Multiscale Imaging Reveals Aberrant Functional Connectome Organization and Elevated Dorsal Striatal Arc Expression in Advanced Age

eNeuro. 2019 Dec 26;6(6):ENEURO.0047-19.2019. doi: 10.1523/ENEURO.0047-19.2019. Print 2019 Nov/Dec.

Abstract

The functional connectome reflects a network architecture enabling adaptive behavior that becomes vulnerable in advanced age. The cellular mechanisms that contribute to altered functional connectivity in old age, however, are not known. Here we used a multiscale imaging approach to link age-related changes in the functional connectome to altered expression of the activity-dependent immediate-early gene Arc as a function of training to multitask on a working memory (WM)/biconditional association task (BAT). Resting-state fMRI data were collected from young and aged rats longitudinally at three different timepoints during cognitive training. After imaging, rats performed the WM/BAT and were immediately sacrificed to examine expression levels of Arc during task performance. Aged behaviorally impaired, but not young, rats had a subnetwork of increased connectivity between the anterior cingulate cortex (ACC) and dorsal striatum (DS) that was correlated with the use of a suboptimal response-based strategy during cognitive testing. Moreover, while young rats had stable rich-club organization across three scanning sessions, the rich-club organization of old rats increased with cognitive training. In a control group of young and aged rats that were longitudinally scanned at similar time intervals, but without cognitive training, ACC-DS connectivity and rich-club organization did not change between scans in either age group. These findings suggest that aberrant large-scale functional connectivity in aged animals is associated with altered cellular activity patterns within individual brain regions.

Keywords: anterior cingulate cortex; functional connectivity; graph theory; prefrontal cortex; working memory.

Publication types

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

MeSH terms

  • Aging / metabolism
  • Aging / physiology*
  • Animals
  • Association Learning / physiology*
  • Behavior, Animal / physiology*
  • Connectome*
  • Cytoskeletal Proteins / metabolism*
  • Gyrus Cinguli / diagnostic imaging
  • Gyrus Cinguli / physiology*
  • Magnetic Resonance Imaging
  • Memory, Short-Term / physiology*
  • Neostriatum / diagnostic imaging
  • Neostriatum / metabolism
  • Neostriatum / physiology*
  • Nerve Tissue Proteins / metabolism*
  • Practice, Psychological*
  • Rats

Substances

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