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The Journal of Neuroscience, November 26, 2008, 28(48):12825-12833; doi:10.1523/JNEUROSCI.4542-08.2008

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Behavioral/Systems/Cognitive
Experience-Dependent Eye Movements Reflect Hippocampus-Dependent (Aware) Memory

Christine N. Smith¹ and Larry R. Squire^1,2,3,4

Departments of ¹Psychiatry, ²Neurosciences, and ³Psychology, University of California, San Diego, La Jolla, California 92093, and ⁴Veterans Affairs San Diego Healthcare System, San Diego, California 92161

Correspondence should be addressed to Dr. Larry R. Squire, Veterans Affairs Medical Center 116A, 3550 La Jolla Village Drive, San Diego, CA 92161. Email: lsquire{at}ucsd.edu

We investigated the relationship between experience-dependent eye movements, hippocampus-dependent memory, and aware memory. We measured eye movements in young adults, older adults, and memory-impaired patients with damage to the medial temporal lobe as they viewed 120 novel scenes and 120 previously viewed scenes. Participants indicated if each scene was old or new and also gave a confidence rating for the memory judgment. Young adults and older adults explored old scenes less than they explored new scenes, but the patients did not. For the young and older adults, this effect was observed only when participants were aware of the scene's familiar or novel status. In a second experiment, young adults viewed scenes that were either new, had been viewed previously, or had been viewed previously but had been changed (i.e., an object within the scene was either added or removed). The only instructions were to pay attention to the scenes and view each scene as it appeared, and there was no expectation that memory would be tested. Directly after the first altered scene was presented, participants were asked to classify the scene as new, old, or old but changed. Participants who were aware of the manipulation preferentially viewed the changed region, but participants who were unaware did not. These findings suggest that experience-dependent eye movements reflect hippocampus-dependent (and aware) memory, even when participants have no expectation that memory is being tested; and they are consistent with the view that awareness of what is learned is a fundamental characteristic of hippocampus-dependent memory.

Key words: learning and memory; hippocampus; eye movement; amnesia; declarative; awareness

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Received Sept. 22, 2008; revised Oct. 17, 2008; accepted Oct. 20, 2008.

Correspondence should be addressed to Dr. Larry R. Squire, Veterans Affairs Medical Center 116A, 3550 La Jolla Village Drive, San Diego, CA 92161. Email: lsquire{at}ucsd.edu

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