Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG

Abstract

Facial threat conveys important information about imminent environmental danger. The rapid detection of this information is critical for survival and social interaction. However, due to technical and methodological difficulties, the spatiotemporal profile for facial threat processing is unknown. By utilizing Magnetoencephalography (MEG), a brain-imaging technique with superb temporal resolution and fairly good spatial resolution, Synthetic Aperture Magnetometry (SAM), a recently developed source analysis technique, and a sliding window analysis, we identified the spatiotemporal development of facial threat processing in the gamma frequency band. We also tested the dual-route hypothesis by LeDoux who proposed, based on animal research, that there are two routes to the amygdala: a quick subcortical routeand a slower and cortical route. Direct evidence with humans supporting this model has been lacking. Moreover, it has been unclear whether the subcortical route responds specifically to fearful expressions or to threatening expressions in general. We found early event-related synchronizations (ERS) in response to fearful faces in the hypothalamus/thalamus area (10-20 ms) and then the amygdala (20-30 ms). This was even earlier than the ERS response seen to fearful faces in visual cortex (40-50 ms). These data support LeDoux's suggestion of a quick, subcortical thamaloamygdala route. Moreover, this route was specific for fear expressions; the ERS response in the amygdala to angry expressions had a late onset (150-160 ms). The ERS onset in prefrontal cortex followed that seen within the amygdala (around 160-210 ms). This is consistent with its role in higher-level emotional/cognitive processing.

Cortico-subcortical visual, somatosensory, and motor activations for perceiving dynamic whole-body emotional expressions with and without striate cortex (V1)

“…Standard fMRI methods sample and average brain signal at relatively long time scales and do not enable a fine-grained distinction of the possibly different temporal profiles at which neural activity in various brain areas may occur. For example, investigation of conscious perception of fearful expressions by using the high temporal resolution of magnetoencephalography detected early activity in the Pulv (10-20 ms) and Amg (20-30 ms) (30), which is frequently reported only during nonconscious emotion perception with standard fMRI methods (22). This activity was then followed by cortical responses in the visual cortex (40-50 ms) and in prefrontal areas (160-210 ms) typically observed in conscious perception (30).…”

“…For example, investigation of conscious perception of fearful expressions by using the high temporal resolution of magnetoencephalography detected early activity in the Pulv (10-20 ms) and Amg (20-30 ms) (30), which is frequently reported only during nonconscious emotion perception with standard fMRI methods (22). This activity was then followed by cortical responses in the visual cortex (40-50 ms) and in prefrontal areas (160-210 ms) typically observed in conscious perception (30). Moreover, functional connectivity data suggest that nonconscious emotion perception is supported by positive connectivity and coactivation in the subcortical pathway to the Amg, whereas conscious emotion perception is supported by negative cortico-subcortical connectivity along this pathway (47).…”

“…For example, direct stimulation of the SC in rats induces freezing and flight reactions (29). In healthy human observers, one study combining magnetoencephalography with functional magnetic resonance imaging (fMRI) found that eventrelated synchronization in response to fearful faces occurred in the Pulv after only 10-20 ms after stimulus onset (30). This activity could not be attributed to, and could not be modulated directly by, Amg activity because synchronization in the Amg took place later in time (20-30 ms after stimulus onset), and because the connections between Pulv and Amg are unidirectional (31).…”

From affective blindsight to emotional consciousness

“…The excellent spatial resolution of fMRI, on the order of millimeters, is counterbalanced by its limited temporal resolution, as events occurring during a temporal window of a few seconds are averaged together, thus preventing a fine-grained analysis of the temporal dynamics occurring among the implicated areas. This is a serious limitation when studying emotions, as nonconscious emotional processing takes place within milliseconds after stimulus onset in subcortical brain areas, including the amygdala and structures related to reflex-like motor reactions, and is followed shortly after by later responses engaged in more deliberate responses and in conscious vision (Borgomaneri, Gazzola, & Avenanti 2014;Borgomaneri, Vitale, Gazzola, & Avenanti, 2015;Garrido, Barnes, Sahani, & Dolan, 2012;Garvert, Friston, Dolan, & Garrido, 2014;Luo, Holroyd, Jones, Hendler, & Blair, 2007;Maior, Hori, Tomaz, Ono, & Nishijo, 2010;Nguyen et al, 2014). Because both early nonconscious and later conscious responses take place within the time window of a single volume acquisition in fMRI studies, the different functional values of neural activity in the same structure may be integrated or overridden (Brosch & Wieser, 2011;Costa et al, 2014;Luo et al, 2010).…”

“…One study combining MEG and MRI methods reported early event-related synchronization in the pulvinar at about 10-20 ms after presentation of fearful faces, followed by event-related synchronization in the amygdala at 20-30 ms after onset, whereas synchronization in the striate cortex occurred 40-50 ms after stimulus onset (Luo et al, 2007). Another study revealed dissociation between rapid amygdala responses to automatic fearful face processing and later responses that interacted with voluntary attention.…”