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The Journal of Neuroscience, October 18, 2006, 26(42):10727-10742; doi:10.1523/JNEUROSCI.3317-06.2006

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Behavioral/Systems/Cognitive
Methodological Considerations on the Use of Template Matching to Study Long-Lasting Memory Trace Replay

Masami Tatsuno, Peter Lipa, and Bruce L. McNaughton

Arizona Research Laboratories, Division of Neural Systems, Memory and Aging, University of Arizona, Tucson, Arizona 85724-5115

Correspondence should be addressed to Bruce L. McNaughton, Arizona Research Laboratories, Division of Neural Systems, Memory and Aging, Life Sciences North Building, Room 384, University of Arizona, Tucson, AZ 85724-5115. Email: bruce{at}nsma.arizona.edu

Replay of behaviorally induced neural activity patterns during subsequent sleep has been suggested to play an important role in memory consolidation. Many previous studies, mostly involving familiar experiences, suggest that such reactivation occurs, but decays quickly (1 h). Recently, however, long-lasting (up to 48 h) "reverberation" of neural activity patterns induced by a novel experience was reported on the basis of a template-matching analysis. Because detection and quantification of memory-trace replay depends critically on analysis methods, we investigated the statistical properties of the template-matching method and analyzed rodent neural ensemble activity patterns after a novel experience. For comparison, we also analyzed the same data with an independent analysis technique, the explained variance method. Contrary to the recent report, we did not observe significant long-lasting reverberation using either the template matching or the explained variance approaches. The latter, however, did reveal short-lasting reactivation in the hippocampus and prefrontal cortex. In addition, detailed analysis of the template-matching method shows that, in the present study, coarse mean firing rate differences among neurons, but not fine temporal spike structures, dominate the results of template matching. Most importantly, it is also demonstrated that partial comparisons of template-matching correlations, such as used in the recent paper, may lead to erroneous conclusions. These investigations indicate that the outcome of template-matching analysis is very sensitive to the conditions of how it is applied, and should be interpreted cautiously, and that the existence of long-lasting reverberation after a novel experience requires additional verification.

Key words: neuronal reverberation; memory-trace reactivation; template matching; explained variance; multiple single-unit recording; novel experience

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Received Feb. 21, 2006; revised Aug. 30, 2006; accepted Aug. 31, 2006.

Correspondence should be addressed to Bruce L. McNaughton, Arizona Research Laboratories, Division of Neural Systems, Memory and Aging, Life Sciences North Building, Room 384, University of Arizona, Tucson, AZ 85724-5115. Email: bruce{at}nsma.arizona.edu

This article has been cited by other articles:

				C. S. Lansink, P. M. Goltstein, J. V. Lankelma, R. N. J. M. A. Joosten, B. L. McNaughton, and C. M. A. Pennartz Preferential Reactivation of Motivationally Relevant Information in the Ventral Striatum J. Neurosci., June 18, 2008; 28(25): 6372 - 6382. [Abstract] [Full Text] [PDF]

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