Unraveling the Anxious Mind: Anxiety, Worry, and Frontal Engagement in Sustained Attention Versus Off-Task Processing

Much remains unknown regarding the relationship between anxiety, worry, sustained attention, and frontal function. Here, we addressed this using a sustained attention task adapted for functional magnetic resonance imaging. Participants responded to presentation of simple stimuli, withholding responses to an infrequent “No Go” stimulus. Dorsolateral prefrontal cortex (DLPFC) activity to “Go” trials, and dorsal anterior cingulate (dACC) activity to “No Go” trials were associated with faster error-free performance; consistent with DLPFC and dACC facilitating proactive and reactive control, respectively. Trait anxiety was linked to reduced recruitment of these regions, slower error-free performance, and decreased frontal-thalamo-striatal connectivity. This indicates an association between trait anxiety and impoverished frontal control of attention, even when external distractors are absent. In task blocks where commission errors were made, greater DLPFC-precuneus and DLPFC-posterior cingulate connectivity were associated with both trait anxiety and worry, indicative of increased off-task thought. Notably, unlike trait anxiety, worry was not linked to reduced frontal-striatal-thalamo connectivity, impoverished frontal recruitment, or slowed responding during blocks without commission errors, contrary to accounts proposing a direct causal link between worry and impoverished attentional control. This leads us to propose a new model of the relationship between anxiety, worry and frontal engagement in attentional control versus off-task thought.

[1]  Joshua Carp,et al.  Optimizing the order of operations for movement scrubbing: Comment on Power et al. , 2013, NeuroImage.

[2]  B. Olatunji,et al.  Worry and the anxiety disorders: A meta-analytic synthesis of specificity to GAD , 2010 .

[3]  M. Eysenck.  Anxiety, learning, and memory: A reconceptualization , 1979 .

[4]  R. A. Peterson,et al.  Anxiety sensitivity as a predictor of the development of panic symptoms, panic attacks, and panic disorder: a prospective study. , 2002, Journal of anxiety disorders.

[5]  M. Botvinick,et al.  Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[7]  C. Spielberger,et al.  Manual for the state-trait anxiety inventory (form Y) : "self-evaluation questionnaire" , 1983 .

[8]  Andrew R. A. Conway,et al.  Variation in working memory , 2008 .

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

[10]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[11]  P. Nachev.  Cognition and medial frontal cortex in health and disease , 2006, Current opinion in neurology.

[12]  T. Braver,et al.  Explaining the many varieties of working memory variation: Dual mechanisms of cognitive control. , 2007 .

[13]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[14]  T J Meyer,et al.  Development and validation of the Penn State Worry Questionnaire. , 1990, Behaviour research and therapy.

[15]  A. Richards,et al.  Colour-identification of differentially valenced words in anxiety , 1989 .

[16]  S. Bishop.  Trait anxiety and impoverished prefrontal control of attention , 2009, Nature Neuroscience.

[17]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[18]  A. Mathews,et al.  A Cognitive Model of Selective Processing in Anxiety , 1998, Cognitive Therapy and Research.

[19]  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.

[20]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

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

[22]  Deanna M. Barch,et al.  Extracting core components of cognitive control , 2006, Trends in Cognitive Sciences.

[23]  Katharine N. Thakkar,et al.  Response Inhibition and Response Monitoring in a Saccadic Countermanding Task in Schizophrenia , 2011, Biological Psychiatry.

[24]  I. Robertson,et al.  `Oops!': Performance correlates of everyday attentional failures in traumatic brain injured and normal subjects , 1997, Neuropsychologia.

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

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

[27]  K. Christoff,et al.  Experience sampling during fMRI reveals default network and executive system contributions to mind wandering , 2009, Proceedings of the National Academy of Sciences.

[28]  Karl J. Friston.  Analysing brain images: principles and overview , 1997 .

[29]  Vinod Goel,et al.  Reciprocal neural response within lateral and ventral medial prefrontal cortex during hot and cold reasoning , 2003, NeuroImage.

[30]  Evelyn Barron,et al.  Absorbed in Thought , 2011, Psychological science.

[31]  John Duncan,et al.  COMT val158met Genotype Affects Recruitment of Neural Mechanisms Supporting Fluid Intelligence , 2008, Cerebral cortex.

[32]  T. Pruzinsky,et al.  Preliminary exploration of worry: some characteristics and processes. , 1983, Behaviour research and therapy.

[33]  K. Power,et al.  The relationship between trait vulnerability and anxiety and depressive diagnoses at long-term follow-up of Generalized Anxiety Disorder. , 2004, Journal of anxiety disorders.

[34]  John J. Foxe,et al.  A topography of executive functions and their interactions revealed by functional magnetic resonance imaging. , 2004, Brain research. Cognitive brain research.

[35]  H. Pashler,et al.  Puzzlingly High Correlations in fMRI Studies of Emotion, Personality, and Social Cognition 1 , 2009, Perspectives on psychological science : a journal of the Association for Psychological Science.

[36]  M. Antony,et al.  The State-Trait Anxiety Inventory, Trait version: structure and content re-examined. , 1998, Behaviour research and therapy.

[37]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[38]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[39]  J. Houk,et al.  Model of cortical-basal ganglionic processing: encoding the serial order of sensory events. , 1998, Journal of neurophysiology.

[40]  K. Mogg,et al.  A cognitive-motivational analysis of anxiety. , 1998, Behaviour research and therapy.

[41]  M. Kane,et al.  Does mind wandering reflect executive function or executive failure? Comment on Smallwood and Schooler (2006) and Watkins (2008). , 2010, Psychological bulletin.

[42]  Katsuyuki Sakai,et al.  Reactive mechanism of cognitive control system. , 2010, Cerebral cortex.

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

[44]  Michael J. Frank,et al.  Interactions between frontal cortex and basal ganglia in working memory: A computational model , 2001, Cognitive, affective & behavioral neuroscience.

[45]  C. MacLeod,et al.  Anxiety and the Allocation of Attention to Threat , 1988, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[46]  A. Aron.  From Reactive to Proactive and Selective Control: Developing a Richer Model for Stopping Inappropriate Responses , 2011, Biological Psychiatry.

[47]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.