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The Journal of Neuroscience, March 18, 2009, 29(11):3475-3484; doi:10.1523/JNEUROSCI.5370-08.2009

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Behavioral/Systems/Cognitive
A Specific Role of the Human Hippocampus in Recall of Temporal Sequences

Hanne Lehn,¹ Hill-Aina Steffenach,¹ Niels M. van Strien,¹ Dick J. Veltman,³ Menno P. Witter,² and Asta K. Håberg^1,4

¹Department of Circulation and Medical Imaging and ²Department of Neuroscience, Kavli Institute for Systems Neuroscience and Center for the Biology of Memory, Norwegian University of Science and Technology, 7489 Trondheim, Norway, ³Department of Psychiatry, VU University Medical Center and Academic Medical Center, 1007 MB Amsterdam, The Netherlands, and ⁴Department of Medical Imaging, St. Olavs Hospital, 7006 Trondheim, Norway

Correspondence should be addressed to Asta K. Håberg, Department of Circulation and Medical Imaging, Faculty of Medicine, Norwegian University of Science and Technology, 7489 Trondheim, Norway. Email: asta.haberg{at}ntnu.no

There is a growing interest in how temporal order of episodic memories is represented within the medial temporal lobe (MTL). Animal studies suggest that the hippocampal formation (HF) is critical for retrieving the temporal order of past experiences. However, human imaging studies that have tested recency discrimination between pairs of previously encoded items have generally failed to report HF activation. We hypothesized that recalling a naturalistic sequence of past events would be particularly sensitive to HF function, attributable to greater involvement of associative processes. To test this prediction, we let subjects watch a novel movie and later, during functional magnetic resonance imaging, asked them to rearrange and "replay" scenes from the movie in correct order. To identify areas specifically involved in retrieval of temporal order, we used a control condition where subjects logically inferred the order of scenes from the same movie. Extensive MTL activation was observed during sequence recall. Activation within the right HF was specifically related to retrieval of temporal order and correlated positively with accuracy of sequence recall. Also, the bilateral parahippocampal cortex responded to retrieval of temporal order, but the activation here was not related to performance. Our study is the first to unequivocally demonstrate that correct sequence recall depends on HF.

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Received Nov. 5, 2008; revised Feb. 10, 2009; accepted Feb. 11, 2009.

Correspondence should be addressed to Asta K. Håberg, Department of Circulation and Medical Imaging, Faculty of Medicine, Norwegian University of Science and Technology, 7489 Trondheim, Norway. Email: asta.haberg{at}ntnu.no

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