Spatiotemporal brain dynamics underlying attentional bias modifications.

Exaggerated attentional biases toward specific elements of the environment contribute to the maintenance of several psychiatric conditions, such as biases to threatening faces in social anxiety. Although recent literature indicates that attentional bias modification may constitute an effective approach for psychiatric remediation, the underlying neurophysiological mechanisms remain unclear. We addressed this question by recording EEG in 24 healthy participants performing a modified dot-probe task in which pairs of neutral cues (colored shapes) were replaced by probe stimuli requiring a discrimination judgment. To induce an attentional bias toward or away from the cues, the probes were systematically presented either at the same or at the opposite position of a specific cue color. This paradigm enabled participants to spontaneously develop biases to initially unbiased, neutral cues, as measured by the response speed to the probe presented after the cues. Behavioral result indicated that the ABM procedure induced approach and avoidance biases. The influence of ABM on inhibitory control was assessed in a separated Go/NoGo task: changes in AB did not influence participants' capacity to inhibit their responses to the cues. Attentional bias modification was associated with a topographic modulation of event-related potentials already 50-84 ms following the onset of the cues. Statistical analyses of distributed electrical source estimations revealed that the development of attentional biases was associated with decreased activity in the left temporo-parieto-occipital junction. These findings suggest that attentional bias modification affects early sensory processing phases related to the extraction of information based on stimulus saliency.

[1]  J. Theeuwes,et al.  Electrophysiological Evidence of the Capture of Visual Attention , 2006, Journal of Cognitive Neuroscience.

[2]  G. Pourtois,et al.  Top-down effects on early visual processing in humans: A predictive coding framework , 2011, Neuroscience & Biobehavioral Reviews.

[3]  K. Viacava,et al.  Attentional bias modification based on visual probe task: methodological issues, results and clinical relevance. , 2015, Trends in psychiatry and psychotherapy.

[4]  Greg H. Proudfit,et al.  Electrocortical evidence for rapid allocation of attention to threat in the dot-probe task. , 2015, Social cognitive and affective neuroscience.

[5]  C. MacLeod,et al.  The Attentional Bias Modification Approach to Anxiety Intervention , 2015 .

[6]  M. Browning,et al.  Attentional bias modification (ABM) training induces spontaneous brain activity changes in young women with subthreshold depression: a randomized controlled trial , 2015, Psychological Medicine.

[7]  G. Hajcak,et al.  Single-session attention bias modification and error-related brain activity , 2015, Cognitive, Affective, & Behavioral Neuroscience.

[8]  Mingyi Qian,et al.  Continual training of attentional bias in social anxiety. , 2008, Behaviour research and therapy.

[9]  James T. Townsend,et al.  Methods of Modeling Capacity in Simple Processing Systems , 2014 .

[10]  G. Mangun Neural mechanisms of visual selective attention. , 1995, Psychophysiology.

[11]  C. Michel,et al.  Electromagnetic Inverse Solutions in Anatomically Constrained Spherical Head Models , 2004, Brain Topography.

[12]  Lucas Spierer,et al.  Brain Dynamics Underlying Training-Induced Improvement in Suppressing Inappropriate Action , 2010, The Journal of Neuroscience.

[13]  C. MacLeod,et al.  Attentional bias in emotional disorders. , 1986, Journal of abnormal psychology.

[14]  Christoph M. Michel,et al.  Spatiotemporal Analysis of Multichannel EEG: CARTOOL , 2011, Comput. Intell. Neurosci..

[15]  S. Hillyard,et al.  Event-related brain potentials in the study of visual selective attention. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Reinout W Wiers,et al.  Clinical effectiveness of attentional bias modification training in abstinent alcoholic patients. , 2010, Drug and alcohol dependence.

[17]  Carmel Mevorach,et al.  Opposite biases in salience-based selection for the left and right posterior parietal cortex , 2006, Nature Neuroscience.

[18]  G. Woodman,et al.  Event-related potential studies of attention , 2000, Trends in Cognitive Sciences.

[19]  F. Strack,et al.  Reflective and Impulsive Determinants of Social Behavior , 2004, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[20]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[21]  Matt Field,et al.  Attentional bias modification in tobacco smokers. , 2009, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[22]  M. Field,et al.  Attentional bias in addictive behaviors: a review of its development, causes, and consequences. , 2008, Drug and alcohol dependence.

[23]  Rolando Grave de Peralta,et al.  Comparison of Algorithms for the Localization of Focal Sources: Evaluation with simulated data and analysis of experimental data. , 2002 .

[24]  S J Luck,et al.  Visual event-related potentials index focused attention within bilateral stimulus arrays. II. Functional dissociation of P1 and N1 components. , 1990, Electroencephalography and clinical neurophysiology.

[25]  Charles T. Taylor,et al.  The effect of a single-session attention modification program on response to a public-speaking challenge in socially anxious individuals. , 2008, Journal of abnormal psychology.

[26]  Y. Bar-Haim,et al.  Neural plasticity in response to attention training in anxiety , 2009, Psychological Medicine.

[27]  John J. Foxe,et al.  Spatial attention modulates initial afferent activity in human primary visual cortex. , 2008, Cerebral cortex.

[28]  M. Olmstead Animal models of drug addiction: Where do we go from here? , 2006, Quarterly journal of experimental psychology.

[29]  Mathias Weymar,et al.  The face is more than its parts — Brain dynamics of enhanced spatial attention to schematic threat , 2011, NeuroImage.

[30]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[31]  S. Yantis,et al.  Visual attention: control, representation, and time course. , 1997, Annual review of psychology.

[32]  Micah M. Murray,et al.  Multisensory context portends object memory , 2014, Current Biology.

[33]  Lester Melie-Garcia,et al.  Statistical analysis of multichannel scalp field data , 2009 .

[34]  J. Hewig,et al.  Does a single session of Attentional Bias Modification influence early neural mechanisms of spatial attention? An ERP study. , 2014, Psychophysiology.

[35]  Maria Stein,et al.  Ragu: A Free Tool for the Analysis of EEG and MEG Event-Related Scalp Field Data Using Global Randomization Statistics , 2011, Comput. Intell. Neurosci..

[36]  Christoph M. Michel,et al.  Electrical neuroimaging based on biophysical constraints , 2004, NeuroImage.

[37]  A. Kelly,et al.  Human functional neuroimaging of brain changes associated with practice. , 2005, Cerebral cortex.

[38]  S. Hillyard,et al.  Spatial Selective Attention Affects Early Extrastriate But Not Striate Components of the Visual Evoked Potential , 1996, Journal of Cognitive Neuroscience.

[39]  L. Bizarro,et al.  Attentional bias modification in smokers trying to quit: a longitudinal study about the effects of number of sessions. , 2014, Journal of substance abuse treatment.

[40]  Jean Adès,et al.  Structure factorielle de la traduction française de l'échelle d'impulsivité de Barratt (BIS-10) , 2000 .

[41]  Ute Leonards,et al.  Attentional bias training and cue reactivity in cigarette smokers. , 2008, Addiction.

[42]  D. Lehmann,et al.  Principles of spatial analysis , 1987 .

[43]  F. Perrin,et al.  Mapping of scalp potentials by surface spline interpolation. , 1987, Electroencephalography and clinical neurophysiology.

[44]  Daniel S Pine,et al.  Neural changes with attention bias modification for anxiety: a randomized trial. , 2015, Social cognitive and affective neuroscience.

[45]  R. Snaith,et al.  The Hospital Anxiety and Depression Scale , 1983 .

[46]  Gilles Pourtois,et al.  Motivational Salience Modulates Early Visual Cortex Responses across Task Sets* , 2017, Journal of Cognitive Neuroscience.

[47]  M. Murray,et al.  A Tutorial Review of Electrical Neuroimaging From Group-Average to Single-Trial Event-Related Potentials , 2012, Developmental neuropsychology.

[48]  L. Spierer,et al.  Enhancing frontal top-down inhibitory control with Go/NoGo training , 2015, Brain Structure and Function.

[49]  J. Hewig,et al.  The N2pc component reliably captures attentional bias in social anxiety. , 2017, Psychophysiology.

[50]  Micah M. Murray,et al.  How single-trial electrical neuroimaging contributes to multisensory research , 2005, Experimental Brain Research.

[51]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[52]  Tracy A. Dennis,et al.  Attention training and the threat bias: An ERP study , 2012, Brain and Cognition.

[53]  Guy M. Goodwin,et al.  Lateral Prefrontal Cortex Mediates the Cognitive Modification of Attentional Bias , 2010, Biological Psychiatry.

[54]  Kevin S LaBar,et al.  Happy and fearful emotion in cues and targets modulate event-related potential indices of gaze-directed attentional orienting. , 2007, Social cognitive and affective neuroscience.

[55]  P. Philippot,et al.  Impact of the temporal stability of preexistent attentional bias for threat on its alteration through attention bias modification. , 2015, Journal of behavior therapy and experimental psychiatry.

[56]  M. Wallace,et al.  Multisensory temporal integration: task and stimulus dependencies , 2013, Experimental Brain Research.

[57]  Christoph M. Michel,et al.  Towards the utilization of EEG as a brain imaging tool , 2012, NeuroImage.

[58]  Thomas Koenig,et al.  A Method to Determine the Presence of Averaged Event-Related Fields Using Randomization Tests , 2010, Brain Topography.

[59]  J. Wolfe,et al.  Guided Search 2.0 A revised model of visual search , 1994, Psychonomic bulletin & review.

[60]  M. Giard,et al.  Auditory-Visual Integration during Multimodal Object Recognition in Humans: A Behavioral and Electrophysiological Study , 1999, Journal of Cognitive Neuroscience.

[61]  Patrick Dupont,et al.  Lesion evidence for the critical role of the intraparietal sulcus in spatial attention. , 2011, Brain : a journal of neurology.

[62]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. I. Method Descriptions and Simulations , 2004, Brain Topography.

[63]  M. Tiggemann,et al.  Combined effects of cognitive bias for food cues and poor inhibitory control on unhealthy food intake , 2015, Appetite.

[64]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

[65]  Gregor Thut,et al.  Prediction of response speed by anticipatory high‐frequency (gamma band) oscillations in the human brain , 2005, Human brain mapping.

[66]  Zhe Qu,et al.  Earliest stages of visual cortical processing are not modified by attentional load , 2014, Human brain mapping.

[67]  Maria Stein,et al.  Establishing correlations of scalp field maps with other experimental variables using covariance analysis and resampling methods , 2008, Clinical Neurophysiology.

[68]  T. Koenig,et al.  Electroencephalographic Topography Measures of Experienced Utility , 2011, The Journal of Neuroscience.

[69]  Susan L. Franzel,et al.  Guided search: an alternative to the feature integration model for visual search. , 1989, Journal of experimental psychology. Human perception and performance.

[70]  N. Fox,et al.  Modification of threat-processing in non-anxious individuals: a preliminary behavioral and ERP study. , 2013, Journal of behavior therapy and experimental psychiatry.

[71]  J. Richards,et al.  Dimensions of impulsive behavior: Personality and behavioral measures , 2006 .

[72]  C. Gilbert,et al.  Top-down influences on visual processing , 2013, Nature Reviews Neuroscience.

[73]  S. Dawe,et al.  Reward drive and rash impulsiveness as dimensions of impulsivity: implications for substance misuse. , 2004, Addictive behaviors.

[74]  Gilles Pourtois,et al.  Errors recruit both cognitive and emotional monitoring systems: Simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI , 2010, Neuropsychologia.

[75]  George R. Mangun,et al.  Sustained visual-spatial attention produces costs and benefits in response time and evoked neural activity , 1998, Neuropsychologia.

[76]  Steven J. Luck,et al.  Behavioral and ERP measures of attentional bias to threat in the dot-probe task: poor reliability and lack of correlation with anxiety , 2014, Front. Psychol..

[77]  Martin Eimer,et al.  Involuntary Attentional Capture is Determined by Task Set: Evidence from Event-related Brain Potentials , 2008, Journal of Cognitive Neuroscience.

[78]  Lucas Spierer,et al.  Plasticity in representations of environmental sounds revealed by electrical neuroimaging , 2008, NeuroImage.

[79]  A. Keil,et al.  Modulation of the C1 visual event-related component by conditioned stimuli: evidence for sensory plasticity in early affective perception. , 2006, Cerebral cortex.

[80]  Aurelie L. Manuel,et al.  Task relevance effects in electrophysiological brain activity: Early, but not first , 2014, NeuroImage.

[81]  A. Guastella,et al.  Attentional bias modification facilitates attentional control mechanisms: Evidence from eye tracking , 2015, Biological Psychology.

[82]  Martin P Paulus,et al.  Neural correlates of a computerized attention modification program in anxious subjects. , 2014, Social cognitive and affective neuroscience.

[83]  S Ullman,et al.  Shifts in selective visual attention: towards the underlying neural circuitry. , 1985, Human neurobiology.

[84]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[85]  Monique Ernst,et al.  Attention Bias Modification Treatment: A Meta-Analysis Toward the Establishment of Novel Treatment for Anxiety , 2010, Biological Psychiatry.

[86]  E. Vogel,et al.  The visual N1 component as an index of a discrimination process. , 2000, Psychophysiology.

[87]  P. Platte,et al.  Attentional bias toward high-calorie food-cues and trait motor impulsivity interactively predict weight gain , 2016, Health psychology open.

[88]  Andrew Mathews,et al.  Cognitive bias modification approaches to anxiety. , 2012, Annual review of clinical psychology.

[89]  K. Mogg,et al.  Electrophysiological evidence for greater attention to threat when cognitive control resources are depleted , 2013, Cognitive, Affective, & Behavioral Neuroscience.

[90]  C. Fairburn,et al.  Effect of psychological treatment on attentional bias in eating disorders , 2008, The International journal of eating disorders.

[91]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[92]  R. Wiers,et al.  Alcohol-related biases in selective attention and action tendency make distinct contributions to dysregulated drinking behaviour. , 2013, Addiction.

[93]  H. de Wit,et al.  Dual determinants of drug use in humans: reward and impulsivity. , 2004, Nebraska Symposium on Motivation. Nebraska Symposium on Motivation.

[94]  Glyn W. Humphreys,et al.  The Left Intraparietal Sulcus Modulates the Selection of Low Salient Stimuli , 2009, Journal of Cognitive Neuroscience.