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The Journal of Neuroscience, April 25, 2007, 27(17):4552-4561; doi:10.1523/JNEUROSCI.0396-07.2007

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Behavioral/Systems/Cognitive
Upregulation of Polysialylated Neural Cell Adhesion Molecule in the Dorsal Hippocampus after Contextual Fear Conditioning Is Involved in Long-Term Memory Formation

Miguel A. Lopez-Fernandez,¹ Marie-Françoise Montaron,² Emilio Varea,¹ Genevieve Rougon,⁴ Cesar Venero,³ Djoher Nora Abrous,² and Carmen Sandi¹

¹Brain Mind Institute, Swiss Federal Institute of Technology, CH-1015 Lausanne, Switzerland, ²Neurogenesis and Pathophysiology Laboratory, Bordeaux Neuroscience Research Center, Institut National de la Santé et de la Recherche Médicale 862 and University of Bordeaux 2, Bordeaux Cedex 33077, France, ³Psychobiology Department, Universidad Nacional de Educacion a Distancia, 28040 Madrid, Spain, and ⁴Centre National de la Recherche Scientifique Unité Mixte de Recherche 6216, Université de la Méditerranée, Institut de Biologie du Développement de Marseille-Luminy Case 907, Marseille Cedex 13288, France

Correspondence should be addressed to Carmen Sandi, Laboratory of Behavioral Genetics, Brain and Mind Institute, Swiss Federal Institute of Technology, CH-1015 Lausanne, Switzerland. Email: carmen.sandi{at}epfl.ch

The role of the hippocampus in pavlovian fear conditioning is controversial. Although lesion and pharmacological inactivation studies have suggested a key role for the dorsal hippocampus in contextual fear conditioning, the involvement of the ventral part is still uncertain. Likewise, the debate is open with regard to the putative implication of each hippocampal subdivision in fear conditioning to a discrete conditioned stimulus. We explored the potential existence of dissociations occurring in the dorsal versus ventral hippocampus at the cellular level while dealing with either contextual or cued fear conditioning and focused in a molecular "signature" linked to structural plasticity, the polysialylated form of the neural cell adhesion molecule (PSA-NCAM). We found an upregulation of PSA-NCAM expression in the dorsal (but not ventral) dentate gyrus at 24 h after contextual (but not tone) fear conditioning. Specific removal of PSA through microinfusion of the enzyme endoneuraminidase-N in the dorsal (but not ventral) hippocampus reduced freezing responses to the conditioned context. Therefore, we present evidence for a specific role of PSA-NCAM in the dorsal hippocampus in the plasticity processes occurring during consolidation of the context representation after "standard" contextual fear conditioning. Interestingly, we also found that exposing animals just to the context induced an activation of PSA-NCAM in both dorsal and ventral dentate gyrus. Altogether, these findings highlighting the distinctive occurrence of these neuroplastic processes in the dorsal hippocampus during the standard contextual fear-conditioning task enlighten the ongoing debate about the involvement of these hippocampal subdivisions in pavlovian fear conditioning.

Key words: PSA-NCAM; hippocampus; fear conditioning; neurogenesis; learning and memory; rat

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Received Dec. 2, 2006; revised March 17, 2007; accepted March 17, 2007.

Correspondence should be addressed to Carmen Sandi, Laboratory of Behavioral Genetics, Brain and Mind Institute, Swiss Federal Institute of Technology, CH-1015 Lausanne, Switzerland. Email: carmen.sandi{at}epfl.ch

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