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The Journal of Neuroscience, November 3, 2004, 24(44):9811-9825; doi:10.1523/JNEUROSCI.1532-04.2004

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Behavioral/Systems/Cognitive
Entorhinal Cortex Lesions Disrupt the Relational Organization of Memory in Monkeys

Cindy A. Buckmaster,^1,3 Howard Eichenbaum,⁴ David G. Amaral,⁵ Wendy A. Suzuki,⁶ and Peter R. Rapp^1,2

¹Fishberg Department of Neuroscience and ²Kastor Neurobiology of Aging Laboratories, Department of Geriatrics and Adult Development, Mount Sinai School of Medicine, New York, New York 10029-6574, ³Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook, New York 11794, ⁴Laboratory of Cognitive Neuroscience, Boston University, Boston, Massachusetts 02215, ⁵The Medical Investigation of Neurodevelopmental Disorders Institute, University of California, Davis, California 95817, and ⁶Center for Neural Science, New York University, New York, New York 10003

Recent accounts suggest that the hippocampal system critically supports two central characteristics of episodic memory: the ability to establish and maintain representations for the salient relationships between experienced events (relational representation) and the capacity to flexibly manipulate memory (flexible memory expression). To test this proposal in monkeys, intact controls and subjects with bilateral aspiration lesions of the entorhinal cortex were trained postoperatively on two standard memory tasks, delayed nonmatchingto-sample (DNMS) and two-choice object discrimination (OD) learning, and three procedures intended to emphasize relational representation and flexible memory expression: a paired associate (PA) task, a transitive inference (TI) test of learning and memory for hierarchical stimulus relationships, and a spatial delayed recognition span (SDRS) procedure. The latter assessments each included critical "probe" tests that asked monkeys to evaluate the relationships among previously learned stimuli presented in novel combinations. Subjects with entorhinal cortex lesions scored as accurately as controls on all phases of DNMS and OD, procedures that can be solved on the basis of memory for individual stimuli. In contrast, experimental monkeys displayed deficits relative to controls on all phases of the PA, TI, and SDRS tasks that emphasized the flexible manipulation of memory for the relationships between familiar items. Together, the findings support the conclusion that the primate hippocampal system critically enables the relational organization of declarative memory.

Key words: memory; hippocampus; relational representation; medial temporal lobe; nonhuman primate

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Received April 22, 2004; revised September 1, 2004; accepted September 1, 2004.

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