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The Journal of Neuroscience, August 23, 2006, 26(34):8691-8701; doi:10.1523/JNEUROSCI.2478-06.2006

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Development/Plasticity/Repair
Major Effects of Sensory Experiences on the Neocortical Inhibitory Circuits

Yuanyuan Jiao,^1,2 Chunzhao Zhang,¹ Yuchio Yanagawa,³ and Qian-Quan Sun^1,2

¹Department of Zoology and Physiology and ²Neuroscience Program, University of Wyoming, Laramie, Wyoming 82071, and ³Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine and Solution-Oriented Research for Science and Technology, Japan Science and Technology Corporation, Maebashi 371-8511, Japan

Correspondence should be addressed to Dr. Qian-Quan Sun at the above address. Email: neuron{at}uwyo.edu

During postnatal development, sensory experiences play critical roles in the refinement of cortical connections. However, both the process of postnatal experience-dependent maturation of neocortical inhibitory networks and its underlying mechanisms remain elusive. Here, we examined the differential properties of intracortical inhibitory networks of layer IV in "sensory-spared" and "sensory-deprived" cortices of glutamate acid decarboxylase 67 (GAD67)–green fluorescent protein (GFP) (neo) and wild-type mouse. Our results showed that row D whisker trimming (WT) begun at postnatal day 7 (P7), but not after P15, induced a robust reduction of parvalbumin (PV) expression, measured by the PV/GFP ratio and PV cell densities, in the deprived barrels. WT also induced a robust reduction in the number of inhibitory perisomatic varicosities and synaptic GAD65/67 immunoreactivities in spiny neurons of the deprived barrels. Although the GAD65/67 expressions in interneurons were also downregulated in the deprived barrels, the GFP expression remained unchanged. Patch-clamp recording from spiny cells showed a 1.5-fold reduction of intracortical evoked IPSCs (eIPSCs) in deprived versus spared cortices. The reduction in eIPSCs occurred via changes in presynaptic properties and unitary IPSC amplitudes. Miniature IPSCs showed subtle but significant differences between the two experimental conditions. In addition, properties of the IPSCs in deprived barrels resemble those of IPSCs recorded in immature brains (P7). Together, these results suggest that the properties of local intracortical inhibitory networks are modified by sensory experiences. Perisomatic inhibition mediated by PV-positive basket cells is pruned by sensory deprivation.

Key words: development; plasticity; barrel cortex; interneuron; GABA; somatosensory

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Received April 10, 2006; revised July 10, 2006; accepted July 19, 2006.

Correspondence should be addressed to Dr. Qian-Quan Sun at the above address. Email: neuron{at}uwyo.edu

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