, 2964–2977 (2000)

    Article  CAS  Google Scholar 

  15. Steckler, T., Drinkenburg, W. H., Sahgal, A. & Aggleton, J. P. Recognition memory in rats II. Neuroanatomical substrates. Prog. Neurobiol. 54, 313–332 (1998)

    Article  CAS  Google Scholar 

  16. Mumby, D. G., Gaskin, S., Glenn, M. J., Schramek, T. E. & Lehmann, H. Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn. Mem. 9, 49–57 (2002)

    Article  Google Scholar 

  17. Eacott, M. J. & Norman, G. Integrated memory for object, place, and context in rats: a possible model of episodic-like memory? J. Neurosci. 24, 1948–1953 (2004)

    Article  CAS  Google Scholar 

  18. Macmillan, N. A. & Creelman, C. D. Detection Theory: A User's Guide (Cambridge Univ. Press, New York, 1991)

    Google Scholar 

  19. Yonelinas, A. P., Kroll, N. E., Dobbins, I., Lazzara, M. & Knight, R. T. Recollection and familiarity deficits in amnesia: convergence of remember-know, process dissociation, and receiver operating characteristic data. Neuropsychology 12, 323–339 (1998)

    Article  CAS  Google Scholar 

  20. Yonelinas, A. P. Components of episodic memory: the contribution of recollection and familiarity. Phil. Trans. R. Soc. Lond. B 356, 1363–1374 (2001)

    Article  CAS  Google Scholar 

  21. Hockley, W. E. Item versus associative information: further comparison of forgetting rates. J. Exp. Psychol. Learn. Mem. Cogn. 18, 1321–1330 (1992)

    Article  Google Scholar 

  22. Yonelinas, A. P. & Levy, B. J. Dissociating familiarity from recollection in human recognition memory: different rates of forgetting over short retention intervals. Psychon. Bull. Rev. 9, 575–582 (2002)

    Article  Google Scholar 

  23. Murray, E. A. & Mishkin, M. Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. J. Neurosci. 18, 6568–6582 (1998)

    Article  CAS  Google Scholar 

  24. Tulving, E. Episodic memory: from mind to brain. Annu. Rev. Psychol. 53, 1–25 (2002)

    Article  ADS  Google Scholar 

  25. Bunsey, M. & Eichenbaum, H. Conservation of hippocampal memory function in rats and humans. Nature 379, 255–257 (1996)

    Article  ADS  CAS  Google Scholar 

  26. Day, M., Langston, R. & Morris, R. G. Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 424, 205–209 (2003)

    Article  ADS  CAS  Google Scholar 

  27. Wood, E. R., Dudchenko, P. A., Robitsek, R. J. & Eichenbaum, H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623–633 (2000)

    Article  CAS  Google Scholar 

  28. Kesner, R. P. in Neurobiology of Comparative Cognition (eds Kesner, R. P. & Olton, D. S.) 179–203 (Lawrence Erlbaum, New Jersey, 1990)

    Google Scholar 

  29. Clark, R. E. & Squire, L. R. Classical conditioning and brain systems: the role of awareness. Science 280, 77–81 (1998)

    Article  ADS  CAS  Google Scholar 

  30. Fortin, N. J., Agster, K. L. & Eichenbaum, H. Critical role of the hippocampus in memory for sequences of events. Nature Neurosci. 5, 458–462 (2002)

    Article  CAS  Google Scholar 

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We thank J. O'Connell, A. Milewski, L. Giocomo, J. Estes, D. Tosa, R. Kline, J. Davidson and B. Goldberg for help with behavioural testing. We also thank R. Komorowski for histological work, A. Yonelinas for providing the least-squares curve-fitting algorithm and J. Manns for comments on an earlier version of this manuscript. Supported by NIA and NIMH.

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Correspondence to Howard Eichenbaum.

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Supplementary information

Supplementary Notes

Presents further notes on analyses of raw and z-tranformed data. (DOC 28 kb)

Supplementary Figure 1

Slopes of linear fits for preoperative, control, and hippocampal group data in z-ROC space. (JPG 44 kb)

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Fortin, N., Wright, S. & Eichenbaum, H. Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature 431, 188–191 (2004).

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