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The Journal of Neuroscience, September 2, 2009, 29(35):10890-10899; doi:10.1523/JNEUROSCI.2012-09.2009

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Behavioral/Systems/Cognitive
Internally Mediated Developmental Desynchronization of Neocortical Network Activity

Peyman Golshani,¹ J. Tiago Gonçalves,¹ Sattar Khoshkhoo,¹ Ricardo Mostany,¹ Stelios Smirnakis,^3,4 and Carlos Portera-Cailliau^1,2

Departments of ¹Neurology and ²Neurobiology, David Geffen School of Medicine at University of California, Los Angeles, Los Angeles, California 90095, and Departments of ³Neurology and ⁴Neuroscience, Baylor College of Medicine, Houston, Texas 77030

Correspondence should be addressed to either Peyman Golshani or Carlos Portera-Cailliau, Department of Neurology, David Geffen School of Medicine at University of California, Los Angeles, 710 Westwood Plaza, Los Angeles, California 90095. Email: pgolshani{at}mednet.ucla.edu or Email: cpcailliau{at}mednet.ucla.edu

During neocortical development, neurons exhibit highly synchronized patterns of spontaneous activity, with correlated bursts of action potential firing dominating network activity. This early activity is eventually replaced by more sparse and decorrelated firing of cortical neurons, which modeling studies predict is a network state that is better suited for efficient neural coding. The precise time course and mechanisms of this crucial transition in cortical network activity have not been characterized in vivo. We used in vivo two-photon calcium imaging in combination with whole-cell recordings in both unanesthetized and anesthetized mice to monitor how spontaneous activity patterns in ensembles of layer 2/3 neurons of barrel cortex mature during postnatal development. We find that, as early as postnatal day 4, activity is highly synchronous within local clusters of neurons. At the end of the second postnatal week, neocortical networks undergo a transition to a much more desynchronized state that lacks a clear spatial structure. Strikingly, deprivation of sensory input from the periphery had no effect on the time course of this transition. Therefore, developmental desynchronization of spontaneous neuronal activity is a fundamental network transition in the neocortex that appears to be intrinsically generated.

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Received April 28, 2009; revised June 12, 2009; accepted July 24, 2009.

Correspondence should be addressed to either Peyman Golshani or Carlos Portera-Cailliau, Department of Neurology, David Geffen School of Medicine at University of California, Los Angeles, 710 Westwood Plaza, Los Angeles, California 90095. Email: pgolshani{at}mednet.ucla.edu or Email: cpcailliau{at}mednet.ucla.edu

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