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The Journal of Neuroscience, March 8, 2006, 26(10):2692-2703; doi:10.1523/JNEUROSCI.3956-05.2006

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Development/Plasticity/Repair
Role of Efficient Neurotransmitter Release in Barrel Map Development

Hui-Chen Lu,¹ Daniel A. Butts,² Pascal S. Kaeser,³ Wei-Chi She,¹ Roger Janz,⁴ and Michael C. Crair¹

¹Department of Neuroscience, Program in Developmental Biology, Baylor College of Medicine, Houston, Texas 77030, ²Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, ³Howard Hughes Medical Institute, Center for Basic Neuroscience, UT Southwestern Medical Center, Dallas, Texas 75390, and ⁴Department of Neurobiology and Anatomy, W. M. Keck Center for the Neurobiology of Learning and Memory, University of Texas–Houston Medical School, Houston, Texas 77030

Correspondence should be addressed to either of the following: Hui-Chen Lu, The Cain Foundation Laboratories, Department of Pediatrics, Division of Neurology/Developmental Neuroscience, Baylor College of Medicine, 6621 Fannin Street, MC3-6365, Houston, TX 77030, Email: hclu{at}bcm.tmc.edu or Michael C. Crair, Department of Neuroscience, Baylor College of Medicine, One Baylor Plaza, S-603, Houston, TX 77030, mcrair{at}bcm.tmc.edu

Cortical maps are remarkably precise, with organized arrays of thalamocortical afferents (TCAs) that project into distinct neuronal modules. Here, we present evidence for the involvement of efficient neurotransmitter release in mouse cortical barrel map development using barrelless mice, a loss-of-function mutant of calcium/calmodulin-activated adenylyl cyclase I (AC1), and mice with a mutation in Rab3-interacting molecule 1 (RIM1), an active zone protein that regulates neurotransmitter release. We demonstrate that release efficacy is substantially decreased in barrelless TCAs. We identify RIMs as important phosphorylation targets for AC1 in the presynaptic terminal. We further show that RIM1 mutant mice have reduced TCA neurotransmitter release efficacy and barrel map deficits, although not as severe as those found in barrelless mice. This supports the role of RIM proteins in mediating, in part, AC1 signaling in barrel map development. Finally, we present a model to show how inadequacies in presynaptic function can interfere with activity-dependent processes in neuronal circuit formation. These results demonstrate how efficient synaptic transmission mediated by AC1 function contributes to the development of cortical barrel maps.

Key words: cAMP; PKA; neurotransmitter release; cortical map; somatosensory; short-term plasticity; barrels

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Received Sept. 19, 2005; revised Jan. 16, 2006; accepted Jan. 21, 2006.

Correspondence should be addressed to either of the following: Hui-Chen Lu, The Cain Foundation Laboratories, Department of Pediatrics, Division of Neurology/Developmental Neuroscience, Baylor College of Medicine, 6621 Fannin Street, MC3-6365, Houston, TX 77030, Email: hclu{at}bcm.tmc.edu or Michael C. Crair, Department of Neuroscience, Baylor College of Medicine, One Baylor Plaza, S-603, Houston, TX 77030, mcrair{at}bcm.tmc.edu

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