Visual experience sculpts whole-cortex spontaneous infraslow activity patterns through an Arc-dependent mechanism

Proc Natl Acad Sci U S A. 2017 Nov 14;114(46):E9952-E9961. doi: 10.1073/pnas.1711789114. Epub 2017 Oct 30.

Abstract

Decades of work in experimental animals has established the importance of visual experience during critical periods for the development of normal sensory-evoked responses in the visual cortex. However, much less is known concerning the impact of early visual experience on the systems-level organization of spontaneous activity. Human resting-state fMRI has revealed that infraslow fluctuations in spontaneous activity are organized into stereotyped spatiotemporal patterns across the entire brain. Furthermore, the organization of spontaneous infraslow activity (ISA) is plastic in that it can be modulated by learning and experience, suggesting heightened sensitivity to change during critical periods. Here we used wide-field optical intrinsic signal imaging in mice to examine whole-cortex spontaneous ISA patterns. Using monocular or binocular visual deprivation, we examined the effects of critical period visual experience on the development of ISA correlation and latency patterns within and across cortical resting-state networks. Visual modification with monocular lid suturing reduced correlation between left and right cortices (homotopic correlation) within the visual network, but had little effect on internetwork correlation. In contrast, visual deprivation with binocular lid suturing resulted in increased visual homotopic correlation and increased anti-correlation between the visual network and several extravisual networks, suggesting cross-modal plasticity. These network-level changes were markedly attenuated in mice with genetic deletion of Arc, a gene known to be critical for activity-dependent synaptic plasticity. Taken together, our results suggest that critical period visual experience induces global changes in spontaneous ISA relationships, both within the visual network and across networks, through an Arc-dependent mechanism.

Keywords: activity-regulated cytoskeleton-associated protein; functional connectivity; infraslow activity; visual critical period.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / physiology
  • Brain Mapping
  • Cerebral Cortex / physiology
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / physiology*
  • Female
  • Gene Deletion
  • Gene Expression Profiling
  • Genotype
  • Humans
  • Image Processing, Computer-Assisted
  • Learning*
  • Life Change Events*
  • Magnetic Resonance Imaging
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Models, Animal
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / physiology*
  • Neuronal Plasticity / genetics*
  • Neuronal Plasticity / physiology*
  • Sensory Deprivation / physiology
  • Visual Cortex / physiology*

Substances

  • Cytoskeletal Proteins
  • Nerve Tissue Proteins
  • activity regulated cytoskeletal-associated protein