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The Journal of Neuroscience, June 4, 2008, 28(23):5931-5943; doi:10.1523/JNEUROSCI.0815-08.2008

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Development/Plasticity/Repair
Cortical Adenylyl Cyclase 1 Is Required for Thalamocortical Synapse Maturation and Aspects of Layer IV Barrel Development

Takuji Iwasato,^1,2 * Melis Inan,^3,4 * Hiroaki Kanki,¹ Reha S. Erzurumlu,⁵ Shigeyoshi Itohara,¹ and Michael C. Crair^3,4

¹Laboratory for Behavioral Genetics, RIKEN Brain Science Institute, Saitama 351-0198, Japan, ²PRESTO, Japan Science and Technology Agency, Saitama 332-0012, Japan, ³Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510, ⁴Program in Developmental Biology, Baylor College of Medicine, Houston, Texas 77030, and ⁵Department of Anatomy and Neurobiology, University of Maryland, Baltimore, School of Medicine, Baltimore, Maryland 21201

Correspondence should be addressed to either of the following: Shigeyoshi Itohara, Laboratory for Behavioral Genetics, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan, Email: sitohara{at}brain.riken.jp; or Michael C. Crair, Department of Neurobiology, Yale University School of Medicine, 333 Cedar Street, SHM B301, New Haven, CT 06510, E-mail: Email: michael.crair{at}yale.edu

Experimental evidence from mutant or genetically altered mice indicates that the formation of barrels and the proper maturation of thalamocortical (TC) synapses in the primary somatosensory (barrel) cortex depend on mechanisms mediated by neural activity. Type 1 adenylyl cyclase (AC1), which catalyzes the formation of cAMP, is stimulated by increases in intracellular Ca²⁺ levels in an activity-dependent manner. The AC1 mutant mouse, barrelless (brl), lacks typical barrel cytoarchitecture, and displays presynaptic and postsynaptic functional defects at TC synapses. However, because AC1 is expressed throughout the trigeminal pathway, the barrel cortex phenotype of brl mice may be a consequence of AC1 disruption in cortical or subcortical regions. To examine the role of cortical AC1 in the development of morphological barrels and TC synapses, we generated cortex-specific AC1 knock-out (CxAC1KO) mice. We found that neurons in layer IV form grossly normal barrels and TC axons fill barrel hollows in CxAC1KO mice. In addition, whisker lesion-induced critical period plasticity was not impaired in these mice. However, we found quantitative reductions in the quality of cortical barrel cytoarchitecture and dendritic asymmetry of layer IV barrel neurons in CxAC1KO mice. Electrophysiologically, CxAC1KO mice have deficits in the postsynaptic but not in the presynaptic maturation of TC synapses. These results suggest that activity-dependent postsynaptic AC1–cAMP signaling is required for functional maturation of TC synapses and the development of normal barrel cortex cytoarchitecture. They also suggest that the formation of the gross morphological features of barrels is independent of postsynaptic AC1 in the barrel cortex.

Key words: somatosensory cortex; activity dependent; AC1; barrel; thalamocortical; conditional knock-out

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Received Feb. 24, 2008; revised April 7, 2008; accepted April 27, 2008.

Correspondence should be addressed to either of the following: Shigeyoshi Itohara, Laboratory for Behavioral Genetics, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan, Email: sitohara{at}brain.riken.jp; or Michael C. Crair, Department of Neurobiology, Yale University School of Medicine, 333 Cedar Street, SHM B301, New Haven, CT 06510, E-mail: Email: michael.crair{at}yale.edu

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