Anterior cingulate activation in high trait anxious subjects is related to altered error processing during decision making

BACKGROUND Individuals with high trait anxiety (HTA) can be studied to examine the effect of elevated levels of anxiety on the processing of stimuli and the selection of actions. The anterior cingulate cortex has been implicated in the detection and processing of errors. This investigation examined the hypothesis that HTA subjects are more sensitive to errors than nonanxious comparison subjects during a simple decision-making task and show increased activation in the anterior cingulate, particularly at low error rates. METHODS Thirteen HTA subjects were compared with 13 normal trait anxiety (NTA: 40th-60th percentile) subjects during functional magnetic resonance imaging while performing a two-choice prediction task at three different error rates. RESULTS Both HTA and NTA subjects performed similarly during a simple two-choice prediction task; however, during the low-error-rate condition, activation in the anterior cingulate and medial prefrontal cortex was significantly higher in HTA subjects and was correlated with trait but not state anxiety. CONCLUSIONS These results support the idea that HTA subjects devote more processing resources to decision making than do NTA subjects during times in which there is little chance of incorrect responding (i.e., the low-error-rate condition). The extent to which this altered activation within the anterior cingulate contributes to anxiety-proneness remains to be determined.

[1]  M. Raichle,et al.  Emotion-induced changes in human medial prefrontal cortex: II. During anticipatory anxiety. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[2]  A. Craig A new view of pain as a homeostatic emotion , 2003, Trends in Neurosciences.

[3]  Karl J. Friston,et al.  Amygdala–Hippocampal Involvement in Human Aversive Trace Conditioning Revealed through Event-Related Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[4]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. , 2001, Cerebral cortex.

[5]  P. Fox,et al.  Differential limbic–cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders , 2000, Biological Psychiatry.

[6]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[7]  R. Elliott,et al.  Ventromedial prefrontal cortex mediates guessing , 1999, Neuropsychologia.

[8]  Jerome R. Busemeyer,et al.  Criterion Learning in a Deferred Decision-Making Task , 1989 .

[9]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[10]  H. Critchley,et al.  Neural Activity in the Human Brain Relating to Uncertainty and Arousal during Anticipation , 2001, Neuron.

[11]  W. Schultz,et al.  Discrete Coding of Reward Probability and Uncertainty by Dopamine Neurons , 2003, Science.

[12]  R. Duncan Luce,et al.  Individual Choice Behavior , 1959 .

[13]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[14]  M. Geyer,et al.  The assessment of sequential response organization in schizophrenic and control subjects , 1994, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[15]  Ludvigson Hw Response units in the prediction of simple event patterns. , 1966 .

[16]  Guessing behavior of normal and retarded children under two random reinforcement conditions. , 1967, Child development.

[17]  R. Dolan,et al.  A Functional Anatomy of Anticipatory Anxiety , 1999, NeuroImage.

[18]  A. Richards,et al.  Anxiety and memory: a recall bias for threatening words in high anxiety. , 1997, Behaviour research and therapy.

[19]  K. Hornik,et al.  Anxiety as a predictor of relapse in detoxified alcohol-dependent patients. , 2002, Alcohol and alcoholism.

[20]  Nathaniel M. Alpert,et al.  The functional neuroanatomy of anxiety: a study of three disorders using positron emission tomography and symptom provocation , 1997, Biological Psychiatry.

[21]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  Christopher K. Hsee,et al.  Risk as Feelings , 2001, Psychological bulletin.

[23]  P. Costa,et al.  Normal Personality Assessment in Clinical Practice: The NEO Personality Inventory. , 1992 .

[24]  M. J. Norušis,et al.  SPSS base system user's guide , 1990 .

[25]  I. Grosse,et al.  MEASURING CORRELATIONS IN SYMBOL SEQUENCES , 1995 .

[26]  C. Spielberger,et al.  Anxiety (drive), stress, and serial-position effects in serial-verbal learning. , 1966, Journal of experimental psychology.

[27]  Andrew W Young,et al.  Anxiety-related bias in the classification of emotionally ambiguous facial expressions. , 2002, Emotion.

[28]  Gregory G. Brown,et al.  Prefrontal, Parietal, and Temporal Cortex Networks Underlie Decision-Making in the Presence of Uncertainty , 2001, NeuroImage.

[29]  R. Ladouceur,et al.  Experimental manipulation of intolerance of uncertainty: a study of a theoretical model of worry. , 2000, Behaviour research and therapy.

[30]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

[31]  Karl J. Friston,et al.  Willed action and the prefrontal cortex in man: a study with PET , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[32]  P. Costa,et al.  Stability and change in personality assessment: the revised NEO Personality Inventory in the year 2000. , 1997, Journal of personality assessment.

[33]  Gregory G. Brown,et al.  Error Rate and Outcome Predictability Affect Neural Activation in Prefrontal Cortex and Anterior Cingulate during Decision-Making , 2002, NeuroImage.

[34]  A. Damasio The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[36]  P. Lang,et al.  Affective information processing and the assessment of anxiety , 1984, Journal of behavioral assessment.

[37]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[38]  K. Mogg,et al.  Implicit and explicit memory for emotional information in non-clinical subjects. , 1994, Behaviour research and therapy.

[39]  P. Montague,et al.  A Computational Role for Dopamine Delivery in Human Decision-Making , 1998, Journal of Cognitive Neuroscience.

[40]  N. V. Lotova,et al.  Pre- and post-stimulus processes in affective task and event-related desynchronization (ERD): do they discriminate anxiety coping styles? , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  A. Henik,et al.  Controlling Stroop effects by manipulating expectations for color words , 1992, Memory & cognition.

[42]  Corianne Rogalsky,et al.  Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism , 2003, NeuroImage.

[43]  S. Reiss,et al.  Anxiety sensitivity, anxiety frequency and the prediction of fearfulness. , 1986, Behaviour research and therapy.

[44]  S. Stewart,et al.  The relations of trait anxiety, anxiety sensitivity, and sensation seeking to adolescents' motivations for alcohol, cigarette, and marijuana use. , 2001, Addictive behaviors.

[45]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

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

[47]  H. Critchley,et al.  Fear Conditioning in Humans The Influence of Awareness and Autonomic Arousal on Functional Neuroanatomy , 2002, Neuron.

[48]  C. MacLeod,et al.  Selective processing of threat cues in anxiety states. , 1985, Behaviour research and therapy.

[49]  W. Edwards,et al.  Response strategies in a two-choice reaction task with a continuous cost for time , 1971 .

[50]  F. Vollenweider,et al.  Decision-making strategies by panic disorder subjects are more sensitive to errors. , 2003, Journal of affective disorders.

[51]  Murray B Stein,et al.  Personality and anxiety disorders: a review. , 2003, Journal of personality disorders.

[52]  T. Robbins,et al.  Choosing between Small, Likely Rewards and Large, Unlikely Rewards Activates Inferior and Orbital Prefrontal Cortex , 1999, The Journal of Neuroscience.

[53]  D L Braff,et al.  Use of methods from chaos theory to quantify a fundamental dysfunction in the behavioral organization of schizophrenic patients. , 1996, The American journal of psychiatry.

[54]  Hanspeter Herzel,et al.  Correlations in DNA sequences: The role of protein coding segments , 1997 .

[55]  J. Allman,et al.  The Anterior Cingulate Cortex , 2001, Annals of the New York Academy of Sciences.

[56]  Matthew S Stanford,et al.  Impulsive and premeditated aggression: a factor analysis of self-reported acts , 1999, Psychiatry Research.

[57]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

[58]  Response units in the prediction of simple event patterns. , 1966, Journal of experimental psychology.

[59]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[60]  T. Palfai,et al.  Negative emotional expectancies and readiness to change among college student binge drinkers. , 2001, Addictive behaviors.

[61]  M. Raichle,et al.  Emotion-induced changes in human medial prefrontal cortex: I. During cognitive task performance. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[63]  M. Eysenck,et al.  Implicit and explicit memory bias in anxiety. , 1989, Journal of abnormal psychology.

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

[65]  R. Luce,et al.  Individual Choice Behavior: A Theoretical Analysis. , 1960 .

[66]  E. Fox,et al.  Mood-congruent free recall bias in anxiety. , 2001, Cognition & emotion.

[67]  W. Boucsein,et al.  The effect of chlordiazepoxide on the anticipation of electric shocks , 1976, Psychopharmacology.

[68]  K. Mogg,et al.  Attentional biases for negative information in induced and naturally occurring dysphoria. , 1997, Behaviour research and therapy.

[69]  J. Gray,et al.  Personality, punishment, and procedural learning: a test of J.A. Gray's anxiety theory. , 1997, Journal of personality and social psychology.

[70]  M. Botvinick,et al.  The Contribution of the Anterior Cingulate Cortex to Executive Processes in Cognition , 1999, Reviews in the neurosciences.

[71]  Monique Ernst,et al.  Decision-making in a Risk-taking Task: A PET Study , 2002, Neuropsychopharmacology.

[72]  Martin P Paulus,et al.  Error‐rate‐related caudate and parietal cortex activation during decision making , 2003, Neuroreport.

[73]  N. Schmidt,et al.  Prospective evaluation of anxiety sensitivity in the pathogenesis of panic: replication and extension. , 1999, Journal of abnormal psychology.

[74]  I. Blanchette,et al.  Anxiety and the interpretation of ambiguous information: beyond the emotion-congruent effect. , 2003, Journal of experimental psychology. General.

[75]  P. Lovibond,et al.  Expectancy bias in trait anxiety. , 1996, Journal of abnormal psychology.

[76]  K. Mogg,et al.  Attentional bias in anxiety and depression: the role of awareness. , 1995, The British journal of clinical psychology.

[77]  Karl J. Friston,et al.  Dissociable Neural Responses in Human Reward Systems , 2000, The Journal of Neuroscience.

[78]  K. Mogg,et al.  Selective processing of threat cues in anxiety states: a replication. , 1989, Behaviour research and therapy.

[79]  Adrian R. Willoughby,et al.  The Medial Frontal Cortex and the Rapid Processing of Monetary Gains and Losses , 2002, Science.

[80]  M. Zuckerman,et al.  Sensation seeking and the endogenous deficit theory of drug abuse. , 1986, NIDA research monograph.

[81]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[82]  J. Stirling,et al.  Vulnerability factors in the anxiety disorders. , 1998, The British journal of medical psychology.

[83]  Jonathan D. Cohen,et al.  A computational model of anterior cingulate function in speeded response tasks: Effects of frequency, sequence, and conflict , 2002, Cognitive, affective & behavioral neuroscience.

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

[85]  M. Eysenck,et al.  Phonological working memory and reading in test anxiety. , 1996, Memory.

[86]  A. Apkarian,et al.  Anxiety in healthy humans is associated with orbital frontal chemistry , 2000, Molecular Psychiatry.

[87]  N. Schmidt,et al.  The role of anxiety sensitivity in the pathogenesis of panic: prospective evaluation of spontaneous panic attacks during acute stress. , 1997, Journal of abnormal psychology.

[88]  Anxiety and memory , 1977 .

[89]  R. Duncan Luce,et al.  Individual Choice Behavior: A Theoretical Analysis , 1979 .

[90]  S. Mineka,et al.  Differential encoding of affective and nonaffective content information in trait anxiety , 2001 .

[91]  J. Newman,et al.  Testing Damasio's somatic marker hypothesis with psychopathic individuals: risk takers or risk averse? , 1999, Journal of abnormal psychology.

[92]  P. Matthews,et al.  Exacerbation of Pain by Anxiety Is Associated with Activity in a Hippocampal Network , 2001, The Journal of Neuroscience.

[93]  R. Atkinson,et al.  Two-choice behavior under limiting cases of contingent reinforcement schedules. , 1966, Journal of comparative and physiological psychology.

[94]  K. Mogg,et al.  Some methodological issues in assessing attentional biases for threatening faces in anxiety: a replication study using a modified version of the probe detection task. , 1999, Behaviour research and therapy.