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The Journal of Neuroscience, May 17, 2006, 26(20):5393-5401; doi:10.1523/JNEUROSCI.0750-06.2006

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Development/Plasticity/Repair
Involvement of Protein Kinase A in Patterning of the Mouse Somatosensory Cortex

Ruth F. Watson,¹ Raja M. Abdel-Majid,² Mark W. Barnett,¹ Brandon S. Willis,³ Alla Katsnelson,¹ Thomas H. Gillingwater,¹ G. Stanley McKnight,³ Peter C. Kind,^1 * and Paul E. Neumann^2 *

¹Centre for Integrative Physiology, Centre for Neuroscience, University of Edinburgh, Edinburgh EH8 9XD, United Kingdom, ²Department of Anatomy and Neurobiology, Dalhousie University, Halifax, Nova Scotia, Canada B3H 1X5, and ³Department of Pharmacology, University of Washington, Seattle, Washington 98195

Correspondence should be addressed to Peter C. Kind, Centre for Integrative Physiology, Centre for Neuroscience, University of Edinburgh, Hugh Robson Building, George Square, Edinburgh EH8 9XD, UK. Email: pkind{at}ed.ac.uk

Patterning of the mouse somatosensory cortex is unusually evident because of the presence of a "barrel field." Presynaptic serotonin and postsynaptic glutamate receptors regulate barrel formation, but little is known of the intracellular signaling pathways through which they act. To determine whether protein kinase A (PKA) plays a role in the development of the barrel field, we examined five viable PKA subunit-specific knock-out (KO) mouse lines for barrel field abnormalities. Barrels are present in these mice, but those lacking the RII subunit display significantly reduced contrast between the cell densities of barrel hollows and sides compared with wild-type animals. Thalamocortical afferent segregation in the posterior medial barrel subfield appeared normal, suggesting a postsynaptic site of gene action for the RII protein. Immunoelectron microscopy confirmed that RII was selectively localized to dendrites and dendritic spines. Mice lacking RII show reduced glutamate receptor A (GluRA) subunit insertion into the postsynaptic density in postnatal day 7 somatosensory cortex; however, GluRA KO mice developed normal barrels. Our results clearly demonstrate a role for postsynaptic PKA signaling pathways in barrel differentiation. They also demonstrate a clear dissociation between the regulation of GluRA trafficking by PKA and its role in barrel formation. Finally, although a role for PKA downstream of cAMP cannot be ruled out, these data suggest that PKA may not be the principle downstream target because none of the mutants showed a barrelless phenotype similar to that observed in adenylate cyclase type 1 KO mice. These results give insight into activity-dependent mechanisms that regulate barrel formation.

Key words: barrel; cAMP; protein kinase A; somatosensory cortex; development; NMDA receptor

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Received Oct. 12, 2005; revised March 23, 2006; accepted March 25, 2006.

Correspondence should be addressed to Peter C. Kind, Centre for Integrative Physiology, Centre for Neuroscience, University of Edinburgh, Hugh Robson Building, George Square, Edinburgh EH8 9XD, UK. Email: pkind{at}ed.ac.uk

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