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The Journal of Neuroscience, November 1, 2006, 26(44):11304-11312; doi:10.1523/JNEUROSCI.3071-06.2006

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Behavioral/Systems/Cognitive
Experience-Dependent Eye Movements, Awareness, and Hippocampus-Dependent Memory

Christine N. Smith,¹ Ramona O. Hopkins,^4,5 and Larry R. Squire^1,2,3,6

Departments of ¹Psychiatry, ²Psychology, and ³Neuroscience, University of California, San Diego, La Jolla, California 92093, ⁴Psychology Department and Neuroscience Center, Brigham Young University, Provo, Utah 84602, ⁵Department of Medicine, Pulmonary, and Critical Care Division, LDS Hospital, Salt Lake City, Utah 84143, and ⁶Veterans Affairs Medical Center 116A, 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 asked what kind of memory is operating when eye movements change as the result of experience. Participants viewed scenes that were either novel, repeated, or manipulated (i.e., a change was introduced in one region of the scene). Eye movements differed depending on the past viewing history of each scene. Participants made fewer fixations and sampled fewer regions when scenes were repeated than when scenes were novel. When scenes were altered, participants made more fixations in the altered region, spent more time looking at the altered region, and made more transitions into and out of the altered region than in unchanged (matched) regions in the repeated scenes. Importantly, these effects occurred only when individuals were aware that a change had occurred. Participants who were unaware that the scene had been altered looked at the changed scenes in the same way that they looked at repeated scenes. Thus, there was no indication that eye movements could reveal an unaware (unconscious) form of memory. Instead, eye movements reflected conscious memory of whether the scene was repeated or manipulated. The findings were the same when awareness was assessed after viewing all the scenes (experiment 1) and when awareness was assessed after each scene was presented (experiment 2). In experiment 3, memory-impaired patients with damage limited to the hippocampus were impaired at deciding whether scenes were novel, repeated, or manipulated. Thus, the ability to consciously recollect recent encounters with scenes reflects a form of hippocampus-dependent memory. The findings show that experience-dependent eye movements in response to altered scenes reflect conscious, declarative memory, and they support the link between aware memory, declarative memory, and hippocampus-dependent memory.

Key words: awareness; eye movements; amnesia; memory; declarative; hippocampus; medial temporal lobe

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Received July 19, 2006; revised Sept. 8, 2006; accepted Sept. 17, 2006.

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

This article has been cited by other articles:

				M. D. Crutcher, R. Calhoun-Haney, C. M. Manzanares, J. J. Lah, A. I. Levey, and S. M. Zola Eye Tracking During a Visual Paired Comparison Task as a Predictor of Early Dementia American Journal of Alzheimer's Disease and Other Dementias, June 1, 2009; 24(3): 258 - 266. [Abstract] [PDF]

				C. N. Smith and L. R. Squire Experience-Dependent Eye Movements Reflect Hippocampus-Dependent (Aware) Memory J. Neurosci., November 26, 2008; 28(48): 12825 - 12833. [Abstract] [Full Text] [PDF]

				A. J. Greene, W. L. Gross, C. L. Elsinger, and S. M. Rao Hippocampal differentiation without recognition: An fMRI analysis of the contextual cueing task Learn. Mem., August 9, 2007; 14(8): 548 - 553. [Abstract] [Full Text] [PDF]

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