Anxiety and performance: the disparate roles of prefrontal subregions under maintained psychological stress.

Despite increasing interest in anxiety and psychological stress in daily life, little is known about neural correlates that underlie maintained psychological stress and their relationship with anxiety. In particular, the activation characteristics of lateral prefrontal subregions and their relationship with anxiety and cognitive performance under maintained psychological stress remain unknown. This study used near-infrared spectroscopy (NIRS), a noninvasive and "real-world" functional neuroimaging method, to investigate the hemodynamic responses in wide areas of the prefrontal cortex (PFC) and the influence of anxiety under conditions of maintained stress induced by a continuous arithmetic task (2 sets, 15 min each) performed in a natural sitting posture. Although anxiety and performance are not directly correlated, the hemodynamic response in the medial portion of the lateral PFC (dorsolateral and frontopolar PFC) was significantly associated with anxiety, while hemodynamic responses in the ventrolateral PFC were associated with performance. Additionally, in the same medial region of the lateral PFC, trait and state anxieties were related to changes in deoxy- and oxy-hemoglobin concentrations, respectively. This NIRS finding suggests disparate roles for prefrontal subregions in anxiety and performance under psychological stress and may lead to a better understanding of neural correlates for anxiety in everyday life.

[1]  S. Kurahashi,et al.  Development of the Uchida-Kraepelin psychodiagnostic test in Japan , 1957 .

[2]  David Badre,et al.  Cognitive control, hierarchy, and the rostro–caudal organization of the frontal lobes , 2008, Trends in Cognitive Sciences.

[3]  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.

[4]  A. Villringer,et al.  Decrease in parietal cerebral hemoglobin oxygenation during performance of a verbal fluency task in patients with Alzheimer's disease monitored by means of near-infrared spectroscopy (NIRS) — correlation with simultaneous rCBF-PET measurements , 1997, Brain Research.

[5]  T. Shors,et al.  Stress, anxiety, and dendritic spines: What are the connections? , 2013, Neuroscience.

[6]  D. Weinberger,et al.  Neocortical modulation of the amygdala response to fearful stimuli , 2003, Biological Psychiatry.

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

[8]  A. Villringer,et al.  Beyond the Visible—Imaging the Human Brain with Light , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[9]  Osamu Abe,et al.  Gender-common and -specific neuroanatomical basis of human anxiety-related personality traits. , 2008, Cerebral cortex.

[10]  T. Johnstone,et al.  Human amygdala responses during presentation of happy and neutral faces: correlations with state anxiety , 2004, Biological Psychiatry.

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

[12]  Makoto Ito,et al.  Decreased cortical reactivity underlies subjective daytime light sleepiness in healthy subjects: A multichannel near-infrared spectroscopy study , 2008, Neuroscience Research.

[13]  Y. Hoshi.  Functional near-infrared optical imaging: utility and limitations in human brain mapping. , 2003, Psychophysiology.

[14]  Marco Ferrari,et al.  A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application , 2012, NeuroImage.

[15]  M. D’Esposito.  Working memory. , 2008, Handbook of clinical neurology.

[16]  G. V. Van Hoesen,et al.  Prefrontal cortex in humans and apes: a comparative study of area 10. , 2001, American journal of physical anthropology.

[17]  Archana K. Singh,et al.  Exploring the false discovery rate in multichannel NIRS , 2006, NeuroImage.

[18]  M. Tamura,et al.  Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. , 2001, Journal of applied physiology.

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

[20]  S. Kühn,et al.  Structural correlates of trait anxiety: reduced thickness in medial orbitofrontal cortex accompanied by volume increase in nucleus accumbens. , 2011, Journal of affective disorders.

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

[22]  Olga V. Demler,et al.  Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. , 2005, Archives of general psychiatry.

[23]  J. Gabrieli,et al.  The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex , 2000, Psychobiology.

[24]  Masaki Kameyama,et al.  Sex and age dependencies of cerebral blood volume changes during cognitive activation: a multichannel near-infrared spectroscopy study , 2004, NeuroImage.

[25]  Lauri Tuominen,et al.  Temperament trait Harm Avoidance associates with μ-opioid receptor availability in frontal cortex: A PET study using [11C]carfentanil , 2012, NeuroImage.

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

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

[28]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[29]  John Duncan,et al.  State Anxiety Modulation of the Amygdala Response to Unattended Threat-Related Stimuli , 2004, The Journal of Neuroscience.

[30]  Eric R. Kandel,et al.  Individual Differences in Trait Anxiety Predict the Response of the Basolateral Amygdala to Unconsciously Processed Fearful Faces , 2004, Neuron.

[31]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[32]  Iroise Dumontheil,et al.  The gateway hypothesis of rostral prefrontal cortex (area 10) function , 2007, Trends in Cognitive Sciences.

[33]  Iole Indovina,et al.  Fear-Conditioning Mechanisms Associated with Trait Vulnerability to Anxiety in Humans , 2011, Neuron.

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

[35]  G. Glover,et al.  Biological Substrates of Emotional Reactivity and Regulation in Adolescence During an Emotional Go-Nogo Task , 2008, Biological Psychiatry.

[36]  E. Siegel,et al.  Cerebral blood flow and anxiety in older men: An analysis of resting anterior asymmetry and prefrontal regions , 2003, Brain and Cognition.

[37]  Mikio Iwase,et al.  Gender difference in relationship between anxiety-related personality traits and cerebral brain glucose metabolism , 2009, Psychiatry Research: Neuroimaging.

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

[39]  M. Eysenck,et al.  Effects of state anxiety on performance using a task-switching paradigm: An investigation of attentional control theory , 2009, Psychonomic bulletin & review.

[40]  Cloninger Cr,et al.  Temperament and personality. , 1994 .

[41]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[42]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[43]  P. Whalen,et al.  The Structural Integrity of an Amygdala–Prefrontal Pathway Predicts Trait Anxiety , 2009, The Journal of Neuroscience.

[44]  Nobumasa Kato,et al.  Effects of creatine on mental fatigue and cerebral hemoglobin oxygenation , 2002, Neuroscience Research.

[45]  Israel Liberzon,et al.  The Neurocircuitry of Fear, Stress, and Anxiety Disorders , 2011 .

[46]  D. Boas,et al.  Non-invasive neuroimaging using near-infrared light , 2002, Biological Psychiatry.

[47]  Jordan Grafman,et al.  Neural correlates of anxiety in healthy volunteers: a voxel-based morphometry study. , 2009 .

[48]  Masako Okamoto,et al.  Virtual spatial registration of stand-alone fNIRS data to MNI space , 2007, NeuroImage.

[49]  J. Detre,et al.  Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[50]  E. Gratton,et al.  Investigation of human brain hemodynamics by simultaneous near-infrared spectroscopy and functional magnetic resonance imaging. , 2001, Medical physics.

[51]  M. Fukuda,et al.  Subjective feeling of psychological fatigue is related to decreased reactivity in ventrolateral prefrontal cortex , 2009, Brain Research.

[52]  Luciano Mecacci,et al.  Anxiety, cognitive self-evaluation and performance: ERP correlates. , 2009, Journal of anxiety disorders.

[53]  M. Petrides.  Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  C. Summerfield,et al.  An information theoretical approach to prefrontal executive function , 2007, Trends in Cognitive Sciences.

[55]  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.

[56]  R. Hembree.  Correlates, Causes, Effects, and Treatment of Test Anxiety , 1988 .

[57]  C. R. Cloninger,et al.  A psychobiological model of temperament and character. , 1993, Archives of general psychiatry.

[58]  G Leone,et al.  Modulation of VLA-4 and L-selectin expression on normal CD34+ cells during mobilization with G-CSF , 1999, Bone Marrow Transplantation.