When neutral is not neutral: Neurophysiological evidence for reduced discrimination between aversive and non-aversive information in generalized anxiety disorder

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Abstract

Generalized anxiety disorder (GAD) is characterized by a range of cognitive and affective disruptions, such as pathological worry. There is debate, however, about whether such disruptions are specifically linked to heightened responses to aversive stimuli, or due to overgeneralized threat monitoring leading to deficits in the ability to discriminate between aversive and non-aversive affective information. The present study capitalized on the temporal and functional specificity of scalp-recorded event-related potentials (ERPs) to examine this question by exploring two targeted neurocognitive responses in a group of adults diagnosed with GAD: 1) visual processing of angry (aversive) versus neutral (non-aversive) faces; and 2) response monitoring of incorrect (aversive) versus correct (non-aversive) responses. Electroencephalography was recorded while 15 adults with GAD and 15 age-matched controls viewed angry and neutral faces prior to individual trials of a flanker task. ERPs to faces were the P1, reflecting attention allocation, the early posterior negativity (EPN), reflecting early affective discrimination, and the N170, reflecting face-sensitive visual discrimination. The error-related negativity (ERN) and positivity (Pe) were generated to incorrect and correct responses. Results showed reduced discrimination between aversive and non-aversive faces and responses in the GAD relative to the control group during visual discrimination (N170) and later-emerging error monitoring (Pe). These effects were driven by exaggerated processing of non-aversive faces and responses, suggesting over-generalized threat monitoring. Implications for cognitive-affective models of GAD are discussed.

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Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging.

Patrik Vuilleumier, Gilles Pourtois (2007)

Brain imaging studies in humans have shown that face processing in several areas is modulated by the affective significance of faces, particularly with fearful expressions, but also with other social signals such gaze direction. Here we review haemodynamic and electrical neuroimaging results indicating that activity in the face-selective fusiform cortex may be enhanced by emotional (fearful) expressions, without explicit voluntary control, and presumably through direct feedback connections from the amygdala. fMRI studies show that these increased responses in fusiform cortex to fearful faces are abolished by amygdala damage in the ipsilateral hemisphere, despite preserved effects of voluntary attention on fusiform; whereas emotional increases can still arise despite deficits in attention or awareness following parietal damage, and appear relatively unaffected by pharmacological increases in cholinergic stimulation. Fear-related modulations of face processing driven by amygdala signals may implicate not only fusiform cortex, but also earlier visual areas in occipital cortex (e.g., V1) and other distant regions involved in social, cognitive, or somatic responses (e.g., superior temporal sulcus, cingulate, or parietal areas). In the temporal domain, evoked-potentials show a widespread time-course of emotional face perception, with some increases in the amplitude of responses recorded over both occipital and frontal regions for fearful relative to neutral faces (as well as in the amygdala and orbitofrontal cortex, when using intracranial recordings), but with different latencies post-stimulus onset. Early emotional responses may arise around 120ms, prior to a full visual categorization stage indexed by the face-selective N170 component, possibly reflecting rapid emotion processing based on crude visual cues in faces. Other electrical components arise at later latencies and involve more sustained activities, probably generated in associative or supramodal brain areas, and resulting in part from the modulatory signals received from amygdala. Altogether, these fMRI and ERP results demonstrate that emotion face perception is a complex process that cannot be related to a single neural event taking place in a single brain regions, but rather implicates an interactive network with distributed activity in time and space. Moreover, although traditional models in cognitive neuropsychology have often considered that facial expression and facial identity are processed along two separate pathways, evidence from fMRI and ERPs suggests instead that emotional processing can strongly affect brain systems responsible for face recognition and memory. The functional implications of these interactions remain to be fully explored, but might play an important role in the normal development of face processing skills and in some neuropsychiatric disorders.

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Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task.

Sander Nieuwenhuis, K. Ridderinkhof, Jos Blom … (2001)

The error negativity (Ne/ERN) and error positivity (Pe) are two components of the event-related brain potential (ERP) that are associated with action monitoring and error detection. To investigate the relation between error processing and conscious self-monitoring of behavior, the present experiment examined whether an Ne and Pe are observed after response errors of which participants are unaware. Ne and Pe measures, behavioral accuracy, and trial-to-trial subjective accuracy judgments were obtained from participants performing an antisaccade task, which elicits many unperceived, incorrect reflex-like saccades. Consistent with previous research, subjectively unperceived saccade errors were almost always immediately corrected, and were associated with faster correction times and smaller saccade sizes than perceived errors. Importantly, irrespective of whether the participant was aware of the error or not, erroneous saccades were followed by a sizable Ne. In contrast, the Pe was much more pronounced for perceived than for unperceived errors. Unperceived errors were characterized by the absence of posterror slowing. These and other results are consistent with the view that the Ne and Pe reflect the activity of two separate error monitoring processes, of which only the later process, reflected by the Pe, is associated with conscious error recognition and remedial action.