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      Ultrastructural and optogenetic dissection of V1 corticotectal terminal synaptic properties

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          Abstract

          The superior colliculus (SC) is a major site of sensorimotor integration in which sensory inputs are processed to initiate appropriate motor responses. Projections from the primary visual cortex (V1) to the SC have been shown to exert a substantial influence on visually-induced behavior, including “freezing”. However, it is unclear how V1 corticotectal terminals affect SC circuits to mediate these effects. To investigate this, we used anatomical and optogenetic techniques to examine the synaptic properties of V1 corticotectal terminals. Electron microscopy revealed that V1 corticotectal terminals labeled by anterograde transport primarily synapse (93%) on dendrites that do not contain gamma amino butyric acid (GABA). This preference was confirmed using optogenetic techniques to photoactivate V1 corticotectal terminals in slices of the SC maintained in vitro. In a mouse line in which GABAergic SC interneurons express green fluorescent protein (GFP), few GFP-labeled cells (11%) responded to activation of corticotectal terminals. In contrast, 67% of nonGABAergic cells responded to activation of V1 corticotectal terminals. Biocytin-labeling of recorded neurons revealed that wide-field vertical (WFV) and non-WFV cells were activated by V1 corticotectal inputs. However, WFV cells were activated in the most uniform manner; 85% of these cells responded with excitatory postsynaptic potentials (EPSPs) that maintained stable amplitudes when activated with light trains at 1–20HZ. In contrast, in the majority of non-WFV cells, the amplitude of evoked EPSPs varied across trials. Our results suggest that V1 corticotectal projections may initiate freezing behavior via uniform activation of the WFV cells, which project to the pulvinar nucleus.

          Graphical Abstract Legend

          Electron microscopy revealed that the majority of corticotectal terminals (purple overlay) contact (arrow) small nonGABAergic dendrites (green overlay). Excitatory postsynaptic responses (green traces) to optogenetic activation of corticotectal terminals (purple) were recorded in vitro in a variety of cell types; wide field vertical cells (green neuron) displayed the most uniform responses.

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          Author and article information

          Journal
          0406041
          4668
          J Comp Neurol
          J. Comp. Neurol.
          The Journal of comparative neurology
          0021-9967
          1096-9861
          2 October 2018
          04 December 2018
          01 March 2019
          01 March 2020
          : 527
          : 4
          : 833-842
          Affiliations
          Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY, 40292 For submission to Journal of Comparative Neurology
          Author notes
          [* ]Correspondence: Martha Bickford, martha.bickford@ 123456louisville.edu , Department of Anatomical Sciences & Neurobiology, University of Louisville, School of Medicine, 511 South Floyd, Room 111, Louisville, KY 40202
          Article
          PMC6333520 PMC6333520 6333520 nihpa1507823
          10.1002/cne.24538
          6333520
          30255935
          224b8641-835d-4a4a-a16e-f93d637d8ca9
          History
          Categories
          Article

          RRID: nif-000-30467,RRID:AB_477652,RRID:AB_91337,RRID:AB_10015246,channelrhodopsin,GAD67,GABA,excitatory postsynaptic potential,electron microscopy,widefield vertical,synapse,superior colliculus

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