Brain activity evidence for recognition without recollection after early hippocampal damage
Abstract
Amnesic patients with early and seemingly isolated hippocampal injury show relatively normal recognition memory scores. The cognitive profile of these patients raises the possibility that this recognition performance is maintained mainly by stimulus familiarity in the absence of recollection of contextual information. Here we report electrophysiological data on the status of recognition memory in one of the patients, Jon. Jon's recognition of studied words lacks the event-related potential (ERP) index of recollection, viz., an increase in the late positive component (500–700 ms), under conditions that elicit it reliably in normal subjects. On the other hand, a decrease of the ERP amplitude between 300 and 500 ms, also reliably found in normal subjects, is well preserved. This so-called N400 effect has been linked to stimulus familiarity in previous ERP studies of recognition memory. In Jon, this link is supported by the finding that his recognized and unrecognized studied words evoked topographically distinct ERP effects in the N400 time window. These data suggest that recollection is more dependent on the hippocampal formation than is familiarity, consistent with the view that the hippocampal formation plays a special role in episodic memory, for which recollection is so critical.
Acknowledgments
We thank Jon and his parents for making this study possible. We also thank Ken Paller, Michael Rugg, and Thomas Münte for helpful comments on earlier versions of the manuscript and Hans-Jürgen Warmbold for technical support. This study was supported by grants from the Deutsche Forschungsgemeinschaft (DFG/SFB 426, TP C7).
References
1
F Vargha-Khadem, D G Gadian, K E Watkins, A Connelly, W Van Paesschen, M Mishkin Science 277, 376–380 (1997).
2
J P Aggleton, C Shaw Neuropsychologia 34, 51–62 (1996).
3
N L Rempel-Clower, S M Zola, L R Squire, D G Amaral J Neurosci 16, 5233–5255 (1996).
4
E A Murray, M Mishkin J Neurosci 18, 6568–6582 (1998).
5
L R Squire, S M Zola Hippocampus 8, 205–211 (1998).
6
M Mishkin, F Vargha-Khadem, D G Gadian Hippocampus 8, 212–216 (1998).
7
E Tulving, H J Markowitsch Hippocampus 8, 198–204 (1998).
8
Baddeley, A., Vargha-Khadem, F. & Mishkin, M., J. Cogn. Neurosci., in press.
9
E Tulving Can Psychol 26, 1–12 (1985).
10
L L Jacoby J Mem Lang 30, 513–541 (1991).
11
A P Yonelinas, N E Kroll, I Dobbins, M Lazzara, R T Knight Neuropsychology 12, 323–339 (1998).
12
J M Gardiner, R I Java, A Richardson-Klavehn Can J Exp Psychol 50, 114–122 (1996).
13
B J Knowlton, L R Squire J Exp Psychol Learn Mem Cogn 21, 699–710 (1995).
14
J R Manns, L R Squire Hippocampus 9, 495–499 (1999).
15
S C Brown, F I M Craik The Oxford Handbook of Memory, eds E Tulving, F I M Craik (Oxford Univ. Press, Oxford), pp. 93–107 (2000).
16
K A Paller, M Kutas J Cogn Neurosci 4, 375–391 (1992).
17
K A Paller, M Kutas, H K McIsaac Psychol Sci 6, 107–111 (1995).
18
M D Rugg, R E Mark, P Walla, A M Schloerscheidt, C S Birch, K Allan Nature (London) 392, 595–598 (1998).
19
E Düzel, A P Yonelinas, G R Mangun, H J Heinze, E Tulving Proc Natl Acad Sci USA 94, 5973–5978 (1997).
20
T Curran Neuropsychologia 37, 771–785 (1999).
21
T Curran Mem Cognit 28, 923–938 (2000).
22
K A Paller, M Kutas, H K McIsaac Conscious Cogn 7, 54–66 (1998).
23
E L Wilding, M D Rugg Brain 119, 889–905 (1996).
24
E Wilding Int J Psychophysiol 35, 81–87 (2000).
25
A P Yonelinas, L L Jacoby Conscious Cognit 5, 131–141 (1996).
26
D Nessler, A Mecklinger, T B Penney Brain Res Cogn Brain Res 10, 283–301 (2001).
27
M Kutas, C K Van Petten Handbook of Psycholinguistics, ed M A Gernsbacher (Academic, San Diego), pp. 83–143 (1994).
28
J M Olichney, C Van Petten, K A Paller, D P Salmon, V J Iragui, M Kutas Brain 123, 1948–1963 (2000).
29
R L Baayen, R Piepenbrock, H von Rijn The CELEX Lexical Database (Linguistic Database Consortium, Univ. of Pennsylvania, Philadelphia, 1993).
30
E Düzel, R Cabeza, T W Picton, A P Yonelinas, H Scheich, H J Heinze, E Tulving Proc Natl Acad Sci USA 96, 1794–1799 (1999).
31
B J Winer Statistical Principles in Experimental Design (McGraw-Hill, New York, 1971).
32
G McCarthy, C C Wood Electroencephalogr Clin Neurophysiol 62, 203–208 (1985).
33
M D Rugg Mem Cognit 18, 367–379 (1990).
34
T F Münte, P U Urbach, E Düzel, M Kutas Handbook of Neuropsychology, ed M Kutas (Elsevier, Amsterdam, in press. (2001).
35
W A Suzuki Neuron 24, 295–298 (1999).
36
C E Stark, L R Squire J Neurosci 20, 7776–7781 (2000).
37
L L Eldridge, B J Knowlton, C S Furmanski, S Y Bookheimer, S A Engel Nat Neurosci 3, 1149–1152 (2000).
38
M A Wheeler, D T Stuss, E Tulving Psychol Bull 121, 331–354 (1997).
39
E A Murray, T J Bussey Trends Cogn Sci 3, 142–151 (1999).
Information & Authors
Information
Published in
Classifications
Copyright
Copyright © 2001, The National Academy of Sciences.
Submission history
Accepted: April 26, 2001
Published online: July 3, 2001
Published in issue: July 3, 2001
Keywords
Acknowledgments
We thank Jon and his parents for making this study possible. We also thank Ken Paller, Michael Rugg, and Thomas Münte for helpful comments on earlier versions of the manuscript and Hans-Jürgen Warmbold for technical support. This study was supported by grants from the Deutsche Forschungsgemeinschaft (DFG/SFB 426, TP C7).
Authors
Metrics & Citations
Metrics
Altmetrics
Citations
Cite this article
Brain activity evidence for recognition without recollection after early hippocampal damage, Proc. Natl. Acad. Sci. U.S.A.
98 (14) 8101-8106,
https://doi.org/10.1073/pnas.131205798
(2001).
Copied!
Copying failed.
Export the article citation data by selecting a format from the list below and clicking Export.
Cited by
Loading...
View Options
View options
PDF format
Download this article as a PDF file
DOWNLOAD PDFLogin options
Check if you have access through your login credentials or your institution to get full access on this article.
Personal login Institutional LoginRecommend to a librarian
Recommend PNAS to a LibrarianPurchase options
Purchase this article to access the full text.