Functional connectivity patterns predict naturalistic viewing versus rest across development

Neuroimage. 2021 Apr 1:229:117630. doi: 10.1016/j.neuroimage.2020.117630. Epub 2021 Jan 2.

Abstract

Cognitive states, such as rest and task engagement, share an 'intrinsic' functional network organization that is subject to minimal variation over time and yields stable signatures within an individual. Importantly, there are also transient state-specific functional connectivity (FC) patterns that vary across neural states. Here, we examine functional brain organization differences that underlie distinct states in a cross-sectional developmental sample. We compare FC fMRI data acquired during naturalistic viewing (i.e., movie-watching) and resting-state paradigms in a large cohort of 157 children and young adults aged 6-20. Naturalistic paradigms are commonly implemented in pediatric research because they maintain the child's attention and contribute to reduced head motion. It remains unknown, however, to what extent the brain-wide functional network organization is comparable during movie-watching and rest across development. Here, we identify a widespread FC pattern that predicts whether individuals are watching a movie or resting. Specifically, we develop a model for prediction of multilevel neural effects (termed PrimeNet), which can with high reliability distinguish between movie-watching and rest irrespective of age and that generalizes across movies. In turn, we characterize FC patterns in the most predictive functional networks for movie-watching versus rest and show that these patterns can indeed vary as a function of development. Collectively, these effects highlight a 'core' FC pattern that is robustly associated with naturalistic viewing, which also exhibits change across age. These results, focused here on naturalistic viewing, provide a roadmap for quantifying state-specific functional neural organization across development, which may reveal key variation in neurodevelopmental trajectories associated with behavioral phenotypes.

Keywords: Brain state; Development; Functional connectivity; Movie-watching; Naturalistic imaging; Resting-state.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adolescent
  • Brain / diagnostic imaging
  • Brain / growth & development*
  • Child
  • Databases, Factual / trends
  • Female
  • Forecasting
  • Humans
  • Magnetic Resonance Imaging / methods*
  • Magnetic Resonance Imaging / trends
  • Male
  • Motion Pictures / trends
  • Nerve Net / diagnostic imaging
  • Nerve Net / growth & development*
  • Photic Stimulation / methods*
  • Rest / physiology*
  • Rest / psychology
  • Visual Perception / physiology*
  • Young Adult