title: Vision loss shifts the balance of feedforward and intracortical circuits in opposite directions in mouse primary auditory and visual cortices.
abstract: Loss of a sensory modality leads to widespread changes in synaptic function across sensory cortices, which are thought to be the basis for cross-modal adaptation. Previous studies suggest that experience-dependent cross-modal regulation of the spared sensory cortices may be mediated by changes in cortical circuits. Here, we report that loss of vision, in the form of dark exposure (DE) for 1 week, produces laminar-specific changes in excitatory and inhibitory circuits in the primary auditory cortex (A1) of adult mice to promote feedforward (FF) processing and also strengthens intracortical inputs to primary visual cortex (V1). Specifically, DE potentiated FF excitatory synapses from layer 4 (L4) to L2/3 in A1 and recurrent excitatory inputs in A1-L4 in parallel with a reduction in the strength of lateral intracortical excitatory inputs to A1-L2/3. This suggests a shift in processing in favor of FF information at the expense of intracortical processing. Vision loss also strengthened inhibitory synaptic function in L4 and L2/3 of A1, but via laminar specific mechanisms. In A1-L4, DE specifically potentiated the evoked synaptic transmission from parvalbumin-positive inhibitory interneurons to principal neurons without changes in spontaneous miniature IPSCs (mIPSCs). In contrast, DE specifically increased the frequency of mIPSCs in A1-L2/3. In V1, FF excitatory inputs were unaltered by DE, whereas lateral intracortical connections in L2/3 were strengthened, suggesting a shift toward intracortical processing. Our results suggest that loss of vision produces distinct circuit changes in the spared and deprived sensory cortices to shift between FF and intracortical processing to allow adaptation.
authors.affiliation: Solomon H. Snyder Department of Neuroscience, Zanvyl Krieger Mind/Brain Institute, and.
authors.forename: Emily
authors.initials: E
authors.lastname: Petrus
authors.affiliation: Cell, Molecular, Developmental Biology, and Biophysics Graduate Program, Johns Hopkins University, Baltimore, Maryland 21218, and.
authors.forename: Gabriela
authors.initials: G
authors.lastname: Rodriguez
authors.affiliation: Solomon H. Snyder Department of Neuroscience, Zanvyl Krieger Mind/Brain Institute, and.
authors.forename: Ryan
authors.initials: R
authors.lastname: Patterson
authors.affiliation: Cell, Molecular, Developmental Biology, and Biophysics Graduate Program, Johns Hopkins University, Baltimore, Maryland 21218, and.
authors.forename: Blaine
authors.initials: B
authors.lastname: Connor
authors.affiliation: Department of Biology, University of Maryland, College Park, Maryland 20742.
authors.forename: Patrick O
authors.identifier: http://orcid.org/0000-0002-7529-5435
authors.initials: PO
authors.lastname: Kanold
authors.affiliation: Solomon H. Snyder Department of Neuroscience, Zanvyl Krieger Mind/Brain Institute, and Cell, Molecular, Developmental Biology, and Biophysics Graduate Program, Johns Hopkins University, Baltimore, Maryland 21218, and heykyounglee@jhu.edu.
authors.forename: Hey-Kyoung
authors.identifier: http://orcid.org/0000-0002-5554-983X
authors.initials: HK
authors.lastname: Lee
mesh_terms: D000818:Animals; D001303:Auditory Cortex / Q000166:cytology* / Q000502:physiology; D000075402:Channelrhodopsins; D004305:Dose-Response Relationship, Drug; D019706:Excitatory Postsynaptic Potentials / Q000235:genetics / Q000502:physiology; D005260:Female; D066298:In Vitro Techniques; D008164:Luminescent Proteins / Q000235:genetics / Q000378:metabolism; D008239:Lysine / Q000031:analogs & derivatives / Q000378:metabolism; D008297:Male; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D009415:Nerve Net / Q000502:physiology*; D009434:Neural Pathways / Q000502:physiology*; D010320:Parvalbumins / Q000235:genetics / Q000378:metabolism; D010775:Photic Stimulation; D012683:Sensory Deprivation / Q000502:physiology*; D013569:Synapses / Q000502:physiology; D009435:Synaptic Transmission; D014793:Visual Cortex / Q000166:cytology* / Q000502:physiology*; D000097573:Red Fluorescent Protein
chemical_list: D000075402:Channelrhodopsins; D008164:Luminescent Proteins; D008239:Lysine; D010320:Parvalbumins; D000097573:Red Fluorescent Protein; C013411:biocytin
keywords: circuit plasticity; cortical plasticity; cross-modal plasticity; excitatory synaptic transmission; inhibitory synaptic transmission