Autobiographical Memory Retrieval and Hippocampal Activation as a Function of Repetition and the Passage of Time

Nadel, Lynn; Campbell, Jenna; Ryan, Lee

doi:https://doi.org/10.1155/2007/90472

Neural Plasticity

On this page

Abstract References Copyright Related Articles

Research Article | Open Access

Volume 2007 | Article ID 090472 | https://doi.org/10.1155/2007/90472

Autobiographical Memory Retrieval and Hippocampal Activation as a Function of Repetition and the Passage of Time

Lynn Nadel,¹Jenna Campbell,¹and Lee Ryan¹

Academic Editor: Leonardo G. Cohen

Received17 Apr 2007

Revised04 Sept 2007

Accepted08 Oct 2007

Published25 Dec 2007

Abstract

Multiple trace theory (MTT) predicts that hippocampal memory traces expand and strengthen as a function of repeated memory retrievals. We tested this hypothesis utilizing fMRI, comparing the effect of memory retrieval versus the mere passage of time on hippocampal activation. While undergoing fMRI scanning, participants retrieved remote autobiographical memories that had been previously retrieved either one month earlier, two days earlier, or multiple times during the preceding month. Behavioral analyses revealed that the number and consistency of memory details retrieved increased with multiple retrievals but not with the passage of time. While all three retrieval conditions activated a similar set of brain regions normally associated with autobiographical memory retrieval including medial temporal lobe structures, hippocampal activation did not change as a function of either multiple retrievals or the passage of time. However, activation in other brain regions, including the precuneus, lateral prefrontal cortex, parietal cortex, lateral temporal lobe, and perirhinal cortex increased after multiple retrievals, but was not influenced by the passage of time. These results have important implications for existing theories of long-term memory consolidation.

References

D. Marr, “A theory for cerebral neocortex,” Proceedings of the Royal Society of London, Series B., vol. 176, no. 43, pp. 161–234, 1970.
View at: Google Scholar
D. Marr, “Simple memory: a theory for archicortex,” Philosophical transactions of the Royal Society of London, Series B, vol. 262, no. 841, pp. 23–81, 1971.
View at: Publisher Site | Google Scholar
L. R. Squire, N. J. Cohen, and L. Nadel, “The medial temporal region and memory consolidation: a new hypothesis,” in Memory Consolidation: Psychobiology of Cognition, H. Weingartner and E. Parker, Eds., pp. 185–210, Hillsdale, NJ, USA, 1984.
View at: Google Scholar
F. C. Bartlett, Remembering: A Study in Experimental and Social Psychology, Cambridge University Press, Cambridge, UK, 1932.
L. R. Squire and S. Zola-Morgan, “The medial temporal lobe memory system,” Science, vol. 253, no. 5026, pp. 1380–1386, 1991.
View at: Publisher Site | Google Scholar
L. R. Squire, “Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans,” Psychological Review, vol. 99, no. 2, pp. 195–231, 1992.
View at: Publisher Site | Google Scholar
L. R. Squire and P. Alvarez, “Retrograde amnesia and memory consolidation: a neurobiological perspective,” Current Opinion in Neurobiology, vol. 5, no. 2, pp. 169–177, 1995.
View at: Publisher Site | Google Scholar
P. Alvarez and L. R. Squire, “Memory consolidation and the medial temporal lobe: a simple network model,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 15, pp. 7041–7045, 1994.
View at: Publisher Site | Google Scholar
E. Teng and L. R. Squire, “Memory for places learned long ago is intact after hippocampal damage,” Nature, vol. 400, no. 6745, pp. 675–677, 1999.
View at: Publisher Site | Google Scholar
K. Niki and J. Luo, “An fMRI study on the time-limited role of the medial temporal lobe in long-term topographical autobiographic memory,” Journal of Cognitive Neuroscience, vol. 14, no. 3, pp. 500–507, 2002.
View at: Publisher Site | Google Scholar
M. Piefke, P. H. Weiss, K. Zilles, H. J. Markowitsch, and G. R. Fink, “Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory,” Brain, vol. 126, no. 3, pp. 650–668, 2003.
View at: Publisher Site | Google Scholar
K. Deisseroth, S. Singla, H. Toda, M. Monje, T. D. Palmer, and R. C. Malenka, “Excitation-neurogenesis coupling in adult neural stem/progenitor cells,” Neuron, vol. 42, no. 4, pp. 535–552, 2004.
View at: Publisher Site | Google Scholar
L. Nadel and M. Moscovitch, “Memory consolidation, retrograde amnesia and the hippocampal complex,” Current Opinion in Neurobiology, vol. 7, no. 2, pp. 217–227, 1997.
View at: Publisher Site | Google Scholar
E. A. Maguire, R. N. A. Henson, C. J. Mummery, and C. D. Frith, “Activity in prefrontal cortex, not hippocampus, varies parametrically with the increasing remoteness of memories,” NeuroReport, vol. 12, no. 3, pp. 441–444, 2001.
View at: Publisher Site | Google Scholar
R. Lee, L. Nadel, and K. Keil, “Hippocampal complex and retrieval of recent and very remote autobiographical memories: evidence from functional magnetic resonance imaging in neurologically intact people,” Hippocampus, vol. 11, no. 6, pp. 707–714, 2001.
View at: Publisher Site | Google Scholar
A. Gilboa, G. Winocur, C. L. Grady, S. J. Hevenor, and M. Moscovitch, “Remembering our past: functional neuroanatomy of recollection of recent and very remote personal events,” Cerebral Cortex, vol. 14, no. 11, pp. 1214–1225, 2004.
View at: Publisher Site | Google Scholar
S. Steinvorth, B. Levine, and S. Corkin, “Medial temporal lobe structures are needed to re-experience remote autobiographical memories: evidence from H.M. and W.R.,” Neuropsychologia, vol. 43, no. 4, pp. 479–496, 2005.
View at: Publisher Site | Google Scholar
P. V. Rekkas and R. T. Constable, “Evidence that autobiographical memory retrieval does not become independent of the hippocampus: an fMRI study contrasting very recent with remote events,” Journal of Cognitive Neuroscience, vol. 17, no. 12, pp. 1950–1961, 2005.
View at: Publisher Site | Google Scholar
M. Moscovitch, R. S. Rosenbaum, A. Gilboa et al., “Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory,” Journal of Anatomy, vol. 207, no. 1, pp. 35–66, 2005.
View at: Publisher Site | Google Scholar
B. Levine, E. Svoboda, J. F. Hay, G. Winocur, and M. Moscovitch, “Aging and autobiographical memory: dissociating episodic from semantic retrieval,” Psychology and Aging, vol. 17, no. 4, pp. 677–689, 2002.
View at: Publisher Site | Google Scholar
K. I. Forster and J. C. Forster, “DMDX: a windows display program with millisecond accuracy,” Behavior Research Methods, Instruments, and Computers, vol. 35, no. 1, pp. 116–124, 2003.
View at: Google Scholar
G. H. Glover and C. S. Law, “Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts,” Magnetic Resonance in Medicine, vol. 46, no. 3, pp. 515–522, 2001.
View at: Publisher Site | Google Scholar
R. W. Cox, “AFNI: software for analysis and visualization of functional magnetic resonance neuroimages,” Computers and Biomedical Research, vol. 29, no. 3, pp. 162–173, 1996.
View at: Publisher Site | Google Scholar
L. Ryan and D. Schnyer, “Regional specificity of format-specific priming effects in mirror word reading using functional magnetic resonance imaging,” Cerebral Cortex, vol. 17, no. 4, pp. 982–992, 2007.
View at: Publisher Site | Google Scholar
C.-Y. Lin and L. Ryan, “Repetition priming without identification of the primes: evidence for a component process view of priming,” NeuroImage, vol. 38, no. 3, pp. 589–603, 2007.
View at: Publisher Site | Google Scholar
S. Steinvorth, S. Corkin, and E. Halgren, “Ecphory of autobiographical memories: an fMRI study of recent and remote memory retrieval,” NeuroImage, vol. 30, no. 1, pp. 285–298, 2006.
View at: Publisher Site | Google Scholar
D. R. Addis, A. T. Wong, and D. L. Schacter, “Remembering the past and imagining the future: common and distinct neural substrates during event construction and elaboration,” Neuropsychologia, vol. 45, no. 7, pp. 1363–1377, 2007.
View at: Publisher Site | Google Scholar
S. M. Daselaar, H. J. Rice, D. L. Greenberg, R. Cabeza, K. S. LaBar, and D. C. Rubin, “The spatiotemporal dynamics of autobiographical memory: neural correlates of recall, emotional intensity, and reliving,” Cerebral Cortex, 2007.
View at: Publisher Site | Google Scholar
M. Brett, J. L. Anton, R. Valabregue, and J. B. Poline, “Region of interest analysis using an SPM toolbox,” in Proceedings of the 8th International Conference on Functional Mapping of the Human Brain, vol. 16, pp. 2–6, Sendai, Japan, June 2002.
View at: Google Scholar
D. G. Payne, “Hypermnesia and reminiscence in recall: a historical and empirical review,” Psychological Bulletin, vol. 101, no. 1, pp. 5–27, 1987.
View at: Publisher Site | Google Scholar
M. H. Erdelyi and J. Becker, “Hypermnesia for pictures: incremental memory for pictures but not words in multiple recall trials,” Cognitive Psychology, vol. 6, no. 1, pp. 159–171, 1974.
View at: Publisher Site | Google Scholar
A. J. Barnier, L. Hung, and M. A. Conway, “Retrieval-induced forgetting of emotional and unemotional autobiographical memories,” Cognition and Emotion, vol. 18, no. 4, pp. 457–477, 2004.
View at: Publisher Site | Google Scholar
S. Bluck, L. J. Levine, and T. M. Laulhere, “Autobiographical remembering and hypermnesia: a comparison of older and younger adults,” Psychology and Aging, vol. 14, no. 4, pp. 671–682, 1999.
View at: Publisher Site | Google Scholar
U. Neisser, “John Dean's memory: a case study,” Cognition, vol. 9, no. 1, pp. 1–22, 1981.
View at: Publisher Site | Google Scholar
E. J. Marsh, “Retelling is not the same as recalling: implications for memory,” Current Directions in Psychological Science, vol. 16, no. 1, pp. 16–20, 2007.
View at: Publisher Site | Google Scholar
K. Nader, G. E. Schafe, and J. E. LeDoux, “Fear memories require protein synthesis in the amygdale for reconsolidation after retrieval,” Nature, vol. 406, pp. 722–726, 2000.
View at: Publisher Site | Google Scholar
J. Przybyslawski and S. J. Sara, “Reconsolidation of memory after its reactivation,” Behavioural Brain Research, vol. 84, no. 1-2, pp. 241–246, 1997.
View at: Publisher Site | Google Scholar
D. J. Lewis, N. J. Bregman, and J. J. Mahan Jr., “Cue-dependent amnesia in rats,” Journal of Comparative and Physiological Psychology, vol. 81, no. 2, pp. 243–247, 1972.
View at: Publisher Site | Google Scholar
S. J. Sara, P. Roullet, and J. Przybyslawski, “Consolidation of memory for odor-rewarded association: $β$ -adrenergic receptor involvement in the late phase,” Learning and Memory, vol. 6, pp. 88–95, 1999.
View at: Google Scholar
E. M. Robertson, A. Pascual-Leone, and R. C. Miall, “Current conceptions of procedural consolidation,” Nature Reviews Neuroscience, vol. 5, pp. 576–582, 2004.
View at: Publisher Site | Google Scholar
E. M. Robertson and D. A. Cohen, “Understanding consolidation through the architecture of memories,” Neuroscientist, vol. 12, no. 3, pp. 261–271, 2006.
View at: Publisher Site | Google Scholar
D. R. Addis, A. R. McIntosh, M. Moscovitch, A. P. Crawley, and M. P. McAndrews, “Characterizing spatial and temporal features of autobiographical memory retrieval networks: a partial least squares approach,” NeuroImage, vol. 23, no. 4, pp. 1460–1471, 2004.
View at: Publisher Site | Google Scholar
L. Cahill and J. L. McGaugh, “Mechanisms of emotional arousal and lasting declarative memory,” Trends in Neurosciences, vol. 21, no. 7, pp. 294–299, 1998.
View at: Publisher Site | Google Scholar
M. A. Wilson and B. L. McNaughton, “Reactivation of hippocampal ensemble memories during sleep,” Science, vol. 265, no. 5172, pp. 676–679, 1994.
View at: Publisher Site | Google Scholar
G. R. Sutherland and B. McNaughton, “Memory trace reactivation in hippocampal and neocortical neuronal ensembles,” Current Opinion in Neurobiology, vol. 10, no. 2, pp. 180–186, 2000.
View at: Publisher Site | Google Scholar
R. Stickgold and M. P. Walker, “Memory consolidation and reconsolidation: what is the role of sleep?” Trends in Neurosciences, vol. 28, no. 8, pp. 408–415, 2005.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2007 Lynn Nadel et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation Order printed copies

Views

1041

Downloads

1939

Citations