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The Journal of Neuroscience, September 23, 2009, 29(38):11817-11827; doi:10.1523/JNEUROSCI.3431-09.2009

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Development/Plasticity/Repair
Reliable and Precise Neuronal Firing during Sensory Plasticity in Superficial Layers of Primary Somatosensory Cortex

Brett L. Benedetti,^1,2 Stanislaw Glazewski,³ and Alison L. Barth^1,2

¹Department of Biological Sciences and ²Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, and ³School of Life Sciences, Institute for Science and Technology in Medicine, Keele University, Staffordshire, Keele, ST5 5BG, United Kingdom

Correspondence should be addressed to Alison L. Barth, Box 142, Mellon Institute, Carnegie Mellon University, 4400 Fifth Avenue, Pittsburgh, PA 15213. Email: barth{at}cmu.edu

Neocortical neurons show astonishing variation in the presence and timing of action potentials across stimulus trials, a phenomenon whose function and significance has been the subject of great interest. Here we present data showing that this response variability can be significantly reduced by altered sensory experience. Removal of all but one whisker from the side of the mouse face results in the rapid (within 24 h) potentiation of mean firing rates within the cortical representation of the spared whisker in young postnatal animals (postnatal days 13–16). Analysis of single-unit responses from whisker-spared animals shows that this potentiation can be attributed to an enhancement of trial-to-trial reliability (i.e., reduced response failures), as well as an increase in the mean number of spikes evoked within a successful trial. Changes were confined to superficial layers 2/3 and were not observed in the input layer of the cortex, layer 4. In addition to these changes in firing rates, we also observed profound changes in the precise timing of sensory-evoked responses. Trial-to-trial temporal precision was enhanced and the absolute latency of responses was reduced after single-whisker experience. Enhanced spike-timing precision and trial-to-trial reliability could also be triggered in adolescent animals with longer periods (7 d) of single-whisker experience. These experiments provide a quantitative analysis of how sensory experience can enhance both reliability and temporal precision in neocortical neurons and provide a framework for testing specific hypotheses about the role of response variability in cortical function and the molecular mechanisms underlying this phenomenon.

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Received July 16, 2009; accepted Aug. 10, 2009.

Correspondence should be addressed to Alison L. Barth, Box 142, Mellon Institute, Carnegie Mellon University, 4400 Fifth Avenue, Pittsburgh, PA 15213. Email: barth{at}cmu.edu

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