Closed-Loop Neurofeedback of α Synchrony during Goal-Directed Attention

J Neurosci. 2021 Jun 30;41(26):5699-5710. doi: 10.1523/JNEUROSCI.3235-20.2021. Epub 2021 May 21.

Abstract

α Oscillations in sensory cortex, under frontal control, desynchronize during attentive preparation. Here, in a selective attention study with simultaneous EEG in humans of either sex, we first demonstrate that diminished anticipatory α synchrony between the mid-frontal region of the dorsal attention network and ventral visual sensory cortex [frontal-sensory synchrony (FSS)] significantly correlates with greater task performance. Then, in a double-blind, randomized controlled study in healthy adults, we implement closed-loop neurofeedback (NF) of the anticipatory α FSS signal over 10 d of training. We refer to this closed-loop experimental approach of rapid NF integrated within a cognitive task as cognitive NF (cNF). We show that cNF results in significant trial-by-trial modulation of the anticipatory α FSS measure during training, concomitant plasticity of stimulus-evoked α/θ responses, as well as transfer of benefits to response time (RT) improvements on a standard test of sustained attention. In a third study, we implement cNF training in children with attention deficit hyperactivity disorder (ADHD), replicating trial-by-trial modulation of the anticipatory α FSS signal as well as significant improvement of sustained attention RTs. These first findings demonstrate the basic mechanisms and translational utility of rapid cognitive-task-integrated NF.SIGNIFICANCE STATEMENT When humans prepare to attend to incoming sensory information, neural oscillations in the α band (8-14 Hz) undergo desynchronization under the control of prefrontal cortex. Here, in an attention study with electroencephalography, we first show that frontal-sensory synchrony (FSS) of α oscillations during attentive preparation significantly correlates with task performance. Then, in a randomized controlled study in healthy adults, we show that neurofeedback (NF) training of this α FSS signal within the attention task is feasible. We show that this rapid cognitive NF (cNF) approach engenders plasticity of stimulus-evoked neural responses, and improves performance on a standard test of sustained attention. In a final study, we implement cNF in children with attention deficit hyperactivity disorder (ADHD), replicating the improvement of sustained attention found in adults.

Keywords: attention deficit hyperactivity disorder; brain computer interface; cognitive neurofeedback; dorsal attention network; neuroplasticity; synchrony.

Publication types

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

MeSH terms

  • Adult
  • Alpha Rhythm / physiology*
  • Attention / physiology*
  • Attention Deficit Disorder with Hyperactivity* / physiopathology
  • Cerebral Cortex / physiology*
  • Child
  • Double-Blind Method
  • Female
  • Goals
  • Humans
  • Male
  • Neurofeedback / methods*
  • Neurofeedback / physiology
  • Neuronal Plasticity / physiology
  • Reaction Time / physiology