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The Journal of Neuroscience, February 25, 2004, 24(8):2013-2026; doi:10.1523/JNEUROSCI.3763-03.2004

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Behavioral/Systems/Cognitive
The Hippocampal/Parahippocampal Regions and Recognition Memory: Insights from Visual Paired Comparison versus Object-Delayed Nonmatching in Monkeys

Sarah Nemanic, Maria C. Alvarado, and Jocelyne Bachevalier

Department of Neurobiology and Anatomy, University of Texas Health Science Center, Houston, Texas 77030

Recognition memory was assessed by submitting the same adult monkeys to visual paired comparison (VPC) with mixed delays (10-120 sec), followed by three consecutive versions of object-delayed nonmatching-to-sample (DNMS): increasing delays (10-600 sec), lengthened lists (3-10 objects), and intervening distractors in the delays (light at 10 sec, motor task at 30-600 sec, or context change at 600 sec). Four groups were tested: normal controls, monkeys with ibotenic acid lesions of the hippocampal formation (H), and monkeys with aspiration lesions of either the perirhinal (PRh) or parahippocampal (areas TH/TF) cortex. Group H was impaired on VPC at delays 60 sec but had difficulty on DNMS only at 600 sec delays with distraction. In group TH/TF, the VPC impairment emerged earlier (30 sec); yet, once the nonmatching rule was mastered, no significant change occurred on any DNMS condition. Only group PRh behaved congruently on VPC and DNMS, exhibiting a deficit at the easiest condition that worsened with increasing delays as well as in DNMS lengthened list and distraction conditions. These results led us to postulate that VPC and DNMS, as previously administered to monkeys, were not equivalent visual recognition memory probes. Specifically, we propose that, for VPC, because of passive (incidental) encoding, the animal's performance rests on both item familiarity and event recollection, whereas, for DNMS, because of active (purposeful) encoding, performance relies more on item familiarity. This proposal converges with current models postulating distinct, but interactive, mnemonic roles for the hippocampal and adjacent TH/TF regions.

Key words: familiarity; recollection; perirhinal; associative recognition; incidental learning; intentional learning

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Received Aug 12, 2003; revised December 15, 2003; accepted December 16, 2003.

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