Visual cortical activity reflects faster accumulation of information from cortically blind fields

Abstract

Brain responses (from functional magnetic resonance imaging) and components of information processing were investigated in nine cortically blind observers performing a global direction discrimination task. Three of these subjects had responses in perilesional cortex in response to blind field stimulation, whereas the others did not. We used the EZ-diffusion model of decision making to understand how cortically blind subjects make a perceptual decision on stimuli presented within their blind field. We found that these subjects had slower accumulation of information in their blind fields as compared with their good fields and to intact controls. Within cortically blind subjects, activity in perilesional tissue, V3A and hMT+ was associated with a faster accumulation of information for deciding direction of motion of stimuli presented in the blind field. This result suggests that the rate of information accumulation is a critical factor in the degree of impairment in cortical blindness and varies greatly among affected individuals. Retraining paradigms that seek to restore visual functions might benefit from focusing on increasing the rate of information accumulation.

Figure 1

T₁-weighted structural MRIs of the nine V1-damaged patients (CB1–9) recruited for this study, illustrating the location of their V1 damage in both horizontal and coronal planes. Next to each patient’s brain scan are representations of his/her Humphrey visual field perimetry (24-2 test) averaged across the two eyes. The grey scale indicates average detection sensitivity in dB. Light grey circles represent the visual field locations and sizes of random dot stimuli the subjects were asked to discriminate. MRIs are oriented so that the left side of the image corresponds to the left side of the brain.

Figure 2

Schematic illustration of the global direction discrimination task performed during functional MRI. On each trial, moving dots were presented in a 5° window at one of four locations. Dots could move in the same direction, or randomly within a specified range (usually near 320°) of directions centred on a single direction (right or left), with the range near the threshold for discriminating direction of motion for each participant, as measured psychophysically before scanning.

Figure 3

Schematic illustration of the diffusion model decision process. Information begins to accumulate from a starting point at 0, and drifts towards a decision boundary with some degree of stochastic fluctuation. The decision time is determined by how quickly information accumulates (drift rate) and how much information must accumulate before the observer initiates a response (boundary separation). RT = reaction time.

Figure 4

Summary of behavioural measures. Error bars represent 95% confidence intervals, using pooled error estimates from a multivariate repeated measures ANOVA of the data. See text for statistical results. NDT = Non-decision time.

Figure 5

Results of the Right–Left (R–L) and Left–Right (L–R) t-contrasts in a representative set of participants (two controls and two subjects with cortical blindness). The R–L contrast is colour-coded in blue-white, whereas the L–R contrast is coded orange-yellow. Numbered arrows indicate common anatomical locations of detectable BOLD clusters around the calcarine sulcus (putative V1/V2), the inferior occipital lobe (putative V3v/V4), V3A and the occipital/temporal/parietal junction (putative hMT+). (A) Subject C3 is a control participant stimulated in the upper visual field, showing activation of the lower bank of the calcarine fissure (putative V1/V2) and a relatively symmetric response to left and right stimulation. (B) Subject C9 is also a control participant stimulated in the lower visual field to match Patient CB9, showing activation of the upper bank of the calcarine fissure (putative V1/V2), as well as putative V3A and MT+. The response of the left hemisphere to right visual field stimulation was present but much smaller. (C) Patient CB4: example of a hemianope with activation of perilesional cortex. (D) Patient CB8: example of a hemianope without a detectable response in perilesional cortex. The intact brain hemisphere responds normally, with significant clusters in the lower bank of the calcarine (expected given that stimulus presentation was in the upper hemifield), the ventral occipital cortex and putative hMT+.

Figure 6

Summary of the relationship between activation of perilesional cortex, putative hMT+ and putative V3A with accuracy and drift rate. (A) Comparison of accuracy in response to blind field stimulation between subjects with cortical blindness with and without detectable BOLD responses in perilesional cortex. (B) Comparison of accuracy in response to blind field stimulation between subjects with cortical blindness with and without detectable BOLD responses in putative hMT+. (C) Comparison of drift rate estimated with the EZ-diffusion model in response to blind field stimulation between subjects with cortical blindness with and without detectable BOLD responses in perilesional cortex. (D) Comparison of drift rate between subjects with cortical blindness with and without detectable BOLD responses in putative hMT+. Corresponding t-test results are given in detail in the text. Error bars represent 95% confidence intervals.