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      Columnar Lesions in Barrel Cortex Persistently Degrade Object Location Discrimination Performance

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          Abstract

          Primary sensory cortices display functional topography, suggesting that even small cortical volumes may underpin perception of specific stimuli. Traditional loss-of-function approaches have a relatively large radius of effect (>1 mm), and few studies track recovery following loss-of-function perturbations. Consequently, the behavioral necessity of smaller cortical volumes remains unclear. In the mouse primary vibrissal somatosensory cortex (vS1), “barrels” with a radius of ∼150 μm receive input predominantly from a single whisker, partitioning vS1 into a topographic map of well defined columns. Here, we train animals implanted with a cranial window over vS1 to perform single-whisker perceptual tasks. We then use high-power laser exposure centered on the barrel representing the spared whisker to produce lesions with a typical volume of one to two barrels. These columnar-scale lesions impair performance in an object location discrimination task for multiple days without disrupting vibrissal kinematics. Animals with degraded location discrimination performance can immediately perform a whisker touch detection task with high accuracy. Animals trained de novo on both simple and complex whisker touch detection tasks showed no permanent behavioral deficits following columnar-scale lesions. Thus, columnar-scale lesions permanently degrade performance in object location discrimination tasks.

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          The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex.

          Local microcircuits within neocortical columns form key determinants of sensory processing. Here, we investigate the excitatory synaptic neuronal network of an anatomically defined cortical column, the C2 barrel column of mouse primary somatosensory cortex. This cortical column is known to process tactile information related to the C2 whisker. Through multiple simultaneous whole-cell recordings, we quantify connectivity maps between individual excitatory neurons located across all cortical layers of the C2 barrel column. Synaptic connectivity depended strongly upon somatic laminar location of both presynaptic and postsynaptic neurons, providing definitive evidence for layer-specific signaling pathways. The strongest excitatory influence upon the cortical column was provided by presynaptic layer 4 neurons. In all layers we found rare large-amplitude synaptic connections, which are likely to contribute strongly to reliable information processing. Our data set provides the first functional description of the excitatory synaptic wiring diagram of a physiologically relevant and anatomically well-defined cortical column at single-cell resolution.
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            A Suite of Transgenic Driver and Reporter Mouse Lines with Enhanced Brain-Cell-Type Targeting and Functionality

            Modern genetic approaches are powerful in providing access to diverse cell types in the brain and facilitating the study of their function. Here, we report a large set of driver and reporter transgenic mouse lines, including 23 new driver lines targeting a variety of cortical and subcortical cell populations and 26 new reporter lines expressing an array of molecular tools. In particular, we describe the TIGRE2.0 transgenic platform and introduce Cre-dependent reporter lines that enable optical physiology, optogenetics, and sparse labeling of genetically defined cell populations. TIGRE2.0 reporters broke the barrier in transgene expression level of single-copy targeted-insertion transgenesis in a wide range of neuronal types, along with additional advantage of a simplified breeding strategy compared to our first-generation TIGRE lines. These novel transgenic lines greatly expand the repertoire of high-precision genetic tools available to effectively identify, monitor, and manipulate distinct cell types in the mouse brain.
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              Cortical layer–specific critical dynamics triggering perception

              Perceptual experiences may arise from neuronal activity patterns in mammalian neocortex. We probed mouse neocortex during visual discrimination using a red-shifted channelrhodopsin (ChRmine, discovered through structure-guided genome mining) alongside multiplexed multiphoton-holography (MultiSLM), achieving control of individually-specified neurons spanning large cortical volumes with millisecond precision. Stimulating a critical number of stimulus-orientation-selective neurons drove widespread recruitment of functionally-related neurons, a process enhanced by (but not requiring) orientation-discrimination task learning. Optogenetic targeting of orientation-selective ensembles elicited correct behavioral discrimination. Cortical layer specific-dynamics were apparent, as emergent neuronal activity asymmetrically propagated from layer-2/3 to layer-5, and smaller layer-5 ensembles were as effective as larger layer-2/3 ensembles in eliciting orientation discrimination behavior. Population dynamics emerging after optogenetic stimulation both correctly predicted behavior and resembled natural neural representations of visual stimuli.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                31 October 2022
                11 November 2022
                Nov-Dec 2022
                : 9
                : 6
                : ENEURO.0393-22.2022
                Affiliations
                [1]Center for Neural Science, New York University , New York, New York 10003
                Author notes

                The authors declare no competing financial interests.

                Author contributions: L.R. and S.P. designed research; L.R., M.L., A.S.-Y, S.C., and R.P. performed research; L.R., M.L., and S.P. analyzed data; L.R. and S.P. wrote the paper.

                This work was supported by the Whitehall Foundation and the National Institutes of Health (Grant R01-NS-117536).

                Correspondence should be addressed to Simon Peron at speron@ 123456nyu.edu .
                Author information
                https://orcid.org/0000-0001-5188-2945
                https://orcid.org/0000-0001-8265-6940
                Article
                eN-NWR-0393-22
                10.1523/ENEURO.0393-22.2022
                9665881
                36316120
                3fffa09e-e7b1-46fb-918d-985a47939568
                Copyright © 2022 Ryan et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 19 September 2022
                : 3 October 2022
                : 21 October 2022
                Page count
                Figures: 8, Tables: 1, Equations: 0, References: 52, Pages: 13, Words: 00
                Funding
                Funded by: HHS | National Institutes of Health (NIH), doi 10.13039/100000002;
                Award ID: R01NS117536
                Categories
                8
                Research Article: New Research
                Sensory and Motor Systems
                Custom metadata
                November/December 2022

                barrel cortex,lesion,perception
                barrel cortex, lesion, perception

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