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The maturation of GABAergic transmission in visual cortex requires endocannabinoid-mediated LTD of inhibitory inputs during a critical period.

ABSTRACT: Endocannabinoids are widely regarded as negative modulators of presynaptic release. Here, we present evidence that in visual cortex endocannabinoids are crucial for the maturation of GABAergic release. We found that between eye opening and puberty, release changes from an immature state with high release probability, short-term depression (STD), and high release variability during irregular patterned activity, to a mature state with reduced release probability, STD, and variability. This transition requires visual experience and stimulation of CB1 cannabinoid receptors as it is mimicked by administration of CB1 agonists, blocked by antagonists, and is absent in CB1R KO mice. In immature slices, activation of CB1 receptors induces long-term depression of inhibitory responses (iLTD) and a reduction in STD and response variability. Based on these findings, we propose that visually induced endocannabinoid-dependent iLTD mediates the developmental decrease in release probability, STD, and response variability, which are characteristic of maturation of cortical GABAergic inhibition.

SUBMITTER: Jiang B

PROVIDER: S-EPMC2897012 | biostudies-literature | 2010 Apr

REPOSITORIES: biostudies-literature

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The maturation of GABAergic transmission in visual cortex requires endocannabinoid-mediated LTD of inhibitory inputs during a critical period.

Jiang Bin B Huang Shiyong S de Pasquale Roberto R Millman Daniel D Song Lihua L Lee Hey-Kyoung HK Tsumoto Tadaharu T Kirkwood Alfredo A

Neuron 20100401 2

Endocannabinoids are widely regarded as negative modulators of presynaptic release. Here, we present evidence that in visual cortex endocannabinoids are crucial for the maturation of GABAergic release. We found that between eye opening and puberty, release changes from an immature state with high release probability, short-term depression (STD), and high release variability during irregular patterned activity, to a mature state with reduced release probability, STD, and variability. This transit ...[more]

PMID: 20435001

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Project description:Unified visual perception relies on the integration of bottom-up and top-down inputs in the primary visual cortex (V1), with top-down inputs known to provide behavior-related modulation on visual processing. However, the organization of top-down inputs in V1 remains unclear. Here, using optogenetics-assisted circuit mapping, we characterized how multiple top-down inputs from higher-order cortical and thalamic areas engage excitatory and inhibitory neurons in V1. Systematic layer- and cell-type-specific profiling of the innervation properties of top-down inputs ultimately revealed that each top-down input employs a unique laminar profile when innervating V1. These profiles partially overlap in superficial layers, bypass layer 4 (L4), and clearly segregate upon reaching deep layers. Specifically, inputs from the medial secondary visual cortex (V2M) and anterior cingulate cortex (ACA) preferentially activate L6 neurons, while inputs from the ventrolateral orbitofrontal cortex (ORBvl) and lateral posterior thalamic nucleus (LP) activate L5 neurons. Having defined the inputs, we conducted independent optogenetic activation studies and discovered that ORBvl and LP inputs selectively activate two types of pyramidal neurons (Pyrs) in L5: Pyr <-- ORBvl and Pyr <-- LP neurons, each with specific electrophysiological properties and gene expression profiles. Retrograde mapping subsequently revealed that Pyr <-- ORBvl neurons preferentially innervate subcortical areas and Pyr <-- LP neurons innervate cortical areas, indicating parallel processing of ORBvl and LP inputs in Pyr-type-specific subnetworks. Further, we found mutual inhibition between these two subnetworks, as LP inputs indirectly inhibit Pyr <-- ORBvl neurons and ORBvl inputs inhibit Pyr <-- LP neurons through local inhibitory neurons. Our study thus deepens understanding of the neuronal mechanisms involved in top-down modulation of visual processing by providing a valuable resource characterizing the layer- and cell-type-specific organization of top-down inputs in V1 and by revealing that L5 Pyr-type-specific subnetworks engage in parallel processing of corticocortical and thalamocortical top-down inputs.

Dataset Information

The maturation of GABAergic transmission in visual cortex requires endocannabinoid-mediated LTD of inhibitory inputs during a critical period.

Publications

The maturation of GABAergic transmission in visual cortex requires endocannabinoid-mediated LTD of inhibitory inputs during a critical period.

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