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Clinical anxiety promotes excessive response inhibition

Published online by Cambridge University Press:  25 October 2016

C. Grillon ,
O. J. Robinson ,
K. O'Connell ,
A. Davis ,
G. Alvarez ,
D. S. Pine  and
M. Ernst
C. Grillon*
Affiliation:
Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
O. J. Robinson
Affiliation:
Institute of Cognitive Neuroscience, University College London, London, UK
K. O'Connell
Affiliation:
Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
A. Davis
Affiliation:
Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
G. Alvarez
Affiliation:
Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
D. S. Pine
Affiliation:
Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD, USA
M. Ernst
Affiliation:
Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
*
*Address for correspondence: C. Grillon, Ph.D., Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, National Institutes of Health, North Drive, Building 15K, Room 203, MSC 2670, Bethesda, MD 20892-2670, USA. (Email: Christian.grillon@nih.gov)
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Abstract

Background

Laboratory tasks to delineate anxiety disorder features are used to refine classification and inform our understanding of etiological mechanisms. The present study examines laboratory measures of response inhibition, specifically the inhibition of a pre-potent motor response, in clinical anxiety. Data on associations between anxiety and response inhibition remain inconsistent, perhaps because of dissociable effects of clinical anxiety and experimentally manipulated state anxiety. Few studies directly assess the independent and interacting effects of these two anxiety types (state v. disorder) on response inhibition. The current study accomplished this goal, by manipulating state anxiety in healthy and clinically anxious individuals while they complete a response inhibition task.

Method

The study employs the threat-of-shock paradigm, one of the best-established manipulations for robustly increasing state anxiety. Participants included 82 adults (41 healthy; 41 patients with an anxiety disorder). A go/nogo task with highly frequent go trials was administered during alternating periods of safety and shock threat. Signal detection theory was used to quantify response bias and signal-detection sensitivity.

Results

There were independent effects of anxiety and clinical anxiety on response inhibition. In both groups, heightened anxiety facilitated response inhibition, leading to reduced nogo commission errors. Compared with the healthy group, clinical anxiety was associated with excessive response inhibition and increased go omission errors in both the safe and threat conditions.

Conclusions

Response inhibition and its impact on go omission errors appear to be a promising behavioral marker of clinical anxiety. These results have implications for a dimensional view of clinical anxiety.

Keywords

Anxietyanxiety disordersbehavioral inhibitiongo/nogothreat of shock
Type
Original Articles
Information
Psychological Medicine , Volume 47 , Issue 3 , February 2017 , pp. 484 - 494
Creative Commons
This is a work of the U.S. Government and is not subject to copyright protection in the United States.
Copyright
Copyright © Cambridge University Press 2016

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References

American Psychiatric Association (2000). Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR. American Psychiatric Association: Washington, DC.Google Scholar
Ansari, TL, Derakshan, N (2011). The neural correlates of impaired inhibitory control in anxiety. Neuropsychologia 49, 1146–1153.CrossRefGoogle ScholarPubMed
Ansari, TL, Derakshan, N, Richards, A (2008). Effects of anxiety on task switching: evidence from the mixed antisaccade task. Cognitive, Affective, and Behavioral Neuroscience 8, 229–238.Google Scholar
Aron, A (2011). From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biological Psychiatry 69, 55–68.CrossRefGoogle ScholarPubMed
Baas, JMP, Milstein, J, Donlevy, M, Grillon, C (2006). Brainstem correlates of defensive states in humans. Biological Psychiatry 59, 588–593.CrossRefGoogle ScholarPubMed
Bari, A, Robbins, TW (2013). Inhibition and impulsivity: behavioral and neural basis of response control. Progress in Neurobiology 108, 44–79.CrossRefGoogle ScholarPubMed
Beck, AT, Steer, RA (1987). BDI: Beck Depression Inventory. The Psychological Corporation, Harcourt Brace Jovanovich, Inc.: New York.Google Scholar
Beutel, ME, Stark, R, Pan, H, Silbersweig, D, Dietrich, S (2010). Changes of brain activation pre-post short-term psychodynamic inpatient psychotherapy: an fMRI study of panic disorder patients. Psychiatry Research: Neuroimaging 184, 96–104.CrossRefGoogle ScholarPubMed
Bijsterbosch, J, Smith, S, Bishop, SJ (2015). Functional connectivity under anticipation of shock: correlates of trait anxious affect versus induced anxiety. Journal of Cognitive Neuroscience 27, 1840–1853.Google Scholar
Buss, KA, Davidson, RJ, Kalin, NH, Goldsmith, HH (2004). Context-specific freezing and associated physiological reactivity as a dysregulated fear response. Developmental Psychology 40, 583–594.Google Scholar
Cornwell, BR, Baas, JMP, Johnson, L, Holroyd, T, Carver, FW, Lissek, S, Grillon, C (2007). Neural responses to auditory stimulus deviance under threat of electric shock revealed by spatially-filtered magnetoencephalography. NeuroImage 37, 282–289.CrossRefGoogle ScholarPubMed
Daugherty, TK, Quay, HC, Ramos, L (1993). Response perseveration, inhibitory control, and central dopaminergic activity in childhood behavior disorders. Journal of Genetic Psychology 154, 177–188.Google Scholar
Derakshan, N, Ansari, TL, Hansard, M, Shoker, L, Eysenck, MW (2009). Anxiety, inhibition, efficiency, and effectiveness. Experimental Psychology (formerly Zeitschrift für Experimentelle Psychologie) 56, 48–55.Google Scholar
Epstein, J, Johnson, D, Varia, I, Conners, CK (2001). Neuropsychological assessment of response inhibition in adults with ADHD. Journal of Clinical and Experimental Neuropsychology 23, 362–371.Google Scholar
Eysenck, MW, Derakshan, N, Santos, R, Calvo, MG (2007). Anxiety and cognitive performance: attentional control theory. Emotion 7, 336–353.CrossRefGoogle ScholarPubMed
Forster, S, Lavie, N (2014). Distracted by your mind? Individual differences in distractibility predict mind wandering. Journal of Experimental Psychology – Learning Memory and Cognition 40, 251–260.CrossRefGoogle ScholarPubMed
Geen, RG (1985). Test anxiety and visual vigilance. Journal of Personality and Social Psychology 49, 963–970.Google Scholar
Gold, JI, Shadlen, MN (2007). The neural basis of decision making. Annual Review of Neuroscience 30, 535–574.CrossRefGoogle ScholarPubMed
Gray, JA, McNaughton, N (2000). The Neuropsychology of Anxiety: An Inquiry into the Function of the Septo-Hippocampal System. Oxford University Press: Oxford.Google Scholar
Grillon, C, Baas, JM (2003). A review of the modulation of the startle reflex by affective states and its application to psychiatry. Clinical Neurophysiology 114, 1557–1579.CrossRefGoogle ScholarPubMed
Grillon, C, Robinson, O, Krimsky, M, O'Connell, K, Alvarez, G, Ernst, M (2016). Anxiety-mediated facilitation of behavioral inhibition: threat processing and defensive reactivity during a go/nogo task. Emotion. Published online 19 September 2016. doi:10.1037/emo0000214.Google Scholar
Hagenaars, MA, Oitzl, M, Roelofs, K (2014). Updating freeze: aligning animal and human research. Neuroscience and Biobehavioral Reviews 47, 165–176.Google Scholar
Hagopian, LP, Ollendick, TH (1994). Behavioral inhibition and test anxiety: an empirical investigation of Gray's theory. Personality and Individual Differences 16, 597–604.Google Scholar
Helton, WS (2009). Impulsive responding and the sustained attention to response task. Journal of Clinical and Experimental Neuropsychology 31, 39–47.Google Scholar
Insel, T, Cuthbert, B, Garvey, M, Heinssen, R, Pine, DS, Quinn, K, Sanislow, C, Wang, P (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. American Journal of Psychiatry 167, 748–751.Google Scholar
Kagan, J, Reznick, JS, Snidman, N (1988). Biological basis of childhood shyness. Science 240, 167–171.CrossRefGoogle Scholar
Karch, S, Jäger, L, Karamatskos, E, Graz, C, Stammel, A, Flatz, W, Lutz, J, Holtschmidt-Täschner, B, Genius, J, Leicht, G, Pogarell, O, Born, C, Möller, H-J, Hegerl, U, Reiser, M, Soyka, M, Mulert, C (2008). Influence of trait anxiety on inhibitory control in alcohol-dependent patients: simultaneous acquisition of ERPs and BOLD responses. Journal of Psychiatric Research 42, 734–745.Google Scholar
Kaye, JT, Bradford, DE, Curtin, JJ (2016). Psychometric properties of startle and corrugator response in NPU, affective picture viewing, and resting state tasks. Psychophysiology 53, 1241–1255.Google Scholar
Kim, JJ, Lee, HJ, Han, JS, Packard, MG (2001). Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. Journal of Neuroscience 21, 5222–5228.CrossRefGoogle ScholarPubMed
Kooijmans, R, Scheres, A, Oosterlaan, J (2000). Response inhibition and measures of psychopathology: a dimensional analysis. Child Neuropsychology 6, 175–184.Google Scholar
Li, CS, Chao, HH, Lee, TW (2009). Neural correlates of speeded as compared with delayed responses in a stop signal task: an indirect analog of risk taking and association with an anxiety trait. Cerebral Cortex 19, 839–848.CrossRefGoogle Scholar
Maack, DJ, Tull, MT, Gratz, KL (2012). Examining the incremental contribution of behavioral inhibition to generalized anxiety disorder relative to other Axis I disorders and cognitive–emotional vulnerabilities. Journal of Anxiety Disorders 26, 689–695.Google Scholar
McVay, JC, Kane, MJ (2009). Conducting the train of thought: working memory capacity, goal neglect, and mind wandering in an executive-control task. Journal of Experimental Psychology. Learning, Memory, and Cognition 35, 196–204.Google Scholar
McVay, JC, Meier, ME, Touron, DR, Kane, MJ (2013). Aging ebbs the flow of thought: adult age differences in mind wandering, executive control, and self-evaluation. Acta Psychologica 142, 136–147.CrossRefGoogle ScholarPubMed
Morgan, BE, van Honk, J, Hermans, EJ, Scholten, MRM, Stein, DJ, Kahn, RS (2009). Gray's BIS/BAS dimensions in non-comorbid, non-medicated social anxiety disorder. World Journal of Biological Psychiatry 10, 925–928.CrossRefGoogle ScholarPubMed
Neo, PSH, Thurlow, J, McNaughton, N (2011). Stopping, goal-conflict, trait anxiety and frontal rhythmic power in the stop-signal task. Cognitive, Affective and Behavioral Neuroscience 11, 485–493.Google Scholar
Oosterlaan, J, Sergeant, JA (1996). Inhibition in ADHD, aggressive, and anxious children: a biologically based model of child psychopathology. Journal of Abnormal Child Psychology 24, 19–36.Google Scholar
Peebles, D, Bothell, D (editors) (2004). Modelling Performance in the Sustained Attention to Response Task. Carnegie Mellon University/University of Pittsburgh: Pittsburgh, PA.Google Scholar
Pessoa, L, Padmala, S, Kenzer, A, Bauer, A (2012). Interactions between cognition and emotion during response inhibition. Emotion 12, 192–197.Google Scholar
Quay, H (1988). The behavioral reward and inhibition system in childhood behavior disorder. In Attention Deficit Disorder (ed. Bloomingdale, LM), pp. 176–186. Pergamon Press: Oxford, UK.Google Scholar
Quay, HC (1997). Inhibition and attention deficit hyperactivity disorder. Journal of Abnormal Child Psychology 25, 7–13.Google Scholar
Righi, S, Mecacci, L, Viggiano, M (2009). Anxiety, cognitive self-evaluation and performance: ERP correlates. Journal of Anxiety Disorders 23, 1132–1138.Google Scholar
Robinson, OJ, Krimsky, M, Grillon, C (2013 a). The impact of induced anxiety on response inhibition. Frontiers in Human Neuroscience 7, 69.Google Scholar
Robinson, OJ, Lieberman, L, Allen, P, Vytal, K, Grillon, C (2015). The dorsal medial prefrontal-amygdala ‘aversive amplification’ circuit in unmedicated generalized and social anxiety disorders. Lancet Psychiatry 1, 294–302.CrossRefGoogle Scholar
Robinson, OJ, Vytal, K, Cornwell, BR, Grillon, C (2013 b). The impact of anxiety upon cognition: perspectives from human threat of shock studies. Frontiers in Human Neuroscience 7, 203.CrossRefGoogle ScholarPubMed
Roelofs, K, van Peer, J, Berretty, E, Jong, Pd, Spinhoven, P, Elzinga, BM (2009). Hypothalamus–pituitary–adrenal axis hyperresponsiveness is associated with increased social avoidance behavior in social phobia. Biological Psychiatry 65, 336–343.Google Scholar
Rosenbaum, JF, Biederman, J, Hirshfeld, DR, Bolduc, EA, Faraone, SV, Kagan, J, Snidman, N, Reznick, JS (1991). Further evidence of an association between behavioral inhibition and anxiety disorders – results from a family study of children from a non-clinical sample. Journal of Psychiatry Research 25, 49–65.Google Scholar
Saucedo Marquez, CM, Zhang, X, Swinnen, SP, Meesen, R, Wenderoth, N (2013). Task-specific effect of transcranial direct current stimulation on motor learning. Frontiers in Human Neuroscience 7, 333.Google Scholar
Schwabe, L, Dalm, S, Schächinger, H, Oitzl, MS (2008). Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiology of Learning and Memory 90, 495–503.Google Scholar
Schwabe, L, Wolf, OT (2009). Stress prompts habit behavior in humans. Journal of Neuroscience 29, 7191–7198.CrossRefGoogle ScholarPubMed
Sehlmeyer, C, Konrad, C, Zwitserlood, P, Arolt, V, Falkenstein, M, Beste, C (2010). ERP indices for response inhibition are related to anxiety-related personality traits. Neuropsychologia 48, 2488–2495.Google Scholar
Seli, P (2016). The attention-lapse and motor decoupling accounts of SART performance are not mutually exclusive. Consciousness and Cognition 41, 189–198.Google Scholar
Seli, P, Risko, EF, Smilek, D (2016). On the necessity of distinguishing between unintentional and intentional mind wandering. Psychological Science 27, 685–691.Google Scholar
Smallwood, J (2013). Penetrating the fog of the decoupled mind: the effects of visual salience in the sustained attention to response task. Canadian Journal of Experimental Psychology 67, 32–40.CrossRefGoogle ScholarPubMed
Snodgrass, JG, Corwin, J (1988). Pragmatics of measuring recognition memory: applications to dementia and amnesia. Journal of Experimental Psychology: General 117, 34–50.Google Scholar
Spielberger, CD (1983). Manual for the State-Trait Anxiety Inventory. Consulting Psychologist Press: Palo Alto, CA.Google Scholar
Stuss, DT, Shallice, T, Alexander, MP, Picton, TW (1995). A multidisciplinary approach to anterior attentional functions. Annals of the New York Academy of Sciences 769, 191–212.Google Scholar
Sylwan, RP (2004). The control of deliberate waiting strategies in a stop-signal task. Brazilian Journal of Medical and Biological Research 37, 853–862.Google Scholar
Thomas, SJ, Gonsalvez, CJ, Johnstone, SJ (2016). Electrophysiology of facilitation priming in obsessive–compulsive and panic disorders. Clinical Neurophysiology 127, 464–478.Google Scholar
Vuilleumier, P (2005). How brains beware: neural mechanisms of emotional attention. Trends in Cognitive Science 9, 585–594.Google Scholar
Wright, L, Lipszyc, J, Dupuis, A, Thayapararajah, S, Schachar, R (2014). Response inhibition and psychopathology: a meta-analysis of go/no-go task performance. Journal of Abnormal Psychology 123, 429–439.Google Scholar
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