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The Journal of Neuroscience, April 14, 2004, 24(15):3826-3836; doi:10.1523/JNEUROSCI.0410-04.2004

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Behavioral/Systems/Cognitive
Corticohippocampal Contributions to Spatial and Contextual Learning

Rebecca D. Burwell, Michael P. Saddoris, David J. Bucci, and Kjesten A. Wiig

Departments of Psychology and Neuroscience, Brown University, Providence, Rhode Island 02912

Spatial and contextual learning are considered to be dependent on the hippocampus, but the extent to which other structures in the medial temporal lobe memory system support these functions is not well understood. This study examined the effects of individual and combined lesions of the perirhinal, postrhinal, and entorhinal cortices on spatial and contextual learning. Lesioned subjects were consistently impaired on measures of contextual fear learning and consistently unimpaired on spatial learning in the Morris water maze. Neurotoxic lesions of perirhinal or postrhinal cortex that were previously shown to impair contextual fear conditioning (Bucci et al., 2000) or contextual discrimination (Bucci et al., 2002) caused little or no impairment in place learning and incidental learning in the water maze. Combined lesions of perirhinal plus lateral entorhinal or postrhinal plus medial entorhinal cortices resulted in deficits in acquisition of contextual discrimination but had no effect on place learning in the water maze. Finally, a parahippocampal lesion comprising combined neurotoxic damage to perirhinal, postrhinal, and entorhinal cortices resulted in profound impairment in acquisition of a standard passive avoidance task but failed to impair place learning. In the same experiment, rats with hippocampal lesions were impaired in spatial navigation. These results indicate that tasks requiring the association between context and an aversive stimulus depend on corticohippocampal circuitry, whereas place learning in the water maze can be accomplished without the full complement of highly processed information from the cortical regions surrounding the hippocampus. The evidence that different brain systems underlie spatial navigation and contextual learning has implications for research on memory when parahippocampal regions are involved.

Key words: perirhinal; postrhinal; entorhinal; parahippocampal; hippocampal; water maze; fear conditioning; passive avoidance

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Received Dec 17, 2003; revised March 5, 2004; accepted March 5, 2004.

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