Anticipation across modalities in children and adults: Relating anticipatory alpha rhythm lateralization, reaction time, and executive function

• Published in: Developmental science Vol. 26; no. 1; pp. e13277 - n/a
• Main Authors: Meredith Weiss, Staci, Marshall, Peter J.
• Format: Journal Article
• Language: English
• Published: England Wiley 01-01-2023; Wiley Subscription Services, Inc; John Wiley and Sons Inc
• Subjects: Adolescent; Adult; alpha; Alpha Rhythm - physiology; anticipation; Anticipation, Psychological - physiology; Attention Control; Auditory Stimuli; Behavior Patterns; Brain Hemisphere Functions; Case Studies; Child; Children; Cognition & reasoning; Cognitive Ability; Comparative Analysis; Correlation; Cross-Sectional Studies; development; Diagnostic Tests; EEG; Electroencephalography; Executive Function; Hearing; Hemispheric laterality; Humans; Individual Differences; Lateral Dominance; multimodal; Nervous system; Neurosciences; Ontogeny; Oscillations; prediction; Reaction Time; Reaction Time - physiology; Rhythm; Sensory integration; Tactual Perception; Visual Perception; Visual Stimuli; Young Adult; Young Adults; prediction; development; multimodal; EEG; anticipation; alpha
• ISSN: 1363-755X; 1467-7687
• DOI: 10.1111/desc.13277

The development of the ability to anticipate—as manifested by preparatory actions and neural activation related to the expectation of an upcoming stimulus—may play a key role in the ontogeny of cognitive skills more broadly. This preregistered study examined anticipatory brain potentials and behavioral responses (reaction time; RT) to anticipated target stimuli in relation to individual differences in the ability to use goals to direct action (as indexed by measures of executive function; EF). A cross‐sectional investigation was conducted in 40 adults (aged 18–25 years) and 40 children (aged 6–8 years) to examine the association of changes in the amplitude of modality‐specific alpha‐range rhythms in the electroencephalogram (EEG) during anticipation of lateralized visual, tactile, or auditory stimuli with inter‐ and intraindividual variation in RT and EF. Children and adults exhibited contralateral anticipatory reductions in the mu rhythm and the visual alpha rhythm for tactile and visual anticipation, respectively, indicating modality and spatially specific attention allocation. Variability in within‐subject anticipatory alpha lateralization (the difference between contralateral and ipsilateral alpha power) was related to single‐trial RT. This relation was more prominent in adults than in children, and was not apparent for auditory stimuli. Multilevel models indicated that interindividual differences in anticipatory mu rhythm lateralization contributed to the significant association with variability in EF, but this was not the case for visual or auditory alpha rhythms. Exploratory microstate analyses were undertaken to cluster global field power (GFP) into a distribution‐free temporal analysis examining developmental differences across samples and in relation to RT and EF. Anticipation is suggested as a developmental bridge construct connecting neuroscience, behavior, and cognition, with anticipatory EEG oscillations being discussed as quantifiable and potentially malleable indicators of stimulus prediction.
Participants analyzed included 40 adults aged 18–20 and 40 children aged 6–8, who were cued with a sound that directed their attention to the location of an upcoming stimulus. The stimulus presented to the right or left of the participant in either the tactile, auditory or visual modalities and participants responded to the stimulus by pressing a foot pedal as quickly as possible. During this task, we recorded EEG brain activity and analyzed the power of a select band, alpha which oscillates from 8–12 Hz. Relative alpha power was calculated relative to baseline, averaged over the 500 ms prior to stimulus onset. Group averages for adults and children are displayed, with decreases in alpha power are indicated by blue, while increases are indicated in red. Adults show the most robust disengagement from the audiovisual cue, particularly at occipital sites and anticipatory decreases in alpha and mu power at contralateral central sites; anticipatory lateralization like this suggestions predictions are both specific to spatial location and sensory modality, especially when the expected stimulus was multi‐modal (visual or tactile). Children exhibit focal decreases in mu at contralateral central cites but exhibited less lateralization overall, such that their predictions were somewhat less spatially‐selective than adults, but still appear as modality‐specific. These differences in lateralization of alpha power per participant and trial were submitted for further analysis. Our multi‐level model examined variability between participants in executive function, as explained by each participant's reaction time and alpha power responses at the trial and individual level. Individual differences in executive function related to subject‐levelalpha lateralization, beyond trial‐level variability in reaction time. The magnitude of anticipatory mu was related to executive function but this differed in child and adults especially for anticipation of tactile stimuli, such that adults' α lateralization is positively associated with their executive function, while children's α lateralization is negatively associated with EF. This suggests adults and children might engage in different strategies for optimal prediction children who exhibit higher executive function might be more vigilant to unexpected stimuli, unlike adults with higher executive function, who seem to suppress processing at the uncued, unexpected spatial location.