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

Abstract

There is significant controversy over the existence and function of a direct subcortical visual pathway to the amygdala. It is thought that this pathway rapidly transmits low spatial frequency information to the amygdala independently of the cortex, and yet the directionality of this function has never been determined. We used magnetoencephalography to measure neural activity while human participants discriminated the gender of neutral and fearful faces filtered for low or high spatial frequencies. We applied dynamic causal modeling to demonstrate that the most likely underlying neural network consisted of a pulvinar-amygdala connection that was uninfluenced by spatial frequency or emotion, and a cortical-amygdala connection that conveyed high spatial frequencies. Crucially, data-driven neural simulations revealed a clear temporal advantage of the subcortical connection over the cortical connection in influencing amygdala activity. Thus, our findings support the existence of a rapid subcortical pathway that is nonselective in terms of the spatial frequency or emotional content of faces. We propose that that the "coarseness" of the subcortical route may be better reframed as "generalized."

Affective blindsight relies on low spatial frequencies

“…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).…”

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

“…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).…”

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

“…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).…”

“…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).…”