The superior colliculus is sensitive to gestalt-like stimulus configuration in hemispherectomy patients

Abstract

Patients with cortical blindness following a lesion to the primary visual cortex (V1) may retain nonconscious visual abilities (blindsight). One intriguing, though largely unexplored question, is whether nonconscious vision in the blind hemifield of hemianopic patients can be sensitive to higher-order perceptual organization, and which V1-independent structure underlies such effect. To answer this question, we tested two rare hemianopic patients who had undergone hemispherectomy, and in whom the only post-chiasmatic visual structure left intact in the same side of the otherwise damaged hemisphere was the superior colliculus (SC). By using a variant of the redundant target effect (RTE), we presented single dots, patterns composed by the same dots organized in quadruple gestalt-like configurations, or patterns of four dots arranged in random configurations, either singly to the intact visual hemifield or bilaterally to both hemifields. As reported in a number of prior studies on blindsight patients, we found that bilateral stimulation yielded faster reaction times (RTs) than single stimulation of the intact field for all conditions (i.e., there was an implicit RTE). In addition to this effect, both patients showed a further speeding up of RTs when the gestalt-like, but not the random shape, quadruple patterns were projected to their blind hemifield during bilateral stimulation. Because other retino-recipient subcortical and cortical structures in the damaged hemisphere are absent, the SC on the lesioned side seems solely responsible for such an effect. The present results provide initial support to the notion that nonconscious vision might be sensitive to perceptual organization and stimulus configuration through the pivotal contribution of the SC, which can enhance the processing of gestalt-like or structured stimuli over meaningless or randomly assembled ones and translate them into facilitatory motor outputs.

Amygdala Response to Emotional Stimuli without Awareness: Facts and Interpretations

“…Unseen facial and bodily expressions have yielded similar findings when presented in the blind fields of patients with affective blindsight. This indicates that a functional subcortical route to the Amg is invovled in emotion perception during sensory unawareness (Morris et al, 2001; de Gelder et al, 2005, 2011; Pegna et al, 2005; Tamietto and de Gelder, 2010; Van den Stock et al, 2011a,b, 2013, 2015a; Georgy et al, 2016). The involvement of the superior colliculus and pulvinar is in keeping with their connectional pattern and physiological properties.…”

A Prototypical Template for Rapid Face Detection Is Embedded in the Monkey Superior Colliculus

“…A neurophysiological study reported that rat SC neurons responded similarly to normal and contrast-reversed circles, suggesting that the SC might detect edges of forms (Girman and Lund, 2007), which is important for object detection and form processing (Kubilius et al, 2014). Furthermore, a neuropsychological study using a human blindsight patient due to removal of the cerebral cortex, pulvinar, and lateral geniculate body but not the SC in the affected hemisphere reported that the SC represented configuration of multiple stimuli and responded differentially to gestalt-like complex assemblies of stimuli (Georgy et al, 2016). Consistent with this finding, configural processing of face features is required for face detection in the initial stage of face information processing (see ''Introduction'' section).…”

The primitive retino-tecto-reticular pathway is functional in hemidecorticate patients

“…We studied two rare hemispherectomy patients (see Supplemental Information for details): DR, who lacked the entire right hemisphere including cortex, pulvinar and LGN, with no possibility that a structure on the operated side could support visual processing (Figures 1A and S1); and SE, who had an intact frontal lobe but with all visual areas on one side surgically removed. Both patients had primitive blindsight but no visual awareness ( Figure S1) [3][4][5]. Each patient was asked to generate a horizontal anti-saccade directed towards their blind hemifi eld, to the mirror location of a visual cue fl ashed in their seeing hemifi eld ( Figures 1A and S1).…”