The human hippocampus contributes to both the recollection and familiarity components of recognition memory

Edited by Larry R. Squire, Veterans Affairs San Diego Healthcare System, San Diego, CA, and approved September 30, 2015 (received for review July 31, 2015)
November 2, 2015
112 (46) 14378-14383

Significance

Recognition memory is thought to be composed of recollection, accompanied by vivid details, and familiarity or a general sense of knowing. A fundamental and long-standing question remains: Which of these processes does the hippocampus support? We measured high-frequency activity (HFA), a spatiotemporally precise signal of neural activation, in subjects undergoing direct brain recordings and found that hippocampal HFA dissociated based on both the stimulus evidence presented and the response choice. Hippocampal HFA predicted overall memory performance as well as individual differences in both recollection and familiarity estimates. Our findings reject the hypothesis that the hippocampus exclusively supports the recollection component of recognition memory and, instead, indicate that this structure is functionally relevant to both processes thought to support recognition.

Abstract

Despite a substantial body of work comprising theoretical modeling, the effects of medial temporal lobe lesions, and electrophysiological signal analysis, the role of the hippocampus in recognition memory remains controversial. In particular, it is not known whether the hippocampus exclusively supports recollection or both recollection and familiarity—the two latent cognitive processes theorized to underlie recognition memory. We studied recognition memory in a large group of patients undergoing intracranial electroencephalographic (iEEG) monitoring for epilepsy. By measuring high-frequency activity (HFA)—a signal associated with precise spatiotemporal properties—we show that hippocampal activity during recognition predicted recognition memory performance and tracked both recollection and familiarity. Through the lens of dual-process models, these results indicate that the hippocampus supports both the recollection and familiarity processes.

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Acknowledgments

We thank Dale H. Wyeth and Edmund Wyeth for technical assistance; Erin N. Beck for data collection; and Ashwin Ramayya, Nicole Long, M. Karl Healey, and Youssef Ezzyat for helpful discussion and input. We also thank members of the clinical teams where the data were collected: Ashwini Sharan, James Evans, Michael Sperling, Timothy Lucas, and Gordon Baltuch. We are indebted to the patients who have selflessly volunteered their time to participate in our study. This work was supported by National Institutes of Health Grant MH055687.

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 112 | No. 46
November 17, 2015
PubMed: 26578784

Classifications

Submission history

Published online: November 2, 2015
Published in issue: November 17, 2015

Keywords

  1. hippocampus
  2. recognition memory
  3. recollection
  4. familiarity
  5. high-frequency activity

Acknowledgments

We thank Dale H. Wyeth and Edmund Wyeth for technical assistance; Erin N. Beck for data collection; and Ashwin Ramayya, Nicole Long, M. Karl Healey, and Youssef Ezzyat for helpful discussion and input. We also thank members of the clinical teams where the data were collected: Ashwini Sharan, James Evans, Michael Sperling, Timothy Lucas, and Gordon Baltuch. We are indebted to the patients who have selflessly volunteered their time to participate in our study. This work was supported by National Institutes of Health Grant MH055687.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Maxwell B. Merkow1 [email protected]
Department of Neurosurgery, University of Pennsylvania, Philadelphia, PA 19104;
John F. Burke
Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104;
Michael J. Kahana
Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: M.B.M. and M.J.K. designed research; M.B.M. performed research; M.B.M. and J.F.B. analyzed data; and M.B.M., J.F.B., and M.J.K. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    The human hippocampus contributes to both the recollection and familiarity components of recognition memory
    Proceedings of the National Academy of Sciences
    • Vol. 112
    • No. 46
    • pp. 14103-E6410

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