Magnocellular and parvocellular pathway contributions to facial threat cue processing

Abstract

Human faces evolved to signal emotions, with their meaning contextualized by eye gaze. For instance, a fearful expression paired with averted gaze clearly signals both presence of threat and its probable location. Conversely, direct gaze paired with facial fear leaves the source of the fear-evoking threat ambiguous. Given that visual perception occurs in parallel streams with different processing emphases, our goal was to test a recently developed hypothesis that clear and ambiguous threat cues would differentially engage the magnocellular (M) and parvocellular (P) pathways, respectively. We employed two-tone face images to characterize the neurodynamics evoked by stimuli that were biased toward M or P pathways. Human observers (N = 57) had to identify the expression of fearful or neutral faces with direct or averted gaze while their magnetoencephalogram was recorded. Phase locking between the amygdaloid complex, orbitofrontal cortex (OFC) and fusiform gyrus increased early (0–300 ms) for M-biased clear threat cues (averted-gaze fear) in the -band (13–30 Hz) while P-biased ambiguous threat cues (direct-gaze fear) evoked increased (4–8 Hz) phase locking in connections with OFC of the right hemisphere. We show that M and P pathways are relatively more sensitive toward clear and ambiguous threat processing, respectively, and characterize the neurodynamics underlying emotional face processing in the M and P pathways.

Schizophrenia and visual perception disturbances

“…El sistema visual consiste en varias vías, que se inician en la retina y se proyectan, a través del (16) núcleo geniculado lateral del tálamo, a diferentes capas de la corteza visual primaria . La tabla 1 resume sus características más resaltantes (16)(17)(18)(19)(20)(21)(22) Tabla 1. Características resaltantes de las vías parvocelular y magnocelular Estas dos vías se proyectan principalmente a las regiones parieto-occipital y témporo-occipital, existiendo una importante interacción entre estas regiones.…”

Fast saccadic and manual responses to faces presented to the koniocellular visual pathway

“…It can resolve low and middle spatial frequencies and high temporal frequencies. We have found the M pathway to be more engaged by clear threat cues conveyed by congruent facial expression and eye gaze (Cushing et al, 2019;Im et al, 2017;Im et al, 2018) and clear threat in visual scenes (Kveraga, 2014). The P pathway, formed from the midget retinal ganglion cells that combine the inputs of L and M cones in color-opponent fashion (i.e., L-M), is sensitive to color in the green-to-red range, and can resolve higher spatial and low temporal frequencies.…”

“…To test these hypotheses, we designed a task in which human observers viewed neutral or angry faces that were male or female and varied in masculinity across the stimulus set. The face stimuli were individually calibrated (see Methods) for each observer so as to bias processing towards the M, P, or K pathways, using procedures previously used in (Anstis & Cavanagh, 1983;Cushing et al, 2019;Im et al, 2017;Im et al, 2018;Kveraga, 2014;Kveraga et al, 2007;Thomas et al 2012) and were briefly presented to the left or right of the central fixation cross. We instructed observers to fixate in the center at the start of a trial, and then to categorize the face as angry or neutral, reporting their decision with a key press as quickly and accurately as possible.…”

“…Recently, we have demonstrated that two of the major visual pathways, the M and P pathways, are attuned to somewhat different aspects of face perception ( Adams et al., 2019 ; Cushing et al., 2019 ; Im et al., 2018 ; Im et al., 2017 ). The M pathway, which is formed from the large retinal ganglion cells that combine the inputs of long ( L ) and medium ( M ) wavelength cones (i.e., L + M ) and some rod contributions, is largely insensitive to color but has high gain and sensitivity to small luminance differences ( Merigan & Maunsell, 1990 ).…”

“…Given its putative role in threat detection ( Isbell, 2006 ; Van Le et al., 2013 ), we predicted that stimuli presented to the K pathway would evoke faster saccadic and manual responses, compared to stimuli presented to the M or P pathways. The threat cues present in faces can be dynamic and fleeting, such as anger or fear expressions that respectively signal danger to the observer and the expresser, with the threat locus indicated by overt attention cues such as eye gaze direction ( Adams et al., 2003 ; Adams & Kleck, 2003 ; Adams & Kleck, 2005 ; Adams et al., 2012 ; Cushing et al., 2018 ; Cushing et al., 2019 ; Im et al., 2017 ; Im et al., 2018 ). Facial threat cues also can be more stable or static, inherent in the facial configuration and texture associated with higher masculinity, such as a low, pronounced brow ridge, small eyes, a prominent jaw, facial hair, and a high facial width-to-height ratio ( Zebrowitz & Collins, 1997 ; Zebrowitz & Montepare, 2008 ).…”