Neural Biases to Covert and Overt Signals of Fear: Dissociation by Trait Anxiety and Depression

Although biases toward signals of fear may be an evolutionary adaptation necessary for survival, heightened biases may be maladaptive and associated with anxiety or depression. In this study, event-related potentials (ERPs) were used to examine the time course of neural responses to facial fear stimuli (versus neutral) presented overtly (for 500 msec with conscious attention) and covertly (for 10 msec with immediate masking to preclude conscious awareness) in 257 nonclinical subjects. We also examined the impact of trait anxiety and depression, assessed using psychometric ratings, on the time course of ERPs. In the total subject group, controlled biases to overtly processed fear were reflected in an enhancement of ERPs associated with structural encoding (120220 msec) and sustained evaluation persisting from 250 msec and beyond, following a temporo-occipital to frontal topography. By contrast, covert fear processing elicited automatic biases, reflected in an enhancement of ERPs prior to structural encoding (80180 msec) and again in the period associated with automatic orienting and emotion encoding (230330 msec), which followed the reverse frontal to temporo-occipital topography. Higher levels of trait anxiety (in the clinical range) were distinguished by a heightened bias to covert fear (speeding of early ERPs), compared to higher depression which was associated with an opposing bias to overt fear (slowing of later ERPs). Anxiety also heightened early responses to covert fear, and depression to overt fear, with subsequent deficits in emotion encoding in each case. These findings are consistent with neural biases to signals of fear which operate automatically and during controlled processing, feasibly supported by parallel networks. Heightened automatic biases in anxiety may contribute to a cycle of hypervigilance and anxious thoughts, whereas depression may represent a burnt out emotional state in which evaluation of fear stimuli is prolonged only when conscious attention is allocated.

[1]  H. Mayberg Limbic-cortical dysregulation: a proposed model of depression. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[2]  P. Lovibond,et al.  The structure of negative emotional states: comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. , 1995, Behaviour research and therapy.

[3]  Donna M. Palmer,et al.  Explicit identification and implicit recognition of facial emotions: I. Age effects in males and females across 10 decades , 2009, Journal of clinical and experimental neuropsychology.

[4]  R A Bryant,et al.  The generality of cognitive bias in acute stress disorder. , 2000, Behaviour research and therapy.

[5]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[6]  Z. Segal,et al.  A priming methodology for studying self-representation in major depressive disorder. , 1995, Journal of abnormal psychology.

[7]  E. Bernat,et al.  Event-related brain potentials differentiate positive and negative mood adjectives during both supraliminal and subliminal visual processing. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[8]  Leanne M Williams,et al.  The integrate model of emotion, thinking and self regulation: an application to the "paradox of aging". , 2008, Journal of integrative neuroscience.

[9]  M. Erb,et al.  Are emotions contagious? Evoked emotions while viewing emotionally expressive faces: quality, quantity, time course and gender differences , 2001, Psychiatry Research.

[10]  Ian H. Gotlib,et al.  Selective Attention in Dysphoric Individuals: The Role of Affective Interference and Inhibition , 2005, Cognitive Therapy and Research.

[11]  Dominique Lamy,et al.  Attentional bias in anxiety: A behavioral and ERP study , 2005, Brain and Cognition.

[12]  E. N. Sokolov,et al.  A psychophysiological model of emotion space , 2000, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[13]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[14]  Jutta Joormann,et al.  Attentional bias in dysphoria: The role of inhibitory processes , 2004 .

[15]  Leanne M Williams,et al.  An integrative neuroscience model of "significance" processing. , 2006, Journal of integrative neuroscience.

[16]  W. J. Williams,et al.  Conscious and nonconscious processes: an ERP index of an anticipatory response in a conditioning paradigm using visually masked stimuli. , 1994, Psychophysiology.

[17]  Leanne M Williams,et al.  Toward an integrated profile of depression: evidence from the brain resource international database. , 2005, Journal of integrative neuroscience.

[18]  Evian Gordon,et al.  A Direct Brainstem–amygdala–cortical Dalarmt System for Subliminal Signals of Fear , 2004 .

[19]  M. Thase,et al.  Can’t shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals , 2002, Biological Psychiatry.

[20]  Evian Gordon,et al.  Processing angry and neutral faces in post-traumatic stress disorder: an event-related potentials study , 2003, Neuroreport.

[21]  Leanne M Williams,et al.  Enhanced amygdala and medial prefrontal activation during nonconscious processing of fear in posttraumatic stress disorder: An fMRI study , 2008, Human brain mapping.

[22]  Le Song,et al.  The ‘when’ and ‘where’ of perceiving signals of threat versus non-threat , 2006, NeuroImage.

[23]  R. Lane,et al.  Levels of emotional awareness: a cognitive-developmental theory and its application to psychopathology. , 1987, The American journal of psychiatry.

[24]  Leanne M Williams,et al.  An "integrative neuroscience" platform: application to profiles of negativity and positivity bias. , 2008, Journal of integrative neuroscience.

[25]  W. Drevets Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders , 2001, Current Opinion in Neurobiology.

[26]  I. Gotlib,et al.  Construct accessibility and clinical depression: a longitudinal investigation. , 1987, Journal of abnormal psychology.

[27]  R A Bryant,et al.  Cognitive bias in acute stress disorder. , 1998, Behaviour research and therapy.

[28]  R. Ihl,et al.  Electrophysiological correlates of emotional and structural face processing in humans , 2000, Neuroscience Letters.

[29]  D L Woods,et al.  Hierarchical processing and level-repetition effect as indexed by early brain potentials. , 2000, Psychophysiology.

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

[31]  P. Lovibond,et al.  Manual for the Depression Anxiety Stress Scales. 2 , 1995 .

[32]  Arne Öhman,et al.  As fast as the blink of an eye: Evolutionary preparedness for preattentive processing of threat. , 1997 .

[33]  Luis Carretié,et al.  Valence-related vigilance biases in anxiety studied through event-related potentials. , 2004, Journal of affective disorders.

[34]  E. Gordon,et al.  A Temporal Dissociation of Subliminal versus Supraliminal Fear Perception: An Event-related Potential Study , 2004, Journal of Cognitive Neuroscience.

[35]  H. Kraemer,et al.  Facial emotion discrimination: II. Behavioral findings in depression , 1992, Psychiatry Research.

[36]  E Gordon,et al.  Eye movement and electrodermal responses to threat stimuli in post-traumatic stress disorder. , 1995, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[37]  K. Mogg,et al.  Biases in eye movements to threatening facial expressions in generalized anxiety disorder and depressive disorder. , 2000, Journal of abnormal psychology.

[38]  K. Mogg,et al.  Subliminal processing of emotional information in anxiety and depression. , 1993, Journal of abnormal psychology.

[39]  R. Bajcsy,et al.  A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies , 2002, Journal of Neuroscience Methods.

[40]  P. Ekman Emotion in the human face , 1982 .

[41]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[42]  K. Mogg,et al.  A cognitive-motivational analysis of anxiety. , 1998, Behaviour research and therapy.

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

[44]  E. Gordon,et al.  Integrative Neuroscience: The Role of a Standardized Database , 2005, Clinical EEG and neuroscience.

[45]  Richard B. Silberstein,et al.  Preliminary Electrophysiological Evidence For Modulation of the Processing of Negative Affect by Serotonin , 2003 .

[46]  C. H. Hansen,et al.  Finding the face in the crowd: an anger superiority effect. , 1988, Journal of personality and social psychology.

[47]  Steven A. Hillyard,et al.  Mechanisms and models of se-lective attention , 1995 .

[48]  Leanne M Williams,et al.  Amygdala–prefrontal dissociation of subliminal and supraliminal fear , 2006, Human brain mapping.

[49]  Robert F. Simons,et al.  Face processing biases in social anxiety: An electrophysiological study , 2008, Biological Psychology.

[50]  B. Jaffe Cognitive Therapy and the Emotional Disorders , 1977 .

[51]  M Esslen,et al.  Brain areas and time course of emotional processing , 2004, NeuroImage.

[52]  Matthew J. Barton,et al.  Neural Networks of Information Processing in Posttraumatic Stress Disorder: A Functional Magnetic Resonance Imaging Study , 2005, Biological Psychiatry.

[53]  T. Dalgleish,et al.  The emotional Stroop task and psychopathology. , 1996, Psychological bulletin.

[54]  Evian Gordon,et al.  Integrative Neuroscience in Psychiatry: The Role of a Standardized Database , 2003 .

[55]  M. Mintun,et al.  Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study , 2001, Biological Psychiatry.

[56]  J. Cacioppo,et al.  The affect system has parallel and integrative processing components: Form follows function. , 1999 .

[57]  Patrik Vuilleumier,et al.  Time course and specificity of event-related potentials to emotional expressions , 2004, Neuroreport.

[58]  O. John,et al.  Automatic vigilance: the attention-grabbing power of negative social information. , 1991, Journal of personality and social psychology.

[59]  Hannah Keage,et al.  Misinterpreting Emotional Expressions in Attention-Deficit/Hyperactivity Disorder: Evidence for a Neural Marker and Stimulant Effects , 2008, Biological Psychiatry.

[60]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[61]  K. Mogg,et al.  Selective processing of negative information: effects of clinical anxiety, concurrent depression, and awareness. , 1995, Journal of abnormal psychology.

[62]  Neil A. Macmillan,et al.  The psychophysics of subliminal perception , 1986, Behavioral and Brain Sciences.

[63]  J. Williams Cognitive Psychology and Emotional Disorders , 1991 .

[64]  C Lenti,et al.  Recognition of Emotional Facial Expressions in Depressed Children and Adolescents , 2000, Perceptual and motor skills.

[65]  Andrew H. Kemp,et al.  Trauma modulates amygdala and medial prefrontal responses to consciously attended fear , 2006, NeuroImage.

[66]  E. N. Sokolov,et al.  The dynamics of cortico-amygdala and autonomic activity over the experimental time course of fear perception. , 2004, Brain research. Cognitive brain research.

[67]  R A Bryant,et al.  Attentional bias in posttraumatic stress disorder. , 1997, Journal of traumatic stress.

[68]  Shelley E. Taylor,et al.  Asymmetrical effects of positive and negative events: the mobilization-minimization hypothesis. , 1991, Psychological bulletin.

[69]  D. Williamson,et al.  Evidence for attention to threatening stimuli in depression. , 1996, Behaviour research and therapy.