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Cerebral Cortex Advance Access originally published online on November 13, 2006
Cerebral Cortex 2007 17(9):2039-2049; doi:10.1093/cercor/bhl112
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© The Author 2006. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Cortical Efferent Control of Subcortical Sensory Neurons by Synaptic Disinhibition

Christian Henneberger1, Stephen J. Redman2 and Rosemarie Grantyn1

1 Developmental and Sensory Neurophysiology, Institute of Neurophysiology, Johannes-Müller-Center for Physiology, Charité—University Medicine Berlin, Tucholskystr. 2, 10117 Berlin, Germany, 2 Movement and Memory Laboratory, John Curtin School of Medical Research, Australian National University, Canberra ACT 0200, Australia

Address correspondence to Prof. Dr R. Grantyn, Sensory and Developmental Physiology, Institute of Neurophysiology, Charité—University Medicine Berlin, Tucholskystr. 2, 10117 Berlin, Germany. Email: Rosemarie.Grantyn{at}charite.de.

A long-standing hypothesis predicts that pyramidal neurons of the cerebral cortex control the influx of sensory information at the level of primary sensory representations areas. Yet little is known about the cellular mechanisms governing selective attention to behaviorally relevant objects in space. Neurons in the superficial layers of the superior colliculus are notably involved in this process, and they are directly targeted by retinal and cortical afferents. To study long-term and short-term effects of the visual cortex (VC) on subcortical visual neurons we established an in vitro model of the developing cortico-tectal projection. To this end, cortical explants expressing Green Fluorescent Protein were allowed to form connections with non-labeled dissociated tectal neurons. The presence of VC explants led to an enhancement of tectal activity by 2 mechanisms. First, glutamatergic input was increased. Second, intrinsic GABAergic inhibition was suppressed. The latter effect was shown to be acute and mediated through postsynaptic metabotropic glutamate receptor activation, G-protein acitivity, and endocannabinoid receptor activation. The VC-induced disinhibition was readily reversed by application of an mGluR antagonist. However, high-frequency activation of the glutamatergic cortico-tectal input turned the labile disinhibition into a persistent suppression of inhibition.

Key Words: developmental plasticity • endocannabinoids • GABA release • mGluR • visual cortex


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