Awareness-related activity in prefrontal and parietal cortices in blindsight reflects more than superior visual performance Navindra Persaud, Mather Davidson, Brian Maniscalco, Dean Mobbs, Richard E. Passingham, Allan Cowey, and Hakwan Lau

Blindsight Upon hearing a tone, fixate on the target. Blindsight patients can fixate on the light despite having no conscious awareness. In the control condition (no light), eye movements are random. Blind field can detect: location size motion direction line orientation simple shapes

Unconscious Vision vs. Degraded Conscious Vision Two types of blindsight 1. Without any conscious awareness 2. With some conscious awareness. New scale to assess blindsight because patients may underestimate conscious experience. Forced choice: circle, square, triangle Concluded that visual discrimination in blindsight is based on degraded conscious vision (Overgaard et al., 2008). The health field vs. the blind field in patient G.R.

Unconscious Vision vs. Degraded Conscious Vision Round 2 Persaud and Cowey, 2008 Exclusion Task: Conscious and unconscious work in opposition. If stimuli appears in upper quadrant, correct response is lower quadrant. Inclusion Task: Conscious and unconscious work together. If stimuli appears in upper quadrant, correct response is upper quadrant. Normal Field: Opposite location was reported in exclusion task and actual location was reported in the inclusion task. Blind Field: Actual location was reported in exclusion and inclusion. Blindsight is NOT due to degraded conscious vision.

PFC and Parietal Lobe in Awareness Prior work with G.Y. has shown that his LPFC is activated for moving stimuli in his normal visual field. The LPFC was also activated for fast moving stimuli in his blind field that he was aware of but not for slow moving stimuli in his blind field that he was not aware of (Sahraie et al. 1997). G.Y. has increased activity in the parietal lobe for stimuli he was aware of even when task performance doesn’t differ for stimuli that he is unaware of (Shurger et al. 2006,2008).

Metacognition Imaging studies have shown that when healthy participants have higher activity in the PFC and parietal lobe when they report visual awareness (Reese et al., 2002). Although, an alternative interpretation is that the PFC is associated with metacognition (Fleming et al., 2010).

It is possible to match performance in the blind and normal field. Because G.Y.’s performance depends on the strength (luminance contrast) of a stimulus, it is possible to manipulate viewing conditions so performance is matched for the stimulus in the normal field (weak stimulus) and blind field (strong stimulus). This allowed them to ask the question of whether or not there will still be higher activity in the PFC and parietal lobe in the normal hemisphere compared to the blind hemisphere even when performance is matched.

Methods Participant: G.Y. is a 52 year old man. He suffered a unilateral lesion to almost his entire left striate cortex when he was 8 years old. His injury left him with right homonymous hemianopia with macular sparing extending 3.5 degrees into his blind field. Image is left homonymous hemianopia with macular sparing

Task Report whether the vertical grating was shown in the upper or lower quadrant. Gratings appeared for 500 ms. 2 meta-response tasks: Coin flip/response: 50/50 chance or use his response for a chance to win 50 pence. Guess/seen: report whether answer was a guess or based on some visual awareness. He received 50 pence for any correct answer. Coin flip/response: 480 trials to blind field, 240 trials to normal field. Guess/seen: 192 trials to blind field, 96 trials to normal field. Before the main experiment, contrast in the blind field was manipulated to match accuracy in the normal field.

fMRI data analysis T-2 weighted images BOLD contrast as an index of local increases in synaptic activity 3 X 3 mm voxels

Behavioral Results Norma field: Trials reported seen were 95% correct and trials reported guess were 64% correct. Blind field: Trials reported seen were 83% correct and trials reported guess were 74% correct. These values are not significantly different (p = .22). Response times were significantly shorter for the blind field than for the normal field (p < .0001).

Behavioral Results A: Percent correct is matched for each hemifield. Blind field: 79% correct Normal field: 76% correct B: More trials were reported seen in the normal hemifield (p < .0000001). Blind field: 3% seen Normal field: 43% seen C: Equally willing to wager on his response over a coin flip for both hemifields. Blind field: 69% trails Normal field: 66% trials G.Y.’s confidence in his blind hemifield may be due to his experience with blindsight

fMRI Results Significantly higher cortical activity for stimuli in normal field compared to blind field despite the fact that performance and confidence were matched for each field. Activity in the PFC and parietal lobe is NOT due to task performance.

fMRI Results Significantly higher activity in normal field: Right intra-parietal sulcus (p < .000001) Right superior temporal sulcus (p < .005) Right ventral PFC (p < .00001) Right frontal polar cortex

fMRI Results Significantly higher activity in blind field: Left Amygdala (p < .029)

fMRI Results for Metacognition Prior work (Kornell et al., 2007) has used the correlation between confidence and accuracy as an index of metacognitive capacity. The ability to distinguish between one’s own correct and incorrect responses The correlation coefficient r was significantly higher in the normal field than in the blind field (p < .001).

Discussion Does activation is the PFC and parietal lobe actually reflect awareness? Alternative: It could reflect signal strength or superior task performance which leads to conscious visual phenomenology. No, activity was found in these regions even when weaker stimuli were used and when controlling for task performance. G.Y. was equally confident for his blind and normal hemifield.

Discussion Response times were shorter in the blind field than the normal field. Overall performance may be higher in the blind field. Having a real visual percept may make performance slower. Peaks in the normal hemisphere: Intra-parietal sulcus, superior temporal sulcus, ventrolateral PFC VLPFC receives projections from the intra-parietal sulcus and the superior temporal sulcus.

Activity in Blind Field Significantly higher activity in the left amygdala for stimuli presented in the blind field (p < .029). Since willingness to wager (thus confidence) was matched for each hemifield, it is unlikely this activity is due to anxiety.

Correct Vs. Incorrect Responses in Blind Field Higher activity in the left parahippocampal gyrus when judgments in blind field were correct (p < .0002). G.Y. was more confident in his correct responses. This activity may be due some aspect of his subjective (non-visual) awareness.

Discussion Previously, the authors had used metacontrast masking to make ‘relative blindsight’ in healthy individuals. Awareness was associated with activity in the anterior PFC (but not parietal lobe). This activity was just posterior to the activity found in the polar PFC in the current study.

Alternative Explanation PFC and parietal lobe make a ‘global workplace’ and when there’s conscious perception then there’s ‘global broadcast’ (Dehaene et al., 2003). This should lead to higher performance. The current study found increased activity in the PFC and parietal lobe in his normal field with out increased performance. The increase was associated with awareness. Alternative: PFC and parietal lobe activity reflects preparatory flexibility. The present study cannot rule out this possibility.

Alternative Explanation PFC and parietal lobe activity is related to metacognition and not necessarily awareness. G.Y. was better at monitoring his performance in his normal field than his blind field. Prior work has shown TMS to the PFC did not decrease performance, only the correlation between confidence and accuracy (decreased metacognition) (Rounis et al., 2010). G.Y. had high activity in the polar PFC in his normal hemisphere. This area has been found to be associated with metacognition (Fleming et al., 2010). The possibility of metacognition cannot be ruled out.

Limitations Because blindsight is rare, the findings may not generalize. G.Y.’s lesion may have led to cortical reorganization. G.Y. has an abnormal connection from his contralesional LGN to his ipsilesional V5/MT.