Neural and psychophysiological correlates of basic and social emotions recognition

Affective blindsight refers to the uncanny ability of patients with cortical blindness following destruction of the primary visual cortex (V1) to discriminate reliably the emotional content of stimuli they cannot consciously perceive because projected in the blind portion of their visual field. Therefore, such clinical condition offers a valuable opportunity to investigate and compare emotion recognition with and without awareness and reveal the psychophysiological and neural properties characteristic of each mode of perception. Here we present several novel evidence related to these issues. First, emotional expressions projected to the blind field elicit spontaneous facial reactions and psychophysiological changes, as indexed by facial EMG and pupil dilation respectively, that are faster and more pronounced than the reactions triggered when the very same stimuli are displayed to the patients’ intact visual field. Noteworthy, not all types of expressions can be discriminated without awareness, but only biologically primitive expressions (e.g., basic emotions like fear or anger). Conversely, facial expressions of so-called social expressions (e.g., guilt or arrogance) do not trigger differential psychophysiological responses and cannot be discriminated without awareness. This pleads in favor of an evolutionary perspective, which argues that only biologically hardwired emotional signals can access phylogenetically ancient subcortical neural structures, such as the amygdala and superior colliculus, that are pivotal for emotion perception without awareness. As this neural network for non-conscious emotion perception seems to draw on the magnocellular visual system, which is tuned to low spatial frequencies, we examined in a combined fMRI/behavioral study the causal role of these factor. We presented broadband, low and high spatial frequency filtered fearful and neutral facial expressions to patients with affective blindsight, who were asked to guess the emotional content of the stimuli. Above chance recognition was possible for broadband and low frequency faces and was associated with activity in the superior colliculus, pulvinar and amygdala. Conversely, correct discrimination dropped to chance level for high frequency stimuli and activity in such subcortical structures was suppressed. Lastly, in vivo tractography (DTI) shows that these subcortical structures have direct anatomical connections in the intact human and non-human brain and that such connections are strengthened in patients with affective blindsight.