A Rapid Subcortical Amygdala Route for Faces Irrespective of Spatial Frequency and Emotion

McFadyen, Jessica; Mermillod, Martial; Mattingley, Jason B.; Halász, Veronika; Garrido, Marta I.

doi:10.1523/jneurosci.3525-16.2017

Cited by 98 publications

(106 citation statements)

References 78 publications

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“…Convincingly, the results showed that amygdala activity arose for BSF and LSF faces, but not for HSF stimuli, arguing in favour of a subcortical pathway biased towards low spatial frequencies (Vuilleumier et al, 2003). Since this report, a number of other studies have highlighted the importance of LSF in emotional face processing (e.g., Bocanegra & Zeelenberg, 2009;Mermillod, Vuilleumier, Peyrin, Alleysson, & Marendaz, 2009), yet the reliance of the subcortical pathway on LSF remains disputed (e.g., De Cesarei & Codispoti, 2013;Garrido, 2012;Garvert, Friston, Dolan, & Garrido, 2014;McFadyen, Mermillod, Mattingley, Halasz, & Garrido, 2017).…”

Section: Introductionmentioning

confidence: 61%

Affective blindsight relies on low spatial frequencies

et al. 2019

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The human brain can process facial expressions of emotions rapidly and without awareness. Several studies in patients with damage to their primary visual cortices have shown that they may be able to guess the emotional expression on a face despite their cortical blindness. This non-conscious processing, called affective blindsight, may arise through an intact subcortical visual route that leads from the superior colliculus to the pulvinar, and thence to the amygdala. This pathway is thought to process the crude visual information conveyed by the low spatial frequencies of the stimuli.In order to investigate whether this is the case, we studied a patient (TN) with bilateral cortical blindness and affective blindsight. An fMRI paradigm was performed in which fearful and happy expressions were presented using faces that were either unfiltered, or filtered to remove high or low spatial frequencies. Unfiltered fearful faces produced right amygdala activation although the patient was unaware of the presence of the stimuli. More BLINDSIGHT AND SPATIAL FREQUENCIES 2 importantly, the low spatial frequency components of fearful faces continued to produce right amygdala activity while the high spatial frequency components did not. Our findings thus confirm that the visual information present in the low spatial frequencies is sufficient to produce affective blindsight, further suggesting that its existence could rely on the subcortical colliculo-pulvino-amygdalar pathway.

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Section: Introductionmentioning

confidence: 61%

Affective blindsight relies on low spatial frequencies

et al. 2019

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“…For example, prior work has shown that PCA components underlying the LPP are differentially sensitive to intrinsic or extrinsic experimental effects, with extrinsic effects modulating later PCA components in particular (MacNamara et al, 2009). Here, an early, occipital PCA component peaking around 500 ms post-stimulus onset was found to be correlated with BOLD activation in the amygdala, perhaps reflecting the amygdala’s role in the rapid identification and early processing of threatening stimuli (e.g., McFadyen, Mermillod, Mattingley, Halász, & Garrido, 2017). Using mean area amplitudes (which extended until stimulus offset), the LPP was correlated with activation in the insula - a brain region implicated in the conscious awareness and anticipation of threat (Critchley, Mathias, & Dolan, 2002; Phelps et al, 2001).…”

Section: Discussionmentioning

confidence: 81%

Convergence of fMRI and ERP measures of emotional face processing in combat‐exposed U. S. military veterans

et al. 2017

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The late positive potential (LPP) and fMRI blood-oxygen-level dependent (BOLD) activity can provide complementary measures of the processing of affective and social stimuli. Separate lines of research using these measures have often employed the same stimuli, paradigms, and samples; however, there remains relatively little understanding of the way in which individual differences in one of these measures relates to the other, and all prior research has been conducted in psychiatrically healthy samples and using emotional scenes (not faces). Here, 32 combat-exposed U. S. military veterans with varying levels of posttraumatic stress symptomatology viewed affective social stimuli (angry, fearful, and happy faces) and geometric shapes during separate EEG and fMRI BOLD recordings. Temporospatial principal component analysis was used to quantify the face-elicited LPP in a data-driven manner, prior to conducting whole-brain correlations between resulting positivities and fMRI BOLD elicited by faces. Participants with larger positivities to fearful faces (> shapes) showed increased activation in the amygdala; larger positivities to angry and happy faces (> shapes) were associated with increased BOLD activation in the posterior fusiform gyrus and inferior temporal gyrus, respectively. Across all face types, larger positivities were associated with increased activation in the fusiform "face" area. Correlations using mean area amplitude LPPs showed an association with increased activation in the anterior insula for angry faces (> shapes). LPP-BOLD associations were not moderated by PTSD. Findings provide the first evidence of correspondence between face-elicited LPP and BOLD activation across a range of (normal to disordered) psychiatric health.

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“…However, there is some debate on how such rapid perception is accomplished. A fast subcortical thalamus‐amygdala route bypassing the visual cortex is thought to transmit coarse face‐related information (LeDoux, 2009; Morris et al, 1998), but its role in face perception is controversial (Krolak‐Salmon et al, 2004; Pessoa & Adolphs, 2011), including whether it is fear‐specific (Méndez‐Bértolo et al, 2016) or non‐specific to expression (Garvert, Friston, Dolan, & Garrido, 2014; McFadyen et al, 2017). On the other hand, multiple fast cortical pathways forming part of a feedforward and feedback mechanism consistute an equally plausible mechanism for rapid expression perception (Liu & Ioannides, 2010; Pessoa & Adolphs, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…However, there is some debate on how such rapid perception is accomplished. A fast subcortical thalamus-amygdala route bypassing the visual cortex is thought to transmit coarse face-related information (LeDoux, 2009;Morris et al, 1998), but its role in face perception is controversial (Krolak-Salmon et al, 2004;Pessoa & Adolphs, 2011), including whether it is fear-specific (M endez-B ertolo et al, 2016) or non-specific to expression (Garvert, Friston, Dolan, & Garrido, 2014;McFadyen et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal dynamics in human visual cortex rapidly encode the emotional content of faces

Dima

Perry

Messaritaki

et al. 2018

Human Brain Mapping

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Recognizing emotion in faces is important in human interaction and survival, yet existing studies do not paint a consistent picture of the neural representation supporting this task. To address this, we collected magnetoencephalography (MEG) data while participants passively viewed happy, angry and neutral faces. Using time‐resolved decoding of sensor‐level data, we show that responses to angry faces can be discriminated from happy and neutral faces as early as 90 ms after stimulus onset and only 10 ms later than faces can be discriminated from scrambled stimuli, even in the absence of differences in evoked responses. Time‐resolved relevance patterns in source space track expression‐related information from the visual cortex (100 ms) to higher‐level temporal and frontal areas (200–500 ms). Together, our results point to a system optimised for rapid processing of emotional faces and preferentially tuned to threat, consistent with the important evolutionary role that such a system must have played in the development of human social interactions.

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A Rapid Subcortical Amygdala Route for Faces Irrespective of Spatial Frequency and Emotion

Cited by 98 publications

References 78 publications

Affective blindsight relies on low spatial frequencies

Affective blindsight relies on low spatial frequencies

Convergence of fMRI and ERP measures of emotional face processing in combat‐exposed U. S. military veterans

Spatiotemporal dynamics in human visual cortex rapidly encode the emotional content of faces

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