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The Journal of Neuroscience, February 1, 2006, 26(5):1507-1515; doi:10.1523/JNEUROSCI.4441-05.2006

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Behavioral/Systems/Cognitive
Fornix Lesions Decouple the Induction of Hippocampal Arc Transcription from Behavior But Not Plasticity

Bonnie R. Fletcher,¹ Michael E. Calhoun,² Peter R. Rapp,¹ and Matthew L. Shapiro¹

¹Fishberg Department of Neuroscience and Alfred B. and Gudrun J. Kastor Neurobiology of Aging Laboratories, Mount Sinai School of Medicine, New York, New York 10029-6574, and ²Department of Cellular Neurology, Hertie-Institute for Clinical Brain Research, University of Tübingen, D-72076 Tübingen, Germany

Correspondence should be addressed to Dr. Matthew L. Shapiro, Mount Sinai School of Medicine, One Gustave Levy Place, Box 1639, New York, NY 10029. Email: matthew.shapiro{at}mssm.edu

The immediate-early gene (IEG) Arc is transcribed after behavioral and physiological treatments that induce synaptic plasticity and is implicated in memory consolidation. The relative contributions of neuronal activity and learning-related plasticity to the behavioral induction of Arc remain to be defined. To differentiate the contributions of each, we assessed the induction of Arc transcription in rats with fornix lesions that impair hippocampal learning yet leave cortical connectivity and neuronal firing essentially intact. Arc expression was assessed after exploration of novel environments and performance of a novel water maze task during which normal rats learned the spatial location of an escape platform. During the same task, rats with fornix lesions learned to approach a visible platform but did not learn its spatial location. Rats with fornix lesions had normal baseline levels of hippocampal Arc mRNA, but unlike normal rats, expression was not increased in response to water maze training. The integrity of signaling pathways controlling Arc expression was demonstrated by stimulation of the medial perforant path, which induced normal synaptic potentiation and Arc in rats with fornix lesions. Together, the results demonstrate that Arc induction can be decoupled from behavior and is more likely to indicate the engagement of synaptic plasticity mechanisms than synaptic or neuronal activity per se. The results further imply that fornix lesions may impair memory in part by decoupling neuronal activity from signaling pathways required for long-lasting hippocampal synaptic plasticity.

Key words: hippocampus; learning; LTP; Arc; fornix lesion; immediate-early gene

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Received Oct. 18, 2005; revised Nov. 28, 2005; accepted Dec. 17, 2005.

Correspondence should be addressed to Dr. Matthew L. Shapiro, Mount Sinai School of Medicine, One Gustave Levy Place, Box 1639, New York, NY 10029. Email: matthew.shapiro{at}mssm.edu

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