Dynamic large-scale connectivity of intrinsic cortical oscillations supports adaptive listening in challenging conditions

PLoS Biol. 2021 Oct 11;19(10):e3001410. doi: 10.1371/journal.pbio.3001410. eCollection 2021 Oct.

Abstract

In multi-talker situations, individuals adapt behaviorally to this listening challenge mostly with ease, but how do brain neural networks shape this adaptation? We here establish a long-sought link between large-scale neural communications in electrophysiology and behavioral success in the control of attention in difficult listening situations. In an age-varying sample of N = 154 individuals, we find that connectivity between intrinsic neural oscillations extracted from source-reconstructed electroencephalography is regulated according to the listener's goal during a challenging dual-talker task. These dynamics occur as spatially organized modulations in power-envelope correlations of alpha and low-beta neural oscillations during approximately 2-s intervals most critical for listening behavior relative to resting-state baseline. First, left frontoparietal low-beta connectivity (16 to 24 Hz) increased during anticipation and processing of a spatial-attention cue before speech presentation. Second, posterior alpha connectivity (7 to 11 Hz) decreased during comprehension of competing speech, particularly around target-word presentation. Connectivity dynamics of these networks were predictive of individual differences in the speed and accuracy of target-word identification, respectively, but proved unconfounded by changes in neural oscillatory activity strength. Successful adaptation to a listening challenge thus latches onto two distinct yet complementary neural systems: a beta-tuned frontoparietal network enabling the flexible adaptation to attentive listening state and an alpha-tuned posterior network supporting attention to speech.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Alpha Rhythm / physiology
  • Auditory Perception / physiology*
  • Behavior
  • Beta Rhythm / physiology
  • Brain Mapping
  • Cerebral Cortex / physiology*
  • Electroencephalography
  • Female
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Nerve Net / physiology*
  • Rest / physiology
  • Task Performance and Analysis