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The Journal of Neuroscience, December 10, 2008, 28(50):13390-13400; doi:10.1523/JNEUROSCI.2680-08.2008

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Behavioral/Systems/Cognitive
Dopamine D₁ Receptor Modulates Hippocampal Representation Plasticity to Spatial Novelty

Anh Hai Tran,^1,4 Teruko Uwano,^2,4 Tatsuo Kimura,^1,4 Etsuro Hori,^1,4 Motoya Katsuki,³ Hisao Nishijo,^1,4 and Taketoshi Ono^1,4,5

¹System Emotional Science and ²Department of Integrative Neuroscience, University of Toyama, Toyama 930-0194, Japan, ³National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki 444-8585, Aichi, Japan, ⁴Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Saitama 332-0012, Japan, and ⁵Department of Emotional Neuroscience, Showa University School of Medicine, Tokyo 142-8555, Japan

Correspondence should be addressed to Taketoshi Ono, System Emotional Science, University of Toyama, Sugitani 2630, Toyama 930-0194, Japan. Email: onotake{at}med.u-toyama.ac.jp

The human hippocampus is critical for learning and memory. In rodents, hippocampal pyramidal neurons fire in a location-specific manner, forming relational representations of environmental cues. The importance of glutamatergic systems in learning and in hippocampal neural synaptic plasticity has been shown. However, the role of dopaminergic systems in the response of hippocampal neural plasticity to novel and familiar spatial stimuli remains unclear. To clarify this important issue, we recorded hippocampal neurons from dopamine D₁ receptor knock-out (D1R-KO) mice and their wild-type (WT) littermates under the manipulation of distinct spatial cues in a familiar and a novel environment. Here we report that in WT mice, the majority of place cells quickly responded to the manipulations of distal and proximal cues in both familiar and novel environments. In contrast, the influence of distal cues on spatial firing in D1R-KO mice was abolished. In the D1R-KO mice, the influence of proximal cues was facilitated in a familiar environment, and in a novel environment most of the place cells were less likely to respond to changes of spatial cues. Our results demonstrate that hippocampal neurons in mice can rapidly and flexibly encode information about space from both distal and proximal cues to cipher a novel environment. This ability is necessary for many types of learning, and lacking D1R can radically alter this learning-related neural activity. We propose that D1R is crucially implicated in encoding spatial information in novel environments, and influences the plasticity of hippocampal representations, which is important in spatial learning and memory.

Key words: dopamine receptor; hippocampus; place cells; brain stimulation reward; neural plasticity; spatial novelty

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Received June 12, 2008; revised Oct. 10, 2008; accepted Oct. 10, 2008.

Correspondence should be addressed to Taketoshi Ono, System Emotional Science, University of Toyama, Sugitani 2630, Toyama 930-0194, Japan. Email: onotake{at}med.u-toyama.ac.jp

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