Lack of awareness despite complex visual processing: Evidence from event-related potentials in a case of selective metamorphopsia

Abstract

Visual awareness is thought to result from integration of low- and high-level processing; instances of integration failure provide a crucial window into the cognitive and neural bases of awareness. We present neurophysiological evidence of complex cognitive processing in the absence of awareness, raising questions about the conditions necessary for visual awareness. We describe an individual with a neurodegenerative disease who exhibits impaired visual awareness for the digits 2 to 9, and stimuli presented in close proximity to these digits, due to perceptual distortion. We identified robust event-related potential responses indicating 1) face detection with the N170 component and 2) task-dependent target-word detection with the P3b component, despite no awareness of the presence of faces or target words. These data force us to reconsider the relationship between neural processing and visual awareness; even stimuli processed by a workspace-like cognitive system can remain inaccessible to awareness. We discuss how this finding challenges and constrains theories of visual awareness.

Keywords: awareness; event-related potentials; metamorphopsia; single case study; visual perception.

Fig. 1.

Coronal slice of R.F.S.’s brain. MRI scan, August 2011, presented in neurological convention (left side of image is right hemisphere). Slice taken at y = −49 Talairach. Radiologists noted abnormal atrophy in the parietal lobes.

Fig. 2.

Category-specific metamorphopsia: R.F.S. was unable to perceive, describe, or copy the form of Arabic digits 2 to 9. This figure depicts a direct copying task with the number 8: Stimulus (Left) and R.F.S.’s copy (Right). R.F.S. was given various pens and markers to choose from to complete the task. He began by drawing the black lines, and then added the orange background. See Movie S1.

Fig. 3.

Impaired digits affect embedded stimuli. R.F.S. was unable to name the object embedded in this 6, but was accurate for the G. Across 60 trials, R.F.S. was 0% correct when objects were embedded in digits 2 to 9 and 100% correct when embedded in a letter or digit 0 or 1.

Fig. 4.

No implicit awareness of identity of embedded stimuli. R.F.S.’s task was to make a decision about the figure presented inside the character, as in these examples. Row 1: “square or diamond?”, Row 2: “up or down arrow?”, Row 3: ”animal or thing word?” His performance was 49% (at chance) when the figures were inside an 8, and 99% when the figures were inside an H.

Fig. 5.

Neurophysiological evidence of face detection despite lack of awareness: N170 component. We found robust differences of the amplitude of the N170 component when faces were compared to nonfaces, embedded in both letters and digits. Asterisks reflect significance of a permutation test comparing the two conditions (**P < .01, ***P < .005). (A) Sample stimuli and averaged response at P9 and P10 electrodes evoked by faces (red) vs. scrambled faces (blue) embedded in the letter H. (B) Same as A, embedded in the digit 8. (C) Difference waves at P9 and P10 electrodes evoked for faces minus scrambled faces embedded in a digit (green) vs. a letter (pink). Gray highlighting indicates time window of interest (170 to 200 ms). (D) Scalp topography indexing main effect of face presence/absence in the time window of interest.

Fig. 6.

Neurophysiological evidence of task-dependent target detection despite lack of awareness: P3b component. We found robust P3b differences on the P3b component when target words were compared to nontargets, embedded in both letters and digits. Asterisks reflect significance of a permutation test comparing the two conditions (****P < .001). (A) Sample stimuli and response at Cz evoked by targets (red) vs. nontargets (blue) embedded in a letter. (B) Same as A, embedded in a digit. (C) Difference waves at Cz for targets – nontargets embedded in a digit (green) vs. a letter (magenta). Gray highlighting indicates time window of interest (550 to 600 ms). (D) Scalp topography indexing main effect of target presence/absence in the time window of interest.