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The Journal of Neuroscience, July 30, 2003, 23(17):6695-6702

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Rapid Critical Period Induction by Tonic Inhibition in Visual Cortex

Youichi Iwai,¹ Michela Fagiolini,¹ Kunihiko Obata,² and Takao K. Hensch¹

¹Laboratory for Neuronal Circuit Development, The Institute of Physical and Chemical Research (RIKEN) Brain Science Institute, Saitama 351-0198, Japan, and ²Laboratory for Neurochemistry, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585 Japan

Mice lacking a synaptic isoform of glutamic acid decarboxylase (GAD65) do not exhibit ocular dominance plasticity unless an appropriate level of GABAergic transmission is restored by direct infusion of benzodiazepines into the brain. To better understand how intracortical inhibition triggers experience-dependent changes, we dissected the precise timing requirement for GABA function in the monocular deprivation (MD) paradigm.

Diazepam (DZ) or vehicle solution was infused daily before and/or during 4 d of MD in GAD65 knock-out mice. Extracellular single-unit recordings from the binocular zone of visual cortex were performed at the end of deprivation. We found that a minimum treatment of 2 d near the beginning of MD was sufficient to fully activate plasticity but did not need to overlap the deprivation per se. Extended delay after DZ infusion eventually led to loss of plasticity accompanied by improved intrinsic inhibitory circuit function. Two day DZ treatment just after eye opening similarly closed the critical period prematurely in wild-type mice.

Raising wild-type mice in complete darkness from birth delayed the peak sensitivity to MD as in other mammals. Interestingly, 2 d DZ infusion in the dark also closed the critical period, whereas equally brief light exposure during dark-rearing had no such effect. Thus, enhanced tonic signaling through GABA_A receptors rapidly creates a milieu for plasticity within neocortex capable of triggering a critical period for ocular dominance independent of visual experience itself.

Key words: GAD65; dark-rearing; GABA; diazepam; critical period; visual cortex

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Received Dec. 16, 2002; revised Apr. 29, 2003; accepted May. 30, 2003.

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