Visual recovery in cortical blindness is limited by high internal noise

Abstract

Damage to the primary visual cortex typically causes cortical blindness (CB) in the hemifield contralateral to the damaged hemisphere. Recent evidence indicates that visual training can partially reverse CB at trained locations. Whereas training induces near-complete recovery of coarse direction and orientation discriminations, deficits in fine motion processing remain. Here, we systematically disentangle components of the perceptual inefficiencies present in CB fields before and after coarse direction discrimination training. In seven human CB subjects, we measured threshold versus noise functions before and after coarse direction discrimination training in the blind field and at corresponding intact field locations. Threshold versus noise functions were analyzed within the framework of the linear amplifier model and the perceptual template model. Linear amplifier model analysis identified internal noise as a key factor differentiating motion processing across the tested areas, with visual training reducing internal noise in the blind field. Differences in internal noise also explained residual perceptual deficits at retrained locations. These findings were confirmed with perceptual template model analysis, which further revealed that the major residual deficits between retrained and intact field locations could be explained by differences in internal additive noise. There were no significant differences in multiplicative noise or the ability to process external noise. Together, these results highlight the critical role of altered internal noise processing in mediating training-induced visual recovery in CB fields, and may explain residual perceptual deficits relative to intact regions of the visual field.

Figures

Figure 1

Structural MRIs of the seven cortically blind participants (CB1–CB7), illustrating the location of their V1 damage and visual field defects. Images are T1-weighed structurals in both horizontal and coronal planes. Left is left and right is right on each MRI picture. Next to each patient's brain scans are composite visual field maps, illustrating visual loss induced by their stroke, averaged across the two eyes. Composites were created by plotting luminance detection values obtained from four 24-2 and 10-2 Humphrey visual field tests into a matrix. If these locations coincided, the values were averaged together. Interpolating between tested data points then filled the empty spaces between values. All values are measured in dB (grayscale legend at far right).

Figure 2

Behavioral paradigms. (A) Coarse, left–right, global direction discrimination task used to train subjects and measure direction range thresholds. (B) Fine direction difference thresholds were collected at different levels of direction range by presenting a random dot stimulus within the blind field, which moved slightly above or below the horizontal meridian. (C) Sample visual field of a subject in the present study. Blue circles indicate locations where performance was mapped in order to select a training location (red circle).

Figure 3

LAM predictions. TvN comparison between two test conditions may present two possible signatures when fit with the LAM: (A) Improved thresholds only at low-noise levels indicate a reduction of equivalent internal noise in the better performing condition relative to the impaired condition. (B) Improved thresholds at all noise levels indicate an improvement in sampling efficiency in the better performing condition relative to the impaired condition.

Figure 4

PTM predictions. TvN comparisons between test conditions may present four possible signatures when fit with the PTM: (A) Lower thresholds at low-noise than high-noise conditions, indicating a reduction of additive internal noise in the better performing conditions compared to the impaired condition, suggestive of stimulus enhancement; (B) Improved performance only in high-noise conditions, suggesting an improved ability to exclude external noise when encoding the stimulus in the better performing condition compared to the impaired condition; (C) Improved performance at all noise conditions, but only at one difficulty level, indicating a reduction of multiplicative internal noise in the better performing condition compared to the impaired condition; (D) Lower thresholds at all noise levels and both difficulty levels, indicating a combined effect of reduced additive internal noise and improved external noise exclusion in the improved condition compared to the impaired condition.

Figure 5

Coarse and fine direction discrimination performance in CB subjects. (A) Pretraining performance for coarse, left–right global direction discrimination in subjects recruited de novo or who had undergone training as part of a previous study (Das et al., 2014). There were no significant differences between these two subject subgroups. (B) Pretraining performance for coarse, left–right global direction discrimination in subjects who received either direction discrimination training only or direction and orientation discrimination training. All subjects were equally impaired prior to the onset of training administered for the present study. (C) Example of training data for CB subjects, showing percent-correct performance on individual training sessions for the global left–right direction discrimination task. All subjects started around or just above chance, but eventually rose to ∼80% correct. (D) Following training, direction range thresholds across all subjects recovered to near-intact field levels. (E) Direction difference thresholds also improved following coarse discrimination training, but they remained significantly higher compared to direction difference thresholds measured at corresponding locations in the intact field of vision (*p = 0.003).

Figure 6

Effect of training on fine direction discrimination performance. (A) Prior to training, fine direction difference thresholds within the blind field were close to ceiling, hovering just below 45°. Following training, thresholds in the blind field improved. (B) This training had no significant effect on subject performance in the intact field of vision. (C) Likewise, repeated testing of visually intact subjects did not alter performance in the absence of training.

Figure 7

LAM and PTM analysis. (A) LAM analysis (fit lines indicate best-fitting model) of blind field pre- and posttraining data indicated a reduction of internal noise with no change in sampling efficiency. However, despite these improvements, thresholds in the intact field of vision remained significantly better than at the posttraining blind field locations, which were computed to have increased internal noise relative to the intact field. (B) TvN data for 82% and 75% correct levels, contrasting direction difference thresholds in the intact field of vision and blind field posttraining. The best-fitting PTM model (fit lines indicate best-fitting model) showed that following training, blind field locations continued to have more additive internal noise compared to the intact visual field. There was no change in multiplicative noise or external noise processing between the posttraining blind field locations and the intact visual field.