Spectral signatures of cross-modal attentional control in the adolescent brain and their link with physical activity and aerobic fitness levels

Top–down attentional control seems to increase and suppress the activity of sensory cortices for relevant stimuli and to suppress activity for irrelevant ones. Higher physical activity (PA) and aerobic fitness (AF) levels have been associated with improved attention, but most studies have focused on unimodal tasks (e.g., visual stimuli only). The impact of higher PA or AF levels on the ability of developing brains to focus on certain stimuli while ignoring distractions remains unknown. The aim of this study was to examine the neural processes in visual and auditory sensory cortices during a cross-modal attention–allocation task using magnetoencephalography in 13–16-year-old adolescents (n = 51). During continuous and simultaneous visual (15 Hz) and auditory (40 Hz) noise-tagging stimulation, participants attended to either visual or auditory targets appearing on their left or right sides. High and low PA groups were formed based on seven-day accelerometer measurements, and high and low AF groups were determined based on the 20-m shuttle-run test. Steady-state (evoked) responses to the visual stimulus were observed in all the adolescents in the primary visual cortex, but some did not show responses in the primary auditory cortices to the auditory stimulus. The adolescents with auditory-tag-driven signals in the left temporal cortex were older than those who did not show responses. Visual cortices showed enhanced visual-tag-related activity with attention, but there was no cross-modal effect, perhaps due to the developmental effect observed in the temporal areas. The visual-tag-related responses in the occipital cortex were enhanced in the higher-PA group, irrespective of task demands. In summary, sensory cortices are unequally involved in cross-modal attention in the adolescent brain. This involvement seems to be enhanced by attention. Higher PA seems to be associated with a specific visual engagement benefit in the adolescent brain. Highlights - Visual and auditory cortices’ engagement differs in cross-modal processing in adolescence. - Adolescents with responses in the left temporal cortex are older than those without responses. - Physical activity, but not aerobic fitness, is associated with visual engagement benefits in the adolescent brain.

[1]  G. Ghose,et al.  Selective attention sharpens population receptive fields in human auditory cortex , 2022, Cerebral cortex.

[2]  R. Salmelin,et al.  Attentional modulation of interhemispheric (a)symmetry in children with developmental language disorder , 2022, Scientific Reports.

[3]  T. Parviainen,et al.  Meggie – easy-to-use graphical user interface for M/EEG analysis based on MNE-python , 2022, bioRxiv.

[4]  Yu-Kai Chang,et al.  Cardiorespiratory fitness is associated with sustained neurocognitive function during a prolonged inhibitory control task in young adults: An ERP study. , 2022, Psychophysiology.

[5]  R. Zatorre,et al.  Supramodality of neural entrainment: Rhythmic visual stimulation causally enhances auditory working memory performance , 2022, Science advances.

[6]  L. Parkkonen,et al.  Activity level in left auditory cortex predicts behavioral performance in inhibition tasks in children , 2020, NeuroImage.

[7]  Michele T. Diaz,et al.  Language immersion and language training: Two paths to enhanced language regulation and cognitive control , 2021, Brain and Language.

[8]  Caroline A. Lea-Carnall,et al.  Modelling neural entrainment and its persistence: influence of frequency of stimulation and phase at the stimulus offset , 2021, bioRxiv.

[9]  S. Leurgans,et al.  Physical activity, brain tissue microstructure, and cognition in older adults , 2021, PloS one.

[10]  Lora T. Likova,et al.  Neuroplasticity and crossmodal connectivity in the normal, healthy brain , 2021 .

[11]  J. Hämäläinen,et al.  Coherence Between Brain Activation and Speech Envelope at Word and Sentence Levels Showed Age-Related Differences in Low Frequency Bands , 2021, Neurobiology of Language.

[12]  S. Kastner,et al.  Attentional sampling of visual and auditory objects is captured by theta-modulated neural activity , 2021, The European journal of neuroscience.

[13]  Linda S. Hynan,et al.  Midlife aerobic exercise and brain structural integrity: Associations with age and cardiorespiratory fitness , 2020, NeuroImage.

[14]  H. Syväoja,et al.  Physical activity and aerobic fitness show different associations with brain processes underlying anticipatory selective visuospatial attention in adolescents , 2020, Brain Research.

[15]  Yijun Wang,et al.  Neural Basis of Semantically Dependent and Independent Cross-Modal Boosts on the Attentional Blink. , 2020, Cerebral cortex.

[16]  V. Steuber,et al.  The effect of alterations of schizophrenia-associated genes on gamma band oscillations , 2020, bioRxiv.

[17]  J. Karvanen,et al.  Physical activity and aerobic fitness in relation to local and interhemispheric functional connectivity in adolescents’ brains , 2020, Brain and behavior.

[18]  C. Hillman,et al.  Cardiorespiratory and muscular fitness associations with older adolescent cognitive control , 2020, Journal of sport and health science.

[19]  Tetsuya Takahashi,et al.  Auditory steady‐state response at 20 Hz and 40 Hz in young typically developing children and children with autism spectrum disorder , 2020, Psychiatry and clinical neurosciences.

[20]  Christopher W. Robinson.  Listen to Your Heart: Examining Modality Dominance Using Cross-Modal Oddball Tasks , 2020, Frontiers in Psychology.

[21]  G. Ottoboni,et al.  Multisensory Perception, Verbal, Visuo-spatial and Motor Working Memory Modulation After a Single Open- or Closed-Skill Exercise Session in Children , 2020, Journal of Cognitive Enhancement.

[22]  Juha Karvanen,et al.  Physical activity, aerobic fitness, and brain white matter: Their role for executive functions in adolescence , 2019, Developmental Cognitive Neuroscience.

[23]  K. Kessler,et al.  Reduced auditory steady state responses in autism spectrum disorder , 2019, bioRxiv.

[24]  R. Salmelin,et al.  Children show hemispheric differences in the basic auditory response properties , 2019, Human Brain Mapping.

[25]  C. Hillman,et al.  The Longitudinal Associations of Fitness and Motor Skills with Academic Achievement , 2019, Medicine and science in sports and exercise.

[26]  J. Karvanen,et al.  Aerobic fitness, but not physical activity, is associated with grey matter volume in adolescents , 2019, Behavioural Brain Research.

[27]  J. Gray,et al.  PsychoPy2: Experiments in behavior made easy , 2019, Behavior research methods.

[28]  Nicola Molinaro,et al.  Delta(but not theta)‐band cortical entrainment involves speech‐specific processing , 2018, The European journal of neuroscience.

[29]  C. Hillman,et al.  Associations Between Aerobic Fitness and Cognitive Control in Adolescents , 2018, Front. Psychol..

[30]  C. Hillman,et al.  Effects of physical activity interventions on cognitive and academic performance in children and adolescents: a novel combination of a systematic review and recommendations from an expert panel , 2018, British Journal of Sports Medicine.

[31]  L. Qin,et al.  Auditory steady-state responses in primary and non-primary regions of the auditory cortex in neonatal ventral hippocampal lesion rats , 2018, PloS one.

[32]  B. H. Lo,et al.  Autism Spectrum Disorder , 2018, Journal of paediatrics and child health.

[33]  S. Haegens,et al.  Rhythmic facilitation of sensory processing: A critical review , 2017, Neuroscience & Biobehavioral Reviews.

[34]  G. Ottoboni,et al.  One bout of open skill exercise improves cross-modal perception and immediate memory in healthy older adults who habitually exercise , 2017, PloS one.

[35]  A. Nobre,et al.  Prioritizing Information during Working Memory: Beyond Sustained Internal Attention , 2017, Trends in Cognitive Sciences.

[36]  I. Tarkka,et al.  Long-term physical activity modifies automatic visual processing , 2017 .

[37]  Robert T. Schultz,et al.  Translating Adult Electrophysiology Findings to Younger Patient Populations: Difficulty Measuring 40-Hz Auditory Steady-State Responses in Typically Developing Children and Children with Autism Spectrum Disorder , 2016, Developmental Neuroscience.

[38]  L. Andersen,et al.  Associations of Adiposity and Aerobic Fitness with Executive Function and Math Performance in Danish Adolescents. , 2015, The Journal of pediatrics.

[39]  Cathy Craig,et al.  Successful balance training is associated with improved multisensory function in fall-prone older adults , 2015, Comput. Hum. Behav..

[40]  Jeannette R. Mahoney,et al.  Visual-Somatosensory Integration is Linked to Physical Activity Level in Older Adults. , 2015, Multisensory research.

[41]  H. Syväoja,et al.  The Associations of Objectively Measured Physical Activity and Sedentary Time with Cognitive Functions in School-Aged Children , 2014, PloS one.

[42]  Lauri Parkkonen,et al.  Human Neuromagnetic Steady-State Responses to Amplitude-Modulated Tones, Speech, and Music , 2014, Ear and hearing.

[43]  M. Murray,et al.  Multisensory Integration: Flexible Use of General Operations , 2014, Neuron.

[44]  Megan M. McClelland,et al.  Physical Activity, Self-Regulation, and Early Academic Achievement in Preschool Children , 2014 .

[45]  A. Nobre,et al.  Top-down modulation: bridging selective attention and working memory , 2012, Trends in Cognitive Sciences.

[46]  Riitta Salmelin,et al.  Speech perception in the child brain: Cortical timing and its relevance to literacy acquisition , 2011, Human brain mapping.

[47]  D. Nieman,et al.  Physical activity predicts gray matter volume in late adulthood: The Cardiovascular Health Study , 2011 .

[48]  Markus Kiefer,et al.  Physical fitness, but not acute exercise modulates event-related potential indices for executive control in healthy adolescents , 2009, Brain Research.

[49]  J. Suckling,et al.  Age-related grey matter volume correlates of response inhibition and shifting in attention-deficit hyperactivity disorder. , 2009, The British journal of psychiatry : the journal of mental science.

[50]  B. Luna.  Developmental changes in cognitive control through adolescence. , 2009, Advances in child development and behavior.

[51]  Lauri Parkkonen,et al.  Early visual brain areas reflect the percept of an ambiguous scene , 2008, Proceedings of the National Academy of Sciences.

[52]  M. Steinschneider,et al.  The maturation of human evoked brain potentials to sounds presented at different stimulus rates , 2008, Hearing Research.

[53]  P. McGuire,et al.  Brain activation in paediatric obsessive-compulsive disorder during tasks of inhibitory control , 2008, British Journal of Psychiatry.

[54]  Chao-Cheng Chen,et al.  Neurophysiological mechanisms in the emotional modulation of attention: The interplay between threat sensitivity and attentional control , 2007, Biological Psychology.

[55]  Carl W. Cotman,et al.  Exercise builds brain health: key roles of growth factor cascades and inflammation , 2007, Trends in Neurosciences.

[56]  D. Amso,et al.  Development of cognitive control and executive functions from 4 to 13 years: Evidence from manipulations of memory, inhibition, and task switching , 2006, Neuropsychologia.

[57]  A. Nobre,et al.  Cognitive control of attention in the human brain: Insights from orienting attention to mental representations , 2006, Brain Research.

[58]  M. L. Demattè,et al.  Cross-modal interactions between olfaction and touch. , 2006, Chemical senses.

[59]  S. Taulu,et al.  Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements , 2006, Physics in medicine and biology.

[60]  C Pantev,et al.  Stimulus induced desynchronization of human auditory 40-Hz steady-state responses. , 2005, Journal of neurophysiology.

[61]  Riitta Salmelin,et al.  Cortical differentiation of speech and nonspeech sounds at 100 ms: implications for dyslexia. , 2005, Cerebral cortex.

[62]  S. Taulu,et al.  Suppression of Interference and Artifacts by the Signal Space Separation Method , 2003, Brain Topography.

[63]  K. Miller.  Executive functions. , 2005, Pediatric annals.

[64]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[65]  David Poeppel,et al.  The analysis of speech in different temporal integration windows: cerebral lateralization as 'asymmetric sampling in time' , 2003, Speech Commun..

[66]  Brenda Rapp,et al.  Principles of cross-modal competition: Evidence from deficits of attention , 2003, Psychonomic bulletin & review.

[67]  K. Uutela,et al.  Detecting and Correcting for Head Movements in Neuromagnetic Measurements , 2001, NeuroImage.

[68]  J. Eggermont,et al.  Maturation of human central auditory system activity: evidence from multi-channel evoked potentials , 2000, Clinical Neurophysiology.

[69]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[70]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[71]  L. Léger,et al.  The multistage 20 metre shuttle run test for aerobic fitness. , 1988, Journal of sports sciences.

[72]  C. Caspersen,et al.  Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research. , 1985, Public health reports.

[73]  J M Tanner,et al.  Variations in the Pattern of Pubertal Changes in Boys , 1970, Archives of disease in childhood.

[74]  J M Tanner,et al.  Variations in pattern of pubertal changes in girls. , 1969, Archives of disease in childhood.