Modulation of brain alpha rhythm and heart rate variability by attention-related mechanisms

According to recent evidence, oscillations in the alpha-band (8–14 Hz) play an active role in attention via allocation of cortical resources: decrease in alpha activity enhances neural processes in task-relevant regions, while increase in alpha activity reduces processing in task-irrelevant regions. Here, we analyzed changes in alpha-band power of 13-channel electroencephalogram (EEG) acquired from 30 subjects while performing four tasks that differently engaged visual, computational and motor attentional components. The complete (visual + computational + motor) task required to read and solve an arithmetical operation and provide a motor response; three simplified tasks involved a subset of these components (visual + computational task, visual task, motor task). Task-related changes in alpha power were quantified by aggregating electrodes into two main regions (fronto-central and parieto-occipital), to test regional specificity of alpha modulation depending on the involved attentional aspects. Independent Component Analysis (ICA) was applied to discover the main independent processes accounting for alpha power over the two scalp regions. Furthermore, we performed analysis of Heart Rate Variability (HRV) from one electrocardiogram signal acquired simultaneously with EEG, to test autonomic reaction to attentional loads. Results showed that alpha power modulation over the two scalp regions not only reflected the number of involved attentional components (the larger their number the larger the alpha power suppression) but was also fine-tuned by the nature of the recruited mechanisms (visual, computational, motor) relative to the functional specification of the regions. ICA revealed topologically dissimilar and differently attention-regulated processes of alpha power over the two regions. HRV indexes were less sensitive to different attentional aspects compared to alpha power, with vagal activity index presenting larger changes. This study contributes to improve our understanding of the electroencephalographic and autonomic correlates of attention and may have practical implications in neurofeedback, brain-computer interfaces, neuroergonomics as well as in clinical practice and neuroscience research exploring attention-deficit disorders.

[1]  John J. Foxe,et al.  The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention , 2011, Front. Psychology.

[2]  Terrence J. Sejnowski,et al.  Independent Component Analysis Using an Extended Infomax Algorithm for Mixed Subgaussian and Supergaussian Sources , 1999, Neural Computation.

[3]  Febo Cincotti,et al.  Human Movement-Related Potentials vs Desynchronization of EEG Alpha Rhythm: A High-Resolution EEG Study , 1999, NeuroImage.

[4]  Chong Zhang,et al.  Relationship between scalp potential and autonomic nervous activity during a mental arithmetic task , 2009, Autonomic Neuroscience.

[5]  M. Hallett,et al.  Task-related coherence and task-related spectral power changes during sequential finger movements. , 1998, Electroencephalography and clinical neurophysiology.

[6]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[7]  S. Luck,et al.  The Oxford handbook of event-related potential components , 2011 .

[8]  N. Weisz,et al.  Not so different after all: The same oscillatory processes support different types of attention , 2015, Brain Research.

[9]  W. Klimesch Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[10]  Jana Wörsching,et al.  Autonomic cardiovascular regulation and cortical tone , 2015, Clinical physiology and functional imaging.

[11]  Tobias Kaufmann,et al.  ARTiiFACT: a tool for heart rate artifact processing and heart rate variability analysis , 2011, Behavior research methods.

[12]  L. Faes,et al.  Information dynamics of brain–heart physiological networks during sleep , 2014, New Journal of Physics.

[13]  Tyler S. Grummett,et al.  Measurement of neural signals from inexpensive, wireless and dry EEG systems , 2015, Physiological measurement.

[14]  G. Glover,et al.  Dissociating Prefrontal and Parietal Cortex Activation during Arithmetic Processing , 2000, NeuroImage.

[15]  E. Basar,et al.  Resting state Rolandic mu rhythms are related to activity of sympathetic component of autonomic nervous system in healthy humans. , 2016, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[16]  Claudio Babiloni,et al.  Visuo-spatial consciousness and parieto-occipital areas: a high-resolution EEG study. , 2006, Cerebral cortex.

[17]  Julien Penders,et al.  Wearable, Wireless EEG Solutions in Daily Life Applications: What are we Missing? , 2015, IEEE Journal of Biomedical and Health Informatics.

[18]  J. Lisman,et al.  Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. , 2002, Cerebral cortex.

[19]  Silke M. Göbel,et al.  Parietal rTMS distorts the mental number line: Simulating ‘spatial’ neglect in healthy subjects , 2006, Neuropsychologia.

[20]  W. Sato,et al.  Frontal midline theta rhythm is correlated with cardiac autonomic activities during the performance of an attention demanding meditation procedure. , 2001, Brain research. Cognitive brain research.

[21]  Bert De Smedt,et al.  Oscillatory EEG correlates of arithmetic strategy use in addition and subtraction , 2009, Experimental Brain Research.

[22]  Shuyou Zhang,et al.  An EEG Study of a Confusing State Induced by Information Insufficiency during Mathematical Problem-Solving and Reasoning , 2018, Comput. Intell. Neurosci..

[23]  Bert De Smedt,et al.  Neurophysiological evidence for the validity of verbal strategy reports in mental arithmetic , 2011, Biological Psychology.

[24]  G. Pfurtscheller,et al.  Event-related synchronization (ERS) in the alpha band--an electrophysiological correlate of cortical idling: a review. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[25]  G. Berntson,et al.  An approach to artifact identification: application to heart period data. , 1990, Psychophysiology.

[26]  J. Thayer,et al.  Vagal influence on working memory and attention. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[27]  Shwu-Lih Huang,et al.  The influence of attention levels on psychophysiological responses. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  Anthony J. Ries,et al.  Usability of four commercially-oriented EEG systems , 2014, Journal of neural engineering.

[29]  Clemens Brunner,et al.  Event-related EEG theta and alpha band oscillatory responses during language translation , 2007, Brain Research Bulletin.

[30]  D. Sanabria,et al.  Heart rate variability and cognitive processing: The autonomic response to task demands , 2016, Biological Psychology.

[31]  T. Fernández,et al.  EEG activation patterns during the performance of tasks involving different components of mental calculation. , 1995, Electroencephalography and clinical neurophysiology.

[32]  S. Bouisset,et al.  [Voluntary movement]. , 1953, Journal de physiologie.

[33]  M. Benedek,et al.  Alpha power increases in right parietal cortex reflects focused internal attention , 2014, Neuropsychologia.

[34]  J. Schoffelen,et al.  Parieto‐occipital sources account for the increase in alpha activity with working memory load , 2007, Human brain mapping.

[35]  Carolyne R Swain,et al.  Electrophysiological, behavioral, and subjective indexes of workload when performing multiple tasks: manipulations of task difficulty and training. , 1999, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[36]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[37]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.