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Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs

Abstract

Distinct classes of GABAergic synapses target restricted subcellular domains, thereby differentially regulating the input, integration and output of principal neurons, but the underlying mechanism for such synapse segregation is unclear. Here we show that the distributions of two major classes of GABAergic synapses along the perisomatic and dendritic domains of pyramidal neurons were indistinguishable between primary visual cortex in vivo and cortical organotypic cultures. Therefore, subcellular synapse targeting is independent of thalamic input and probably involves molecular labels and experience-independent forms of activity.

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Figure 1: Bitufted and basket interneurons preferentially target the dendritic and perisomatic domains of pyramidal neurons in visual cortex.
Figure 2: Perisomatic and dendritic-restricted GABAergic innervation develop in visual cortical organotypic cultures.
Figure 3: Subcellular domain-restricted distributions of GABAergic synapses develop in the absence of thalamic input.

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Acknowledgements

We thank Tim Pal for technical assistance. This work was supported by the Whitehall Foundation and the National Institutes of Health (RO1 EY 13564-01). G.D.C. is a Long Term EMBO Fellow. Z.J.H. is a Pew Scholar.

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Correspondence to Z Josh Huang.

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Supplementary information

Supplementary Fig. 1

Two transgenic reporter lines allow visualization of defined interneurons classes. Left panel. In GIN transgenic mice, GFP labeled cells (green) colocalize with Somatostatin (SOM, red), a marker for bitufted interneurons. Right panel. In G42 transgenic mice, GFP expressing cells colocalize with Parvalbumin (PV, red), a marker for basket interneurons. (PDF 109 kb)

Supplementary Fig. 2

Experimental protocol. a) Schematic representation of experimental methods. GABAergic interneurons are labeled using transgenic mice expressing GFP in either PV positive basket interneurons (G42) or SOM positive bitufted interneurons (GIN). Pyramidal cells are labeled with TexasRed-conjugated dextran by single cell electroporation under infrared DIC guidance. b) Contacts between GFP labeled GABAergic axons and pyramidal cell soma are evaluated for each single bouton by quantifying the overlap between green and red signal in three dimensions. B1 shows a single xy focal plane of a 2-photon stack. Arrowhead indicates one putative contact between the GABAergic axon and the pyramidal soma. B2 shows the yz plane from the same stack (outlined in red in B1). Arrowhead indicates the same contact between the GFP-labeled GABAergic bouton and the pyramidal soma as in b1. c) Putative contacts between GFP labeled axons and pyramidal dendrite are evaluated by plotting the red and green signal fluorescence intensity along a line across the juxtaposition of the dendrite and a bouton in the focal plane in which the green signal is higher (c1). Fluorescent intensity plot along the line in c1 (arrows) is shown in c2. A contact is defined as such when the overlap between the green and red curves (from which background level are subtracted) is at least 500 nm (distance between arrowheads in c2). (PDF 118 kb)

Supplementary Fig. 3

Anatomically identified GFP-positive boutons correspond to synaptic site. a-b) GFP positive boutons (arrowheads) from GIN (a, middle panel) and G42 (b, middle panel) cortical slices colocalize with GAD65 immunoreactivity (left panels, red). Images are projections of 3 confocal optical sections 0.7 mm apart. Scale bar: 5 μm. c) A bitufted interneuron bouton containing dark DAB precipitate, indicating the presence of GFP, is confirmed to be a presynaptic terminal of a symmetric synapse (arrows) on a dendritic spine(star) by immuno-EM. Scale bar: 0.5μm. d) A basket interneuron bouton (outlined by dashed lines) containing dark DAB precipitate, indicating the presence of GFP, is confirmed to be a presynaptic terminal of a symmetric synapse (arrow) on a cell soma (outlined by arrowheads) by immuno-EM. Scale bar: 0.5 μm. (PDF 256 kb)

Supplementary Methods (PDF 31 kb)

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Cristo, G., Wu, C., Chattopadhyaya, B. et al. Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs. Nat Neurosci 7, 1184–1186 (2004). https://doi.org/10.1038/nn1334

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