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The Journal of Neuroscience, September 23, 2009, 29(38):11880-11890; doi:10.1523/JNEUROSCI.2245-09.2009

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Behavioral/Systems/Cognitive
Performance-Related Sustained and Anticipatory Activity in Human Medial Temporal Lobe during Delayed Match-to-Sample

Rosanna K. Olsen,¹ Elizabeth A. Nichols,¹ Janice Chen,¹ Jack F. Hunt,¹ Gary H. Glover,^2,3 John D. E. Gabrieli,⁴ and Anthony D. Wagner^1,3

Departments of ¹Psychology and ²Radiology, and ³Neurosciences Program, Stanford University, Stanford, California 94305, and ⁴Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Correspondence should be addressed to Rosanna K. Olsen, Department of Psychology, Jordan Hall, Building 420, Stanford University, 650 Serra Mall, Stanford, CA 94305. Email: rkolsen{at}stanford.edu

The medial temporal lobe (MTL)—hippocampus and surrounding perirhinal, parahippocampal, and entorhinal cortical areas—has long been known to be critical for long-term memory for events. Recent functional neuroimaging and neuropsychological data in humans performing short-delay tasks suggest that the MTL also contributes to performance even when retention intervals are brief, and single-unit data in rodents reveal sustained, performance-related delay activity in the MTL during delayed-non-match-to-sample tasks. The current study used functional magnetic resonance imaging to examine the relationship between activation in human MTL subregions and performance during a delayed-match-to-sample task with repeated (non-trial-unique) stimuli. On critical trials, the presentation of two faces was followed by a 30 s delay period, after which participants performed two-alternative forced-choice recognition. Functional magnetic resonance imaging revealed significant delay period activity in anterior hippocampus, entorhinal cortex, and perirhinal cortex over the 30 s retention interval, with the magnitude of activity being significantly higher on subsequently correct compared with subsequently incorrect trials. In contrast, posterior hippocampus, parahippocampal cortex, and fusiform gyrus activity linearly increased across the 30 s delay, suggesting an anticipatory response, and activity in parahippocampal cortex and hippocampus was greater during the probe period on correct compared with incorrect trials. These results indicate that at least two patterns of MTL delay period activation—sustained and anticipatory—are present during performance of short-delay recognition memory tasks, providing novel evidence that multiple processes govern task performance. Implications for understanding the role of the hippocampus and surrounding MTL cortical areas in recognition memory after short delays are discussed.

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Received May 12, 2009; revised July 6, 2009; accepted Aug. 5, 2009.

Correspondence should be addressed to Rosanna K. Olsen, Department of Psychology, Jordan Hall, Building 420, Stanford University, 650 Serra Mall, Stanford, CA 94305. Email: rkolsen{at}stanford.edu

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