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Bogart, Luke Joseph

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Luke Joseph

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Bogart, Luke Joseph

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    Synaptic Specificity and Plasticity in Parvalbumin-Basket Cell Circuits
    (2015-09-29) Bogart, Luke Joseph; Murthy, Venkatesh N.; Turrigiano, Gina G.; Arlotta, Paola; Rudolph, Uwe
    Inhibitory interneurons regulate experience-dependent plasticity across brain regions. Perisomatic inhibition by fast-spiking, parvalbumin-positive basket cells (PV-cells) is central to these processes, but which synapses are key remains unknown. Here we show using immunohistochemistry that PV-input to pyramidal cells in layer 5 of primary visual cortex (V1) differs on a cell type-specific basis, with subcortically-projecting pyramidal cells more highly-innervated by PV-cells than callosally-projecting pyramidal cells. Surprisingly, the density of PV-inputs to either pyramidal cell-type was not changed by dark-rearing mice to adulthood, a classical manipulation that delays V1 plasticity. Instead, dark-rearing selectively reduced PV-inputs onto other PV-cells, which normally form highly-recurrent networks. To investigate the circuit-level basis of this plasticity, PV-cells in both normal and dark-reared mice were labeled by Brainbow. In both conditions, individual innervations of PV-cell bodies by PV-axons were mediated on average by just 2 boutons/axon, revealing that loss of inputs to dark-reared PV-cells results from decreased convergence within the PV-network. On a molecular level, PV-cells sorted from dark-reared mice exhibited a reduction in GABAA receptor α1-subunit mRNA, a marker of functionally-mature inhibition. In whole-cell recordings of dark-reared PV-cells in vitro, spontaneous inhibitory postsynaptic currents (sIPSCs) were broader than in light-reared controls, an effect not seen in pyramidal cells in which α1-level was unchanged. Optogenetics experiments revealed that PV-cell-mediated synaptic events exhibited broader currents selectively in PV-cells. Also, consistent with their loss of PV-inputs, the frequency of sIPSCs received by dark-reared PV-cells was markedly lower than in light-reared controls, with sIPSC amplitude decreased as well. We modeled the loss of fast, PV-inhibition onto PV-cells through conditional gene deletion of the α1-subunit from PV-cells. This did not physically disconnect PV-PV connections, but rather decreased the amplitude and broadened the decay of individual sIPSCs. α1-deletion alone was sufficient to extend plasticity in light-reared adult V1, implicating recurrent PV-inhibition in critical period regulation. Together, our results suggest that reorganization of this recurrent PV-cell network by early experience or gene mutation may contribute to aberrant plasticity and associated cognitive disorders more broadly.