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The Journal of Neuroscience, April 19, 2006, 26(16):4338-4349; doi:10.1523/JNEUROSCI.3745-05.2006

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Development/Plasticity/Repair
Barrel Map Development Relies on Protein Kinase A Regulatory Subunit II-Mediated cAMP Signaling

Melis Inan,¹ Hui-Chen Lu,^1,3 Michael J. Albright,² Wei-Chi She,^1,3 and Michael C. Crair^1,2

¹Program in Developmental Biology, ²Department of Neuroscience, and ³The Cain Foundation Laboratories, Department of Pediatrics, Division of Neurology/Developmental Neuroscience, Baylor College of Medicine, Houston, Texas 77030

Correspondence should be addressed to Michael C. Crair, Department of Neuroscience, Baylor College of Medicine, One Baylor Plaza, S-603, Houston, Texas 77030. Email: mcrair{at}bcm.tmc.edu

The cellular and molecular mechanisms mediating the activity-dependent development of brain circuitry are still incompletely understood. Here, we examine the role of cAMP-dependent protein kinase [protein kinase A (PKA)] signaling in cortical development and plasticity, focusing on its role in thalamocortical synapse and barrel map development. We provide direct evidence that PKA activity mediates barrel map formation using knock-out mice that lack type II regulatory subunits of PKA (PKARII). We show that PKARII-mediated PKA function is required for proper dendritogenesis and the organization of cortical layer IV neurons into barrels, but not for the development and plasticity of thalamocortical afferent clustering into a barrel pattern. We localize PKARII function to postsynaptic processes in barrel cortex and show that postsynaptic PKA targets, but not presynaptic PKA targets, have decreased phosphorylation in pkar2b knock-out (PKARII^–/–) mice. We also show that long-term potentiation at TC synapses and the associated developmental increase in AMPA receptor function at these synapses, which normally occurs as barrels form, is absent in PKARII^–/– mice. Together, these experiments support an activity-dependent model for barrel map development in which the selective addition and elimination of thalamocortical synapses based on Hebbian mechanisms for synapse formation is mediated by a cAMP/PKA-dependent pathway that relies on PKARII function.

Key words: somatosensory cortex; activity dependent; glutamate; PKA; barrel; NMDA receptor

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Received Sept. 4, 2005; revised Dec. 31, 2005; accepted Jan. 21, 2006.

Correspondence should be addressed to Michael C. Crair, Department of Neuroscience, Baylor College of Medicine, One Baylor Plaza, S-603, Houston, Texas 77030. Email: mcrair{at}bcm.tmc.edu

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