Failure to filter: anxious individuals show inefficient gating of threat from working memory

Dispositional anxiety is a well-established risk factor for the development of psychiatric disorders along the internalizing spectrum, including anxiety and depression. Importantly, many of the maladaptive behaviors characteristic of anxiety, such as anticipatory apprehension, occur when threat is absent. This raises the possibility that anxious individuals are less efficient at gating threat's access to working memory, a limited capacity workspace where information is actively retained, manipulated, and used to flexibly guide goal-directed behavior when it is no longer present in the external environment. Using a well-validated neurophysiological index of working memory storage, we demonstrate that threat-related distracters were difficult to filter on average and that this difficulty was exaggerated among anxious individuals. These results indicate that dispositionally anxious individuals allocate excessive working memory storage to threat, even when it is irrelevant to the task at hand. More broadly, these results provide a novel framework for understanding the maladaptive thoughts and actions characteristic of internalizing disorders.

[1]  R. Marois,et al.  Posterior parietal cortex activity predicts individual differences in visual short-term memory capacity , 2005, Cognitive, affective & behavioral neuroscience.

[2]  Richard J. Davidson,et al.  Identifying robust and sensitive frequency bands for interrogating neural oscillations , 2010, NeuroImage.

[3]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

[4]  T. Yarkoni Big Correlations in Little Studies: Inflated fMRI Correlations Reflect Low Statistical Power—Commentary on Vul et al. (2009) , 2009, Perspectives on psychological science : a journal of the Association for Psychological Science.

[5]  W. Jung,et al.  Reliability Generalization of Scores on the Spielberger State-Trait Anxiety Inventory , 2002 .

[6]  Thomas V. Wiecki,et al.  Neurocomputational models of motor and cognitive deficits in Parkinson's disease. , 2010, Progress in brain research.

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

[8]  C. Büchel,et al.  Amygdala Activation Predicts Gaze toward Fearful Eyes , 2009, The Journal of Neuroscience.

[9]  R. Kessler,et al.  Twelve‐month and lifetime prevalence and lifetime morbid risk of anxiety and mood disorders in the United States , 2012, International journal of methods in psychiatric research.

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

[11]  Y. Bar-Haim,et al.  Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. , 2007, Psychological bulletin.

[12]  T. Klingberg,et al.  Prefrontal cortex and basal ganglia control access to working memory , 2008, Nature Neuroscience.

[13]  Matthew C. Keller,et al.  Increased sensitivity in neuroimaging analyses using robust regression , 2005, NeuroImage.

[14]  Margaret C Jackson,et al.  Enhanced visual short-term memory for angry faces. , 2009, Journal of experimental psychology. Human perception and performance.

[15]  Jonathan D. Cohen,et al.  Role of prefrontal cortex and the midbrain dopamine system in working memory updating , 2012, Proceedings of the National Academy of Sciences.

[16]  R. Krueger,et al.  Reinterpreting comorbidity: a model-based approach to understanding and classifying psychopathology. , 2006, Annual review of clinical psychology.

[17]  E. Koster,et al.  Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review. , 2010, Clinical psychology review.

[18]  Mark T. Waters,et al.  This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited.Thislicensedoesnot permit commercial exploitation or the creation of derivative works without sp , 2009 .

[19]  N. Cowan The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

[20]  S. Bishop,et al.  Neural Mechanisms Underlying Selective Attention to Threat , 2008, Annals of the New York Academy of Sciences.

[21]  M. Eysenck Anxiety and the worry process , 1984 .

[22]  Richard J. Davidson,et al.  Electromyogenic artifacts and electroencephalographic inferences revisited , 2011, NeuroImage.

[23]  Greg J Siegle,et al.  Neurobiological correlates of cognitions in fear and anxiety: A cognitive–neurobiological information-processing model , 2012, Cognition & emotion.

[24]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[25]  M. Chun,et al.  Dissociable neural mechanisms supporting visual short-term memory for objects , 2006, Nature.

[26]  Rob Jenkins,et al.  Neural processing of fearful faces: effects of anxiety are gated by perceptual capacity limitations. , 2007, Cerebral cortex.

[27]  E. Vogel,et al.  Are old adults just like low working memory young adults? Filtering efficiency and age differences in visual working memory. , 2011, Cerebral cortex.

[28]  P. Downing,et al.  The neural basis of visual body perception , 2007, Nature Reviews Neuroscience.

[29]  J. Dietch Anxiety Disorders and Phobias: A Cognitive Perspective , 1986 .

[30]  Edward K. Vogel,et al.  What ERPs Can Tell Us about Working Memory , 2011 .

[31]  Steven Taylor,et al.  Non-adherence and non-response in the treatment of anxiety disorders. , 2012, Journal of anxiety disorders.

[32]  Katherine E. Prater,et al.  Failure of anterior cingulate activation and connectivity with the amygdala during implicit regulation of emotional processing in generalized anxiety disorder. , 2010, The American journal of psychiatry.

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

[34]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[35]  J. Gross,et al.  Looking Inward , 2012, Psychological science.

[36]  Michael J. Frank,et al.  A dopaminergic basis for working memory, learning and attentional shifting in Parkinsonism , 2008, Neuropsychologia.

[37]  Maro G. Machizawa,et al.  Neural activity predicts individual differences in visual working memory capacity , 2004, Nature.

[38]  B. Postle Working memory as an emergent property of the mind and brain , 2006, Neuroscience.

[39]  Antonio Schettino,et al.  rain mechanisms for emotional influences on perception and attention : hat is magic and what is not , 2012 .

[40]  N. Tzourio-mazoyer,et al.  Neural foundations of logical and mathematical cognition , 2003, Nature Reviews Neuroscience.

[41]  S. Lyubomirsky,et al.  Rethinking Rumination , 2008, Perspectives on psychological science : a journal of the Association for Psychological Science.

[42]  Katherine E. Prater,et al.  Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. , 2009, Archives of general psychiatry.

[43]  E. Koster,et al.  Impaired filtering of irrelevant information in dysphoria: an ERP study. , 2012, Social cognitive and affective neuroscience.

[44]  S. Rauch,et al.  Inhibited and Uninhibited Infants "Grown Up": Adult Amygdalar Response to Novelty , 2003, Science.

[45]  J. Jay Todd,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004, Nature.

[46]  Sonia J. Bishop,et al.  Neurocognitive mechanisms of anxiety: an integrative account , 2007, Trends in Cognitive Sciences.

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

[48]  A. Baddeley Working memory: theories, models, and controversies. , 2012, Annual review of psychology.

[49]  H. Karnath,et al.  Keeping Memory Clear and Stable—The Contribution of Human Basal Ganglia and Prefrontal Cortex to Working Memory , 2010, The Journal of Neuroscience.

[50]  Maro G. Machizawa,et al.  Neural measures reveal individual differences in controlling access to working memory , 2005, Nature.

[51]  M. Botvinick Conflict monitoring and decision making: Reconciling two perspectives on anterior cingulate function , 2007, Cognitive, affective & behavioral neuroscience.

[52]  T. Egner,et al.  Search for a threatening target triggers limbic guidance of spatial attention , 2009, NeuroImage.

[53]  E. Vogel,et al.  Contralateral delay activity provides a neural measure of the number of representations in visual working memory. , 2010, Journal of neurophysiology.

[54]  Klaus Oberauer,et al.  Neural Evidence for a Distinction between Short-term Memory and the Focus of Attention , 2012, Journal of Cognitive Neuroscience.

[55]  J. Clauss,et al.  Behavioral inhibition and risk for developing social anxiety disorder: a meta-analytic study. , 2012, Journal of the American Academy of Child and Adolescent Psychiatry.

[56]  P. Whalen Fear, Vigilance, and Ambiguity , 1998 .

[57]  K. Oberauer Access to information in working memory: exploring the focus of attention. , 2002, Journal of experimental psychology. Learning, memory, and cognition.

[58]  Bradley R. Postle,et al.  Delay-period Activity in the Prefrontal Cortex: One Function Is Sensory Gating , 2005, Journal of Cognitive Neuroscience.

[59]  N. Berggren,et al.  Attentional control deficits in trait anxiety: Why you see them and why you don’t , 2013, Biological Psychology.

[60]  Hans-Jochen Heinze,et al.  Asymmetrical Activation in the Human Brain during Processing of Fearful Faces , 2005, Current Biology.

[61]  R. de Graaf,et al.  Anxiety disorders and risk for suicidal ideation and suicide attempts: a population-based longitudinal study of adults. , 2005, Archives of general psychiatry.

[62]  Richard L. Lewis,et al.  The mind and brain of short-term memory. , 2008, Annual review of psychology.

[63]  P. Goldman-Rakic Regional and cellular fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[64]  F. Schmidt,et al.  Linking "big" personality traits to anxiety, depressive, and substance use disorders: a meta-analysis. , 2010, Psychological bulletin.

[65]  Maro G. Machizawa,et al.  Electrophysiological Measures of Maintaining Representations in Visual Working Memory , 2007, Cortex.

[66]  P. Sessa,et al.  Interhemispheric ERP asymmetries over inferior parietal cortex reveal differential visual working memory maintenance for fearful versus neutral facial identities. , 2011, Psychophysiology.

[67]  Richard J. Davidson,et al.  Validation of ICA-based myogenic artifact correction for scalp and source-localized EEG , 2010, NeuroImage.

[68]  Nelson Cowan,et al.  Working Memory Capacity , 2005 .

[69]  Jane E Raymond,et al.  Familiarity enhances visual working memory for faces. , 2008, Journal of experimental psychology. Human perception and performance.

[70]  M. Poo,et al.  Grand challenges in global mental health , 2011, Nature.

[71]  Nelson Cowan,et al.  Visual working memory deficits in patients with Parkinson's disease are due to both reduced storage capacity and impaired ability to filter out irrelevant information. , 2010, Brain : a journal of neurology.

[72]  B. Lahey,et al.  Public health significance of neuroticism. , 2009, The American psychologist.

[73]  Jennifer Urbano Blackford,et al.  Amygdala and hippocampus fail to habituate to faces in individuals with an inhibited temperament , 2012, Social cognitive and affective neuroscience.

[74]  Michael J. Frank,et al.  A mechanistic account of striatal dopamine function in human cognition: psychopharmacological studies with cabergoline and haloperidol. , 2006, Behavioral neuroscience.

[75]  S. Shelton,et al.  Neural mechanisms underlying heterogeneity in the presentation of anxious temperament , 2013, Proceedings of the National Academy of Sciences.

[76]  Jos J. A. Van Berkum,et al.  TRAIT ANXIETY, DEFENSIVENESS, AND THE STRUCTURE OF WORRY , 1992 .

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

[78]  Monique Ernst,et al.  Attention biases, anxiety, and development: toward or away from threats or rewards? , 2012, Depression and anxiety.

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

[80]  R. Davidson,et al.  The integration of negative affect, pain and cognitive control in the cingulate cortex , 2011, Nature Reviews Neuroscience.

[81]  Jeffrey N. Rouder,et al.  How to measure working memory capacity in the change detection paradigm , 2011, Psychonomic bulletin & review.

[82]  P. Ekman Pictures of Facial Affect , 1976 .

[83]  Andreas Keil,et al.  The Timing of Emotional Discrimination in Human Amygdala and Ventral Visual Cortex , 2009, The Journal of Neuroscience.

[84]  Bradley Voytek,et al.  Prefrontal cortex and basal ganglia contributions to visual working memory , 2010, Proceedings of the National Academy of Sciences.

[85]  J. Gottlieb,et al.  Distinct neural mechanisms of distractor suppression in the frontal and parietal lobe , 2012, Nature Neuroscience.

[86]  M. Eysenck,et al.  New perspectives in attentional control theory , 2011 .

[87]  David G. Amaral,et al.  Neuroanatomy of the primate amygdala. , 2009 .

[88]  Richard J. Davidson,et al.  Electromyogenic Artifacts and Electroencephalographic Inferences , 2009, Brain Topography.

[89]  H Pashler,et al.  Familiarity and visual change detection , 1988, Perception & psychophysics.

[90]  A. Etkin,et al.  Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. , 2007, The American journal of psychiatry.

[91]  Luiz Pessoa,et al.  Segregating the significant from the mundane on a moment-to-moment basis via direct and indirect amygdala contributions , 2009, Proceedings of the National Academy of Sciences.

[92]  D. Pine,et al.  Neural substrates of childhood anxiety disorders: a review of neuroimaging findings. , 2012, Child and adolescent psychiatric clinics of North America.