Abstract
Functional near-infrared (fNIR) spectroscopy is a promising new technology that has demonstrated utility in the study of normal human cognition. We utilized fNIR spectroscopy to examine the effect of social anxiety and performance on hemodynamic activity in the dorsolateral prefrontal cortex (DLPFC). Socially phobic participants and non-clinical participants with varying levels of social anxiety completed a public speaking task in front of a small virtual audience while the DLPFC was being monitored by the fNIR device. The relationship between anxiety and both blood volume (BV) and deoxygenated hemoglobin (Hb) varied significantly as a function of speech performance, such that individuals with low social anxiety who performed well showed an increase in DLPFC activation relative to those who did not perform well. This result suggests that effortful thinking and/or efficient top-down inhibitory control may have been required to complete an impromptu speech task with good performance. In contrast, good performers who were highly socially anxious showed lower DLPFC activation relative to good performers who were low in social anxiety, suggesting autopilot thinking or less-effortful thinking. In poor performers, slight increases in DLPFC activation were observed from low to highly anxious individuals, which may reflect a shift from effortless thinking to heightened self-focused attention. Heightened self-focused attention, poor inhibitory control resulting in excessive fear or anxiety, or low motivation may lower performance. These results suggest that there can be different underlying mechanisms in the brain that affect the level of speech performance in individuals with varying degrees of social anxiety. This study highlights the utility of the fNIR device in the assessment of changes in DLPFC in response to exposure to realistic phobic stimuli, and further supports the potential utility of this technology in the study of the neurophysiology of anxiety disorders.
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Audenaert, K., Brans, B., Van Laere, K., Lahorte, P., Versijpt, J., van Heeringen, K., et al. (2000). Verbal fluency as a prefrontal activation probe: a validation study using 99mTc-ECD brain SPET. European Journal of Nuclear Medicine, 27(12), 1800–1808.
Beaudreau, S. A., & O'Hara, R. (2009). The association of anxiety and depressive symptoms with cognitive performance in community-dwelling older adults. Psychology and Aging., 24(2), 507–512.
Beidel, D. C., Borden, J. W., Turner, S. M., & Jacob, R. G. (1989). The Social Phobia and Anxiety Inventory: Concurrent validity with a clinic sample. Behaviour Research and Therapy, 27(5), 573–576.
Benton, A. L., Hamsher, K. D., & Sivan, A. B. (1994). Multilingual aphasia examination: manual of instructions: AJA Assoc.
Blair, K. S., Geraci, M., Hollon, N., Otero, M., DeVido, J., Majestic, C., et al. (2010). Social norm processing in adult social phobia: atypically increased ventromedial frontal cortex responsiveness to unintentional (embarrassing) transgressions. American Journal of Psychiatry, 167(12), 1526–1532.
Boehme, S., Mohr, A., Becker, M., Miltner, W., & Straube, T. (2014). Area-dependent time courses of brain activation during video-induced symptom provocation in social anxiety disorder. Biology of Mood & Anxiety Disord, 4(6).
Braver, T. S., Reynolds, J. R., & Donaldson, D. I. (2003). Neural mechanisms of transient and sustained cognitive control during task switching. Neuron, 39(4), 713–726.
Cohen, J., & Cohen, P. (1983). Applied multiple regression/correlation analysis for the behavioral sciences (2nd ed.). Hillsdale: Erlbaum.
Cui, X., Bray, S., Bryant, D. M., Glover, G. H., & Reiss, A. L. (2011). A quantitative comparison of NIRS and fMRI across multiple cognitive tasks. NeuroImage, 54(4), 2808–2821.
DiGirolamo, G. J., Kramer, A. F., Barad, V., Cepeda, N. J., Weissman, D. H., Milham, M. P., et al. (2001). General and task-specific frontal lobe recruitment in older adults during executive processes: a fMRI investigation of task-switching. Neuroreport, 12(9), 2065–2071.
Duval, E. R., Javanbakht, A., & Liberzon, I. (2015). Neural circuits in anxiety and stress disorders: a focused review. Therapeutics and Clinical Risk Management, 11, 115.
Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry, 164(10), 1476–1488. doi:10.1176/appi.ajp.2007.07030504.
Fletcher, P., Shallice, T., Frith, C., Frackowiak, R., & Dolan, R. (1996). Brain activity during memory retrieval. Brain, 119(5), 1587–1596.
Freitas-Ferrari, M. C., Hallak, J. E., Trzesniak, C., Filho, A. S., Machado-de-Sousa, J. P., Chagas, M. H., et al. (2010). Neuroimaging in social anxiety disorder: a systematic review of the literature. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 34(4), 565–580. doi:10.1016/j.pnpbp.2010.02.028.
Gagnon, G., Blanchet, S., Grondin, S., & Schneider, C. (2010). Paired-pulse transcranial magnetic stimulation over the dorsolateral prefrontal cortex interferes with episodic encoding and retrieval for both verbal and non-verbal materials. Brain Research, 1344, 148–158.
Glassman, L. H., Herbert, J. D., Forman, E. M., Bradley, L. E., Izzetoglu, M., Ruocco, A. C., et al. (2014). Near-infrared spectroscopic assessment of in vivo prefrontal activation in public speaking anxiety: a preliminary study. Psychology of Consciousness: Theory, Research, and Practice, 1(3), 271–283. doi:10.1037/cns0000009.
Grant, B. E., Hasin, D. S., Blanco, C., Stinson, F. S., Chou, S. P., Goldstein, R. B., et al. (2005). The epidemiology of social anxiety disorder in the United States: Results from the national epidemiologic survey on alcohol and related conditions (Vol. 66). Memphis: Physicians Postgraduate Press.
Guyer, A. E., Lau, J. Y., McClure-Tone, E. B., Parrish, J., Shiffrin, N. D., Reynolds, R. C., et al. (2008). Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Archives of General Psychiatry, 65(11), 1303–1312. doi:10.1001/archpsyc.65.11.1303.
Henson, R., Shallice, T., & Dolan, R. (1999). Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. Brain, 122(7), 1367–1381.
Hopko, D. R., McNeil, D. W., Zvolensky, M. J., & Eifert, G. H. (2002). The relation between anxiety and skill in performance-based anxiety disorders: a behavioral formulation of social phobia. Behavior Therapy, 32(1), 185–207.
Izzetoglu, K. (2008). Neural correlates of cognitive workload and anesthetic depth: fNIR spectroscopy investigation in humans (Unpublished doctoral dissertation). Drexel University, Philadelphia, PA.
Kennan, R. P., Kim, D., Maki, A., Koizumi, H., & Constable, R. T. (2002). Non-invasive assessment of language lateralization by transcranial near infrared optical topography and functional MRI. Human Brain Mapping, 16(3), 183–189.
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62(6), 593–602. doi:10.1001/archpsyc.62.6.593.
Levitan, M. N., & Nardi, A. E. (2009). Social skill deficits in socially anxious subjects. The World Journal of Biological Psychiatry, 10(4–3), 702–709.
MacDonald, A. W., Cohen, J. D., Stenger, V. A., & Carter, C. S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288(5472), 1835–1838.
Mendlowicz, M. V., & Stein, M. B. (2010). Quality of life in individuals with anxiety disorders. American Journal of Psychiatry, 157(5), 669–682.
Ochsner, K. N., & Gross, J. J. (2008). Cognitive emotion regulation insights from social cognitive and affective neuroscience. Current Directions in Psychological Science, 17(2), 153–158.
Rapee, R. M., & Lim, L. (1992). Discrepancy between self- and observer ratings of performance in social Phobics. Journal of Abnormal Psychology, 101(4), 728–731.
Ridderinkhof, K. R., van den Wildenberg, W. P., Segalowitz, S. J., & Carter, C. S. (2004). Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain and Cognition, 56(2), 129–140.
Ruff, R. M., Light, R. H., Parker, S. B., & Levin, H. S. (1996). Benton controlled oral word association test: Reliability and updated norms. Archives of Clinical Neuropsychology, 11(4), 329–338.
Stopa, L., & Clark, D. M. (1993). Cognitive processes in social phobia. Behaviour Research and Therapy, 31(3), 255–267.
Tillfors, M., Furmark, T., Marteinsdottir, I., & Fredrikson, M. (2002). Cerebral blood flow during anticipation of public speaking in social phobia: a PET study. Biological Psychiatry, 52(11), 1113–1119.
Tillfors, M., Furmark, T., Marteinsdottir, I., Fischer, H., Pissiota, A., Långström, B., & Fredrikson, M. (2014). Cerebral blood flow in subjects with social phobia during stressful speaking tasks: a PET study. American Journal of Psychiatry 158(11), 1113–1119.
Toronov, V., Webb, A., Choi, J. H., Wolf, M., Michalos, A., Gratton, E., et al. (2001). Investigation of human brain hemodynamics by simultaneous near-infrared spectroscopy and functional magnetic resonance imaging. Medical Physics, 28, 521.
Turner, S. M., Beidel, D. C., Dancu, C. V., & Stanley, M. A. (1989). An empirically derived inventory to measure social fears and anxiety: the social phobia and anxiety inventory. Psychological Assessment: A Journal of Consulting and Clinical Psychology, 1(1), 35.
Tuscan, L. A., Herbert, J. D., Forman, E. M., Juarascio, A. S., Izzetoglu, M., & Schultheis, M. (2013). Exploring frontal asymmetry using functional near-infrared spectroscopy: a preliminary study of the effects of social anxiety during interaction and performance tasks. Brain Imaging and Behavior, 7(2), 140–153.
Villringer, A., & Chance, B. (1997). Non-invasive optical spectroscopy and imaging of human brain function. Trends in Neurosciences, 20(10), 435–442.
Wolpe, J., & Lazarus, A. A. (1966). Behavior therapy techniques. New York: Pergamon.
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The imaging device used in this study is manufactured by fNIR Devices, LLC. This company is associated with Drexel and the technology and software development have been disclosed and protected by the University. Meltem Izzetoglu (our fifth author) has an ownership interest in this company.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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Informed consent was obtained from all individual participants included in the study.
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An erratum to this article is available at http://dx.doi.org/10.1007/s11682-017-9740-9.
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Glassman, L.H., Kuster, A.T., Shaw, J.A. et al. The relationship between dorsolateral prefrontal activation and speech performance-based social anxiety using functional near infrared spectroscopy. Brain Imaging and Behavior 11, 797–807 (2017). https://doi.org/10.1007/s11682-016-9554-1
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DOI: https://doi.org/10.1007/s11682-016-9554-1