Early Affective Processing in Patients with Acute Posttraumatic Stress Disorder: Magnetoencephalographic Correlates

Burgmer, Markus; Rehbein, Maimu Alissa; Wrenger, Marco; Kandil, Judith; Heuft, Gereon; Steinberg, Christian; Pfleiderer, Bettina; Junghöfer, Markus

doi:10.1371/journal.pone.0071289

Cited by 10 publications

(12 citation statements)

References 72 publications

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“…Our result provides additional support for EPN suppression also using pleasant emotional material. This matches well with Adenauer, Pinosch et al () and Burgmer et al (), confirming a reduced differential responding not only to unpleasant, but also to pleasant visual stimuli in PTSD.…”

Section: Discussionsupporting

confidence: 91%

“…Likewise, these findings are in line with the concept of natural selective attention (Bradley, ), as the perceptual processing of emotional stimuli seems facilitated. However, prior work has shown that ERPs during affective processing can be deviant in individuals with psychiatric disorders (Adenauer, Pinosch et al, ; Burgmer et al, ; Elbert et al, ; Felmingham, Bryant, & Gordon, ; Holmes, Nielsen, & Green, ; Kemp et al, ; Matz et al, ; Rockstroh, Junghöfer, Elbert, Buodo, & Miller, ; Weber et al, ). In the current study, psychopathological symptom clusters were identified using PCA.…”

Section: Discussionmentioning

confidence: 99%

“…In major depressive disorder, a reduced arousal modulation of the right temporo‐parietal activation evoked by visual stimuli was found (Moratti, Rubio, Campo, Keil, & Ortiz, ). Modulated early visual processing of emotional stimuli was also recorded in individuals suffering from post‐traumatic stress disorder (PTSD), depression symptoms, and dissociation (Adenauer, Pinosch et al, ; Burgmer et al, ; Elbert et al, ; Keil, Adenauer, Catani, & Neuner, ; Schalinski, Moran, Schauer, & Elbert, ). Such deviations in neural activity are assumed to be characteristic for this psychopathology.…”

Section: Introductionmentioning

confidence: 99%

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Rapid brain responses to affective pictures indicate dimensions of trauma‐related psychopathology in adolescents

et al. 2019

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A variety of mental disorders are related to deviant brain activity, but these neural alterations do not validate psychiatric diagnostic categories. High symptom overlap and variable symptom patterns encourage a dimensional approach. Following the logic of the Research Domain Criteria (RDoC), we investigated trauma survivors for symptom clusters that might be associated with characteristics of ERPs, in particular with the early posterior negativity (EPN) elicited during affective picture processing. In rapid serial visual presentation, 90 adolescents (40 male/50 female, age M = 15.0 ± 2.5 years) who had been exposed to varying amounts of traumatic stress passively viewed a stream of high‐arousing positive and low‐arousing neutral pictures taken from the International Affective Picture System (IAPS). Using standardized interviews, symptoms of trauma‐related mental disorders were assessed (including those for PTSD, depression, borderline personality disorder, and behavioral problems). A principal component analysis was performed to derive potential dimensions of psychopathology. Multiple regression analysis confirmed a factor comprising problems concentrating, sleeping difficulties, and mistrust as a predictor of a larger EPN difference between high‐arousing positive and low‐arousing neutral IAPS pictures (β = 0.19, p < 0.05). Sex predicted the magnitude of the EPN (β = 0.45, p < 0.001). Male adolescents displayed a stronger EPN suppression than female adolescents. The result suggests that problems concentrating, sleeping difficulties, and mistrust seem to be trans‐diagnostic elements related to diminished early emotional discrimination represented by the EPN. Furthermore, our findings indicate that the EPN in response to emotional processing is modulated by sex.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Rapid brain responses to affective pictures indicate dimensions of trauma‐related psychopathology in adolescents

et al. 2019

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“…Therefore, for our analysis, we arbitrarily split the picture observation period of 2 s into two time windows. Within the early window (0-500 ms), which may contain early emotional images confounded more by perceptual and attentional processes (31,(33)(34)(35)(36)(37), we searched for activity related to the affective picture presentation in contrast to the black screen periods preceding each picture. For emotional activity, we searched in the late window, starting at 500 ms after the visual stimulus onset, because this can be better related to emotional processing after the conceptual knowledge of the presented emotion (represented here in individual ratings of the emotional valence and arousal) is built (32).…”

Section: Significancementioning

confidence: 99%

Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

Sieger

Serranová

Růžička

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Both animal studies and studies using deep brain stimulation in humans have demonstrated the involvement of the subthalamic nucleus (STN) in motivational and emotional processes; however, participation of this nucleus in processing human emotion has not been investigated directly at the single-neuron level. We analyzed the relationship between the neuronal firing from intraoperative microrecordings from the STN during affective picture presentation in patients with Parkinson's disease (PD) and the affective ratings of emotional valence and arousal performed subsequently. We observed that 17% of neurons responded to emotional valence and arousal of visual stimuli according to individual ratings. The activity of some neurons was related to emotional valence, whereas different neurons responded to arousal. In addition, 14% of neurons responded to visual stimuli. Our results suggest the existence of neurons involved in processing or transmission of visual and emotional information in the human STN, and provide evidence of separate processing of the affective dimensions of valence and arousal at the level of single neurons as well.emotion | basal ganglia | subthalamic nucleus | single neuron | arousal A t one time, the subthalamic nucleus (STN), which is an important target for deep brain stimulation (DBS) in the treatment of motor symptoms in Parkinson's disease (PD), was considered an important regulator of motor function (1, 2); however, the occurrence of postoperative neuropsychiatric complications has expanded interest in the nonmotor function of the STN (3, 4). Animal and human studies have already demonstrated the additional functional role of the STN in emotional and motivational processes (5-12). In addition, recent functional MRI studies found STN activation in response to emotional stimuli in healthy subjects (13,14). Therefore, we hypothesized that emotional activity-related neurons should exist in the STN. Participation of the STN in processing emotion has not yet been investigated directly at the single-neuron level in humans. Nonetheless, single-neuron activity related to a priori defined emotional categories (e.g., positive vs. negative) has been detected in a few human brain regions, including the hippocampus, amygdala, and prefrontal and subcallosal cortex (15-18).It has been proposed that emotional behavior is organized along two psychophysiological dimensions: emotional valence, varying from unpleasant to pleasant, and arousal, varying from low to high (19). The individual assessment of these dimensions is closely correlated with somatic and autonomic measures of emotions (20,21). Contrary to a priori categories, they can better reflect emotional characteristics of the stimulus in an individual context, and they take into account interindividual differences based on specific behavioral determinants, such as affective disposition and personality traits (22).In this study, we aimed to detect single-neuron firing pattern changes in the STN that are related to emotional arousal and valence from the in...

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“…The EPN has been interpreted as evidence of processing advantage of emotional stimuli during the initial stages of visual processing, whereas the LPP is thought to reflect the recruitment of selective attention processes related to the motivational signification of the stimuli. Studies using magnetoencephalography (MEG) have also found increased activity in occipitotemporal areas in relation to the arousing value of visual stimuli during the EPN time interval [Burgmer et al, ; D'Hondt et al, ], further supporting that early processing of visual stimuli along the ventral pathway is modulated by their affective value.…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal dynamics of affective picture processing revealed by intracranial high-gamma modulations

et al. 2014

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Our comprehension of the neural mechanisms underlying emotional information processing has largely benefited from noninvasive electrophysiological and functional neuroimaging techniques in recent years. However, the spatiotemporal dynamics of the neural events occurring during emotional processing remain imprecise due to the limited combination of spatial and temporal resolution provided by these techniques. This study examines the modulations of high-frequency activity of intracranial electroencephalography recordings associated with affective picture valence, in epileptic patients awaiting neurosurgery. Recordings were obtained from subdural grids and depth electrodes in eight patients while they viewed a series of unpleasant, pleasant and neutral pictures from the International Affective Picture System. Broadband high-gamma (70-150 Hz) power was computed for separate 100-ms time windows and compared according to ratings of emotional valence. Compared to emotionally neutral or pleasant pictures, unpleasant stimuli were associated with an early and long-lasting (≈200-1,000 ms) bilateral increase in high-gamma activity in visual areas of the occipital and temporal lobes, together with a late and transient (≈500-800 ms) decrease found bilaterally in the lateral prefrontal cortex (PFC). Pleasant pictures were associated with increased gamma activity in the occipital cortex, compared to the emotionally neutral stimuli. Consistent with previous studies, our results provide direct evidence of emotion-related modulations in the visual ventral pathway during picture processing. Results in the lateral PFC also shed light on the neural mechanisms underlying its role in negative emotions processing. This study demonstrates the utility of intracranial high-gamma modulations to study emotional process with a high spatiotemporal precision.

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Early Affective Processing in Patients with Acute Posttraumatic Stress Disorder: Magnetoencephalographic Correlates

Cited by 10 publications

References 72 publications

Rapid brain responses to affective pictures indicate dimensions of trauma‐related psychopathology in adolescents

Rapid brain responses to affective pictures indicate dimensions of trauma‐related psychopathology in adolescents

Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

Spatiotemporal dynamics of affective picture processing revealed by intracranial high-gamma modulations

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