Working memory load reduces the late positive potential and this effect is attenuated with increasing anxiety

Emotion regulation decreases the processing of arousing stimuli, as indexed by the late positive potential (LPP), an electrocortical component that varies in amplitude with emotional arousal. Emotion regulation increases activity in the prefrontal areas associated with cognitive control, including the dosolateral prefrontal cortex (DLPFC). The present study manipulated working memory load, known to activate the DLPFC, and recorded the LPP elicited by aversive and neutral IAPS pictures presented during the retention interval. The LPP was larger on low-load compared to high-load trials, and on trials with aversive compared to neutral pictures. These LPP data suggest that emotional content and working memory load have opposing effects on attention to distracting stimuli. State anxiety was associated with reduced modulation of the LPP by working memory load. Results are discussed in terms of competition for attention between emotion and cognition and suggest a relationship between DLPFC activation and the allocation of attentional resources to distracting visual stimuli–a relationship that may be disrupted with increasing anxiety.

[1]  G. Hajcak,et al.  Event-Related Potentials, Emotion, and Emotion Regulation: An Integrative Review , 2010, Developmental neuropsychology.

[2]  M. Iwanaga,et al.  Test Anxiety and Working Memory System , 1996, Perceptual and motor skills.

[3]  R. Simons,et al.  Modulations of the electrophysiological response to pleasant stimuli by cognitive reappraisal. , 2008, Emotion.

[4]  N. Meiran,et al.  Divergent cognitive costs for online forms of reappraisal and distraction. , 2008, Emotion.

[5]  Greg Hajcak,et al.  The persistence of attention to emotion: brain potentials during and after picture presentation. , 2008, Emotion.

[6]  Ethan Kross,et al.  Facilitating Adaptive Emotional Analysis: Distinguishing Distanced-Analysis of Depressive Experiences From Immersed-Analysis and Distraction , 2008, Personality & social psychology bulletin.

[7]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[8]  R. Veit,et al.  Regulation of emotional responses elicited by threat‐related stimuli , 2007, Human brain mapping.

[9]  Dan Foti,et al.  Deconstructing Reappraisal: Descriptions Preceding Arousing Pictures Modulate the Subsequent Neural Response , 2008, Journal of Cognitive Neuroscience.

[10]  G. A. Miller,et al.  Contrasting patterns of brain activity in anxious apprehension and anxious arousal. , 1999, Psychophysiology.

[11]  O. John,et al.  Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. , 2003, Journal of personality and social psychology.

[12]  Annmarie MacNamara,et al.  Anxiety and spatial attention moderate the electrocortical response to aversive pictures , 2009, Neuropsychologia.

[13]  M. Eysenck,et al.  Anxiety and Performance: The Processing Efficiency Theory , 1992 .

[14]  P. Goldman-Rakic,et al.  Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys , 1981, The Journal of comparative neurology.

[15]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

[16]  M. Bradley,et al.  Aversive picture processing: effects of a concurrent task on sustained defensive system engagement. , 2011, Psychophysiology.

[17]  John Duncan,et al.  State Anxiety Modulation of the Amygdala Response to Unattended Threat-Related Stimuli , 2004, The Journal of Neuroscience.

[18]  Francesco Versace,et al.  Affective picture perception: Emotion, context, and the late positive potential , 2008, Brain Research.

[19]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[20]  M. Ashcraft,et al.  The relationships among working memory, math anxiety, and performance. , 2001, Journal of experimental psychology. General.

[21]  G. McCarthy,et al.  Brain Systems Mediating Cognitive Interference by Emotional Distraction , 2006, The Journal of Neuroscience.

[22]  D. Weinberger,et al.  Neocortical modulation of the amygdala response to fearful stimuli , 2003, Biological Psychiatry.

[23]  Harald T. Schupp,et al.  Emotional Facilitation of Sensory Processing in the Visual Cortex , 2003, Psychological science.

[24]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

[25]  James J. Gross,et al.  Personality and emotional memory: How regulating emotion impairs memory for emotional events , 2006 .

[26]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[27]  P. Lang International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[28]  Henrik Walter,et al.  Cognitive modulation of emotion anticipation , 2006, The European journal of neuroscience.

[29]  William A. Cunningham,et al.  Using fMRI to investigate a component process of reflection: Prefrontal correlates of refreshing a just-activated representation , 2016 .

[30]  Jeremy R. Gray,et al.  Threat-Evoked Anxiety Disrupts Spatial Working Memory Performance: An Attentional Account , 2003, Cognitive Therapy and Research.

[31]  Adam Gazzaley,et al.  Neural Suppression of Irrelevant Information Underlies Optimal Working Memory Performance , 2009, The Journal of Neuroscience.

[32]  S. Nieuwenhuis,et al.  Reappraisal modulates the electrocortical response to unpleasant pictures , 2006, Cognitive, affective & behavioral neuroscience.

[33]  A. Ohman,et al.  Emotion drives attention: detecting the snake in the grass. , 2001, Journal of experimental psychology. General.

[34]  R. Simons,et al.  Intentional modulation of emotional responding to unpleasant pictures: an ERP study. , 2006, Psychophysiology.

[35]  John Polich,et al.  Affective ERP processing in a visual oddball task: Arousal, valence, and gender , 2008, Clinical Neurophysiology.

[36]  G A Miller,et al.  Patterns of regional brain activity differentiate types of anxiety. , 1997, Journal of abnormal psychology.

[37]  P. Lang,et al.  International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (Tech. Rep. No. A-4) , 1999 .

[38]  J. Denollet,et al.  Usefulness of type D personality in predicting five-year cardiac events above and beyond concurrent symptoms of stress in patients with coronary heart disease. , 2006, The American journal of cardiology.

[39]  B. Mensour,et al.  Neural circuitry underlying voluntary suppression of sadness , 2003, Biological Psychiatry.

[40]  J. Gross The Emerging Field of Emotion Regulation: An Integrative Review , 1998 .

[41]  J Radilová,et al.  The late positive component of visual evoked response sensitive to emotional factors. , 1982, Activitas nervosa superior.

[42]  J. Gross,et al.  The social consequences of expressive suppression. , 2003, Emotion.

[43]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[44]  Dan Foti,et al.  Tell me about it: neural activity elicited by emotional pictures and preceding descriptions. , 2009, Emotion.

[45]  Kevin N. Ochsner,et al.  The Neural Bases of Distraction and Reappraisal , 2010, Journal of Cognitive Neuroscience.

[46]  Z. Nahas,et al.  Dorsolateral Prefrontal Cortex Stimulation Modulates Electrocortical Measures of Visual Attention: Evidence from Direct Bilateral Epidural Cortical Stimulation in Treatment-resistant Mood Disorder Ine Regional Specificity of Pfc Stimulation on the Parietally- Maximal Late Positive Potential (lpp), a , 2022 .

[47]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[48]  Kamryn T. Eddy,et al.  Amygdala-frontal connectivity during emotion regulation. , 2007, Social cognitive and affective neuroscience.

[49]  Greg Hajcak,et al.  See no evil: directing visual attention within unpleasant images modulates the electrocortical response. , 2009, Psychophysiology.

[50]  V. Johnston,et al.  Multiple P3s to emotional stimuli and their theoretical significance. , 1986, Psychophysiology.

[51]  R. Heimberg,et al.  Generalized anxiety disorder. , 2002 .

[52]  M. Junghöfer,et al.  Emotion and attention: event-related brain potential studies. , 2006, Progress in brain research.

[53]  Sander L. Koole,et al.  Tuning down the emotional brain: An fMRI study of the effects of cognitive load on the processing of affective images , 2009, NeuroImage.

[54]  R. Rapee,et al.  The utilisation of working memory by worry. , 1993, Behaviour research and therapy.

[55]  D. Mennin,et al.  Evidence of Broad Deficits in Emotion Regulation Associated with Chronic Worry and Generalized Anxiety Disorder , 2006, Cognitive Therapy and Research.

[56]  Brent L. Hughes,et al.  Prefrontal-Subcortical Pathways Mediating Successful Emotion Regulation , 2008, Neuron.

[57]  G. Hajcak,et al.  Differentiating neural responses to emotional pictures: evidence from temporal-spatial PCA. , 2009, Psychophysiology.

[58]  S. Koole,et al.  Clearing the mind: a working memory model of distraction from negative mood. , 2007, Emotion.

[59]  Jeffrey S. Maxwell,et al.  Anxiety selectively disrupts visuospatial working memory. , 2006, Emotion.

[60]  D. Manoach,et al.  Prefrontal cortex fMRI signal changes are correlated with working memory load , 1997, Neuroreport.

[61]  Richard J. Davidson,et al.  Gaze fixations predict brain activation during the voluntary regulation of picture-induced negative affect , 2007, NeuroImage.

[62]  Anna Weinberg,et al.  Beyond good and evil: the time-course of neural activity elicited by specific picture content. , 2010, Emotion.

[63]  M. Eysenck,et al.  Anxiety and cognitive performance: attentional control theory. , 2007, Emotion.

[64]  Susanne Erk,et al.  Valence-specific regulation effects in a working memory task with emotional context , 2007, NeuroImage.

[65]  D. Mennin,et al.  Emotion Regulation Therapy for Generalized Anxiety Disorder. , 2013, Cognitive and behavioral practice.

[66]  E. Keogh,et al.  Test-Anxiety, inferential reasoning and working memory load , 2000 .

[67]  K. Phan,et al.  Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[68]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[69]  M. Eysenck,et al.  Anxiety, Processing Efficiency, and Cognitive Performance New Developments from Attentional Control Theory , 2009 .

[70]  M. Beauregard,et al.  Neural Correlates of Conscious Self-Regulation of Emotion , 2001, The Journal of Neuroscience.

[71]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[72]  R. Cabeza,et al.  Event-related potentials of emotional memory: Encoding pleasant, unpleasant, and neutral pictures , 2002, Cognitive, affective & behavioral neuroscience.

[73]  G. Hajcak,et al.  Distinct electrocortical and behavioral evidence for increased attention to threat in generalized anxiety disorder , 2010, Depression and anxiety.

[74]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[75]  W. McKeachie,et al.  Test Anxiety: Deficits in Information Processing. , 1981 .

[76]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[77]  Evelyn Behar,et al.  Avoidance Theory of Worry and Generalized Anxiety Disorder. , 2004 .

[78]  Anna Weinberg,et al.  The Late Positive Potential Predicts Subsequent Interference with Target Processing , 2011, Journal of Cognitive Neuroscience.

[79]  Heather L. Urry,et al.  Failure to Regulate: Counterproductive Recruitment of Top-Down Prefrontal-Subcortical Circuitry in Major Depression , 2007, The Journal of Neuroscience.

[80]  Dan Foti,et al.  Motivated and controlled attention to emotion: Time-course of the late positive potential , 2009, Clinical Neurophysiology.

[81]  M. Wessa,et al.  How to regulate emotion? Neural networks for reappraisal and distraction. , 2011, Cerebral cortex.

[82]  Richard G. Heimberg,et al.  Generalized anxiety disorder: Advances in research and practice. , 2004 .

[83]  Markus Junghöfer,et al.  Selective Visual Attention to Emotion , 2007, The Journal of Neuroscience.

[84]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[85]  N. Derakshan,et al.  The neural correlates of cognitive effort in anxiety: Effects on processing efficiency , 2011, Biological Psychology.

[86]  J. Denollet,et al.  Type D personality, cardiac events, and impaired quality of life: a review , 2003, European journal of cardiovascular prevention and rehabilitation : official journal of the European Society of Cardiology, Working Groups on Epidemiology & Prevention and Cardiac Rehabilitation and Exercise Physiology.

[87]  M. Junghöfer,et al.  The selective processing of briefly presented affective pictures: an ERP analysis. , 2004, Psychophysiology.