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The Journal of Neuroscience, December 3, 2008, 28(49):13274-13284; doi:10.1523/JNEUROSCI.4074-08.2008

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Behavioral/Systems/Cognitive
Large-Scale Organization of Rat Sensorimotor Cortex Based on a Motif of Large Activation Spreads

Ron D. Frostig,^1,2,3 Ying Xiong,¹ Cynthia H. Chen-Bee,¹ Eugen Kvaák,¹ and Jimmy Stehberg¹

Departments of ¹Neurobiology and Behavior and ²Biomedical Engineering, and ³The Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, California 92697-4550

Correspondence should be addressed to Ron D. Frostig, Department of Neurobiology and Behavior, 2205 McGaugh Hall, University of California, Irvine, Irvine, CA 92697. Email: rfrostig{at}uci.edu

Parcellation according to function (e.g., visual, somatosensory, auditory, motor) is considered a fundamental property of sensorimotor cortical organization, traditionally defined from cytoarchitectonics and mapping studies relying on peak evoked neuronal activity. In the adult rat, stimulation of single whiskers evokes peak activity at topographically appropriate locations within somatosensory cortex and provides an example of cortical functional specificity. Here, we show that single whisker stimulation also evokes symmetrical areas of suprathreshold and subthreshold neuronal activation that spread extensively away from peak activity, effectively ignoring cortical borders by spilling deeply into multiple cortical territories of different modalities (auditory, visual and motor), where they were blocked by localized neuronal activity blocker injections and thus ruled out as possibly caused by "volume conductance." These symmetrical activity spreads were supported by underlying border-crossing, long-range horizontal connections as confirmed with transection experiments and injections of anterograde neuronal tracer experiments. We found such large evoked activation spreads and their underlying connections regardless of whisker identity, cortical layer, or axis of recorded responses, thereby revealing a large scale nonspecific organization of sensorimotor cortex based on a motif of large symmetrical activation spreads. Because the large activation spreads and their underlying horizontal connections ignore anatomical borders between cortical modalities, sensorimotor cortex could therefore be viewed as a continuous entity rather than a collection of discrete, delineated unimodal regions, an organization that could coexist with established specificity of cortical organization and that could serve as a substrate for associative learning, direct multimodal integration and recovery of function after injury.

Key words: whiskers; somatosensory cortex; barrel; extracellular recordings; local field potentials; action potential

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Received Aug. 25, 2008; accepted Oct. 18, 2008.

Correspondence should be addressed to Ron D. Frostig, Department of Neurobiology and Behavior, 2205 McGaugh Hall, University of California, Irvine, Irvine, CA 92697. Email: rfrostig{at}uci.edu

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