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Cerebral Cortex Advance Access published online on November 13, 2006
Cerebral Cortex, 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

Article

Cortical Efferent Control of Subcortical Sensory Neurons by Synaptic Disinhibition

Christian Henneberger 1, Stephen J. Redman 2, and Rosemarie Grantyn 1 *

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

* To whom correspondence should be addressed.
Rosemarie Grantyn, E-mail: Rosemarie.Grantyn{at}charite.de


  Abstract

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.

Keywords: developmental plasticity; endocannabinoids; GABA release; mGluR; visual cortex.
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