Abstract
It is widely thought that emotional facial expressions receive privileged neural status compared to their non-affective counterparts. This prioritization, however, comes at a cost, as the neural capacity of the human brain is finite; the prioritization of any one object comes at the expense of other concurrent objects in the visual array competing for awareness (Desimone & Duncan, 1995). Despite this reality, little work has examined the functional benefit derived from the perceptual prioritization of affective information. Why do we preferentially attend to emotional faces? According to evolutionary accounts, emotions originated as adaptations towards action, helping to prepare the organism for locomotion (Darwin, 1872; Frijda, 1986). To directly examine this relationship between emotion and action, we reasoned that the prioritization of affective events may occur via two parallel pathways originating from the retina - a parvocellular (P) pathway projecting to ventral stream structures responsible for object recognition, or a faster and phylogenetically older magnocellular (M) pathway projecting to dorsal stream structures responsible for localization and action. Here we tested whether the fast propagation along the dorsal-action pathway drives an accelerated conduction of fear-based content. We took advantage of the fact that retinal exposure to red diffuse light suppresses M cell neural activity. Using a visual prior entry procedure, accelerated stimulus perception was assessed while either suppressing the M pathway with red diffuse light, or leaving it unaffected with green diffuse light. We show that that the encoding of a fearful face is accelerated, but not when M-channel activity is suppressed. Additional control experiments confirmed that this affective prioritization is driven by coarse low spatial frequency information, and that red diffuse uniquely affects dorsal competition but not top-down ventral competition. Together, our results reveal a dissociation that implicates a privileged neural link between emotion and action that begins at the retina.
This work was supported by a Natural Science and Engineering Research Council of Canada grant to J.P. and a Canada graduate scholarship from the Natural Sciences and Engineering Research Council of Canada to G.L.W.