Neural Control of Vascular Reactions: Impact of Emotion and Attention

This study investigated the neural regions involved in blood pressure reactions to negative stimuli and their possible modulation by attention. Twenty-four healthy human subjects (11 females; age = 24.75 ± 2.49 years) participated in an affective perceptual load task that manipulated attention to negative/neutral distractor pictures. fMRI data were collected simultaneously with continuous recording of peripheral arterial blood pressure. A parametric modulation analysis examined the impact of attention and emotion on the relation between neural activation and blood pressure reactivity during the task. When attention was available for processing the distractor pictures, negative pictures resulted in behavioral interference, neural activation in brain regions previously related to emotion, a transient decrease of blood pressure, and a positive correlation between blood pressure response and activation in a network including prefrontal and parietal regions, the amygdala, caudate, and mid-brain. These effects were modulated by attention; behavioral and neural responses to highly negative distractor pictures (compared with neutral pictures) were smaller or diminished, as was the negative blood pressure response when the central task involved high perceptual load. Furthermore, comparing high and low load revealed enhanced activation in frontoparietal regions implicated in attention control. Our results fit theories emphasizing the role of attention in the control of behavioral and neural reactions to irrelevant emotional distracting information. Our findings furthermore extend the function of attention to the control of autonomous reactions associated with negative emotions by showing altered blood pressure reactions to emotional stimuli, the latter being of potential clinical relevance.

[1]  Jan Gläscher,et al.  Visualization of Group Inference Data in Functional Neuroimaging , 2009, Neuroinformatics.

[2]  Hugo D. Critchley,et al.  Following One's Heart: Cardiac Rhythms Gate Central Initiation of Sympathetic Reflexes , 2009, The Journal of Neuroscience.

[3]  K. Amunts,et al.  Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps , 2005, Anatomy and Embryology.

[4]  L. Laux,et al.  Das State-Trait-Angstinventar. Theoretische Grundlagen and Handanweisung. , 1981 .

[5]  Karl J. Friston,et al.  Stochastic Designs in Event-Related fMRI , 1999, NeuroImage.

[6]  Cheree James,et al.  Identification of sites of sympathetic outflow at rest and during emotional arousal: concurrent recordings of sympathetic nerve activity and fMRI of the brain. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[7]  A. Villringer,et al.  Sexual dimorphism in the human brain: evidence from neuroimaging. , 2013, Magnetic resonance imaging.

[8]  Christian Büchel,et al.  Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans , 2010, Proceedings of the National Academy of Sciences.

[9]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[10]  Cheree James,et al.  Real-time imaging of cortical and subcortical control of muscle sympathetic nerve activity in awake human subjects , 2013, NeuroImage.

[11]  Alexandru D. Iordan,et al.  Neural signatures of the response to emotional distraction: a review of evidence from brain imaging investigations , 2013, Front. Hum. Neurosci..

[12]  Elizabeth A. Phelps,et al.  Insula and Orbital Frontal Cortex Activity Underlying Emotion Interference Resolution in Working Memory , 2010, Journal of Cognitive Neuroscience.

[13]  M. Bradley,et al.  Aversive picture processing: effects of a concurrent task on sustained defensive system engagement. , 2011, Psychophysiology.

[14]  J. Gläscher,et al.  Independent Effects of Emotion and Working Memory Load on Visual Activation in the Lateral Occipital Complex , 2007, The Journal of Neuroscience.

[15]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

[16]  S. Manuck,et al.  Acute psychophysiologic reactivity and risk of cardiovascular disease: a review and methodologic critique. , 1984, Psychological bulletin.

[17]  J. Richard Jennings,et al.  Is the brain the essential in hypertension? , 2009, NeuroImage.

[18]  Orrin Devinsky,et al.  Role of the left amygdala and right orbital frontal cortex in emotional interference resolution facilitation in working memory , 2011, Neuropsychologia.

[19]  G. Gravlee,et al.  Accuracy of four indirect methods of blood pressure measurement, with hemodynamic correlations , 1990, Journal of Clinical Monitoring.

[20]  James J Gross,et al.  The temporal dynamics of two response-focused forms of emotion regulation: experiential, expressive, and autonomic consequences. , 2011, Psychophysiology.

[21]  Cheree James,et al.  Autonomic markers of emotional processing: skin sympathetic nerve activity in humans during exposure to emotionally charged images , 2012, Front. Physio..

[22]  Peter Schulz,et al.  Trierer Inventar zur Erfassung von chronischem Streß (TICS): Skalenkonstruktion, teststatistische Überprüfung und Validierung der Skala Arbeitsüberlastung , 1999 .

[23]  A. Sherwood,et al.  Hemodynamics of blood pressure responses during active and passive coping. , 1990, Psychophysiology.

[24]  Peter J. Gianaros,et al.  Higher blood pressure predicts lower regional grey matter volume: Consequences on short-term information processing , 2006, NeuroImage.

[25]  David R. Williams,et al.  Blood Pressure Reactivity to Psychological Stress Predicts Hypertension in the CARDIA Study , 2004, Circulation.

[26]  lotte van dillen,et al.  Working memory load reduces facilitated processing of threatening faces: an ERP study. , 2012, Emotion.

[27]  Ludovico Minati,et al.  Emotional modulation of visual cortex activity: a functional near-infrared spectroscopy study , 2009, Neuroreport.

[28]  P. Lang International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[29]  Martin Baruch,et al.  The Structure of the Radial Pulse - A Novel Noninvasive Ambulatory Blood Pressure Device , 2007, MMVR.

[30]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Noga Cohen,et al.  Dynamic modulation of emotional processing , 2013, Biological Psychology.

[32]  Ahmad R. Hariri,et al.  Preclinical Atherosclerosis Covaries with Individual Differences in Reactivity and Functional Connectivity of the Amygdala , 2009, Biological Psychiatry.

[33]  L. Pessoa How do emotion and motivation direct executive control? , 2009, Trends in Cognitive Sciences.

[34]  Gilles Pourtois,et al.  Temporal precedence of emotion over attention modulations in the lateral amygdala: Intracranial ERP evidence from a patient with temporal lobe epilepsy , 2010, Cognitive, affective & behavioral neuroscience.

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

[36]  J. Suls,et al.  Reproducibility of blood pressure and heart rate reactivity: a meta-analysis. , 1996, Psychophysiology.

[37]  Cheree James,et al.  Real-time imaging of cortical areas involved in the generation of increases in skin sympathetic nerve activity when viewing emotionally charged images , 2012, NeuroImage.

[38]  H. Okon-Singer,et al.  Distinguishing between automaticity and attention in the processing of emotionally significant stimuli. , 2007, Emotion.

[39]  H. Critchley,et al.  Brain systems for baroreflex suppression during stress in humans , 2012, Human brain mapping.

[40]  Peter J. Gianaros,et al.  A review of neuroimaging studies of stressor-evoked blood pressure reactivity: Emerging evidence for a brain-body pathway to coronary heart disease risk , 2009, NeuroImage.

[41]  M. Bradley,et al.  Looking at pictures: affective, facial, visceral, and behavioral reactions. , 1993, Psychophysiology.

[42]  P. Lang,et al.  Fear and anxiety: animal models and human cognitive psychophysiology. , 2000, Journal of affective disorders.

[43]  Jennifer A. Silvers,et al.  Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion , 2012, Annals of the New York Academy of Sciences.

[44]  C. M. Adkins,et al.  Pulse Decomposition Analysis of the digital arterial pulse during hemorrhage simulation , 2011, Nonlinear biomedical physics.

[45]  Jason A. Oliver,et al.  The smoking N-back: a measure of biased cue processing at varying levels of cognitive load. , 2011, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[46]  Antonio Schettino,et al.  rain mechanisms for emotional influences on perception and attention : hat is magic and what is not , 2012 .

[47]  Gabriele Lohmann,et al.  Within-subject variability of BOLD response dynamics , 2003, NeuroImage.

[48]  Swann Pichon,et al.  Threat prompts defensive brain responses independently of attentional control. , 2012, Cerebral cortex.

[49]  I. Christie,et al.  Heightened Resting Neural Activity Predicts Exaggerated Stressor-Evoked Blood Pressure Reactivity , 2009, Hypertension.

[50]  C. Büchel,et al.  Separate amygdala subregions signal surprise and predictiveness during associative fear learning in humans , 2013, The European journal of neuroscience.