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The Journal of Neuroscience, May 17, 2006, 26(20):5484-5491; doi:10.1523/JNEUROSCI.2685-05.2006

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Behavioral/Systems/Cognitive
Context Fear Learning in the Absence of the Hippocampus

Brian J. Wiltgen,¹ Matthew J. Sanders,¹ Stephan G. Anagnostaras,² Jennifer R. Sage,² and Michael S. Fanselow¹

¹Psychology and the Brain Research Institute, University of California, Los Angeles, Los Angeles, California 90095, and ²Psychology and Neurosciences Program, University of California, San Diego, La Jolla, California 92093

Correspondence should be addressed to Michael S. Fanselow, Psychology Department, University of California, Los Angeles, 1285 Franz Hall, Box 95163, Los Angeles, CA 90095-1563. Email: fanselow{at}psych.ucla.edu

Lesions of the rodent hippocampus invariably abolish context fear memories formed in the recent past but do not always prevent new learning. To better understand this discrepancy, we thoroughly examined the acquisition of context fear in rats with pretraining excitotoxic lesions of the dorsal hippocampus. In the first experiment, animals received a shock immediately after placement in the context or after variable delays. Immediate shock produced no context fear learning in lesioned rats or controls. In contrast, delayed shock produced robust context fear learning in both groups. The absence of fear with immediate shock occurs because animals need time to form a representation of the context before shock is presented. The fact that it occurs in both sham and lesioned rats suggests that they learn about the context in a similar manner. However, despite learning about the context in the delay condition, lesioned rats did not acquire as much fear as controls. The second experiment showed that this lesion-induced deficit could be overcome by increasing the number of conditioning trials. Lesioned animals learned normally after multiple shocks, regardless of freezing level or trial spacing. The last experiment showed that animals with complete hippocampus lesions could also learn about the context, although the same lesions produced devastating retrograde amnesia. These results demonstrate that alternative systems can acquire context fear but do so less efficiently than the hippocampus.

Key words: amnesia; memory; conditioning; emotion; rats; spatial

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Received Feb. 25, 2005; revised April 7, 2006; accepted April 8, 2006.

Correspondence should be addressed to Michael S. Fanselow, Psychology Department, University of California, Los Angeles, 1285 Franz Hall, Box 95163, Los Angeles, CA 90095-1563. Email: fanselow{at}psych.ucla.edu

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