Beyond blindsight: properties of visual relearning in cortically blind fields

Abstract

Damage to the primary visual cortex (V1) or its immediate afferents results in a dense scotoma, termed cortical blindness (CB). CB subjects have residual visual abilities, or blindsight, which allow them to detect and sometimes discriminate stimuli with high temporal and low spatial frequency content. Recent work showed that with training, discriminations in the blind field can become more reliable, and even reach consciousness. However, the narrow spatiotemporal bandwidth of blindsight limits its functional usefulness in everyday vision. Here, we asked whether visual training can induce recovery outside the spatiotemporal bandwidth of blindsight. Specifically, could human CB subjects learn to discriminate static, nonflickering stimuli? Can such learning transfer to untrained stimuli and tasks, and does double training with moving and static stimuli provide additional advantages relative to static training alone? We found CB subjects capable of relearning static orientation discriminations following single as well as double training. However, double training with complex, moving stimuli in a separate location was necessary to recover complex motion thresholds at locations trained with static stimuli. Subjects trained on static stimuli alone could only discriminate simple motion. Finally, both groups had approximately equivalent, incomplete recovery of fine orientation and direction discrimination thresholds, as well as contrast sensitivity. These results support two conclusions: (1) from a practical perspective, complex moving stimuli and double training may be superior training tools for inducing visual recovery in CB, and (2) the cortically blind visual system can relearn to perform a wider range of visual discriminations than predicted by blindsight alone.

Keywords: contrast sensitivity; direction discrimination; hemianopia; orientation discrimination; perceptual learning.

Copyright © 2014 the authors 0270-6474/14/3311652-13$15.00/0.

Figures

Figure 1.

Structural MRIs of the nine cortically blind subjects (CB1–CB9) that participated in this study, illustrating the location of their V1 damage. For all but CB3, the images are T1-weighed structurals in both horizontal and coronal planes. For CB3, both images are in horizontal plane, as his coronal scans were not of sufficient quality to resolve the lesion. Left is left and right is right on each MRI picture. Next to each subject's brain scans are representations of their Humphrey 24-2 visual field perimetry, averaged across the two eyes. The gray scale indicates average luminance detection sensitivity in decibels across the central 24 or so degrees of visual angle in each person's visual field.

Figure 2.

Behavioral paradigms and performance on trained tasks. A, Group 1 subjects were trained on a static vertical–horizontal orientation discrimination task with nonflickering [temporal frequency (TF) of 0 Hz], low spatial frequency (SF) Gabors. The size of the stimuli and training locations used in subject CB1 are indicated by circles on the subject's Humphrey visual field composite. B, Group 2 subjects were trained with two different tasks, at two locations in their blind field. One location was trained only on a global left–right direction discrimination task with random dot stimuli in which the range of dot directions was progressively increased during each training session. A second blind-field location was trained on only the same orientation discrimination task as Group 1 subjects (as described in A). The size of the stimuli and training locations used in subject CB4 are indicated by circles on the subject's Humphrey visual-field composite. C, Trial sequence for the static orientation discrimination task. Subjects were required to precisely fixate a centrally placed target on a computer monitor in front of them for 1000 ms. A Gabor patch then appeared at a selected location for 500 ms. Subjects were required to maintain fixation on the central target during stimulus presentation. After 500 ms, the stimulus and fixation target disappeared and subjects were required to press to the right arrow key if they perceived a horizontal Gabor, or the left arrow key if they perceived a vertical Gabor. This was immediately followed by auditory response feedback. D, Trial sequence for the global direction discrimination task. Methods were identical to static orientation task, except a moving random dot stimulus was presented at a selected location. Subjects were required to press to the right arrow key if they perceived motion to the right, or the left arrow key if they perceived motion to the left. This was immediately followed by auditory response feedback. E, Plot of mean percentage-correct performance ± SEM for subjects in Group 1 when they were asked to perform Task 7 in their intact hemifield of vision (white bar, Good field), the chosen blind-field locations before the onset of training (black bar, Pretrain bad) and the same blind-field locations after orientation training (dark gray bar, Ori train only). F, Plots of mean percentage-correct performance ± SEM in Group 2 subjects performing global direction discrimination or static orientation discrimination tasks in their intact hemifield of vision (white bars, Good field), the chosen blind-field locations before the onset of training (black bars, Pretrain bad) and the same blind-field locations after either direction training (light gray bar, DR train) or orientation training (dark gray bar, Ori train). Note that percentage-correct performance for both tasks was collected during testing with a staircase procedure, so that maximal performance averaged ∼82% correct.

Figure 3.

Impact of training in Group 1 (single-trained) subjects. A, Percentage-correct performance across consecutive training sessions at two blind-field locations trained on orientation discrimination in CB1 and CB2. For CB1, these two locations are indicated by circles on the Humphrey field composite in Figure 2A. Both subjects showed improvement as a function of the number of training sessions, which was similar at their two trained locations. The dotted lines indicate chance performance on this task (50% correct). TF, Temporal frequency. B, Mean percentage-correct performance (± SEM) for subjects in Group 1 when performing a simple direction discrimination task with high-contrast, drifting gratings after training. Post-training performance at blind-field locations trained only on the static orientation discrimination task (Ori train only) were not significantly different from that in their intact hemifield of vision (Good field; see text for statistics). C, Mean coherence and DR thresholds (± SEM) for subjects in Group 1 following orientation training only. Post-training thresholds at blind-field locations trained only on the static orientation discrimination task (Ori train only) were significantly worse than thresholds in the same subjects' intact hemifields of vision (Good field). Data for B and C were collected in the laboratory with controlled fixation.

Figure 4.

Impact of training in Group 2 (double-trained) subjects. A, Percentage correct performance for CB4 across consecutive training sessions at one blind-field location trained on static orientation discrimination (upper graph) and one blind-field location trained with a global direction discrimination task (bottom graph). These two locations are indicated by circles on CB4's Humphrey field composite in Figure 2B. Improvement as a function of the number of training sessions can be seen at both trained locations. The dotted lines indicate chance performance on this task (50% correct). TF, Temporal frequency. B, Mean percentage-correct performance (± SEM) for the six subjects in Group 2 when doing a static orientation discrimination task in their intact hemifield of vision (white bars, Good field), blind-field locations where they were trained with the DR task (light gray bars, DR train) and blind-field locations trained on the static orientation discrimination task (dark gray bars, Ori train). Note that percentage-correct performance improves from approximately chance (Fig. 2F) to levels not significantly different from good field levels following both types of training (see text for statistics). C, DR thresholds (± SEM) for the six subjects in Group 2 when performing a global left–right direction discrimination task either in their intact hemifield of vision (Good field) or at blind-field locations trained either on DR (DR train) or static orientation discrimination (Ori train). Post-training performance at retrained blind-field locations was not significantly different from that in the intact hemifield of vision. D, Mean coherence thresholds (± SEM) for the six subjects in Group 2 following double training. As for DR thresholds, post-training coherence thresholds were not significantly different from those in the same subjects' intact hemifields of vision. Data for B–D were collected in the laboratory with controlled fixation.

Figure 5.

Transfer of learning to untrained direction and orientation axes. A, Comparison plot of post-training DR thresholds for coarse direction discrimination (180° direction difference) across four different directional axes (oriented arrows). Data are mean thresholds (± SEM) computed separately in the intact hemifield of vision (white dots, Good field), as well as at direction-trained (light gray dots, DR train) and orientation-trained (dark gray dots, Ori train) locations in the blind field of six double-trained CB subjects. Group 1 subjects did not provide reliable DR thresholds after training (Fig. 3C) and were thus not used in this task. In addition, among Group 2 subjects, post-training blind-field data were not collected for the direction-trained location in CB4 and the orientation-trained location in CB3. Statistical analysis (see text for details) revealed a lack of significant difference between performance at the trained and untrained axes of motion. B, Comparison plot of post-training luminance contrast thresholds for coarse orientation discrimination (90° direction difference) across four different orientation axes (indicated by oriented bars). Data are mean thresholds (±SEM) computed separately in the intact hemifield of vision as well as at direction-trained and orientation-trained locations in the blind field of five double-trained and two single-trained subjects. Labeling conventions are as in A. Among Group 2 subjects, post-training blind-field data were only collected in three of five subjects for the direction-trained location. Statistical analysis (see text for details) revealed a lack of significant difference between performance at the trained and untrained orientation axes, regardless of visual-field location tested. However, note that contrast thresholds were significantly worse in the trained blind-field locations relative to good field values. This contrast sensitivity deficit after training is further detailed in Figure 7. Data for this figure were collected in the laboratory with controlled fixation.

Figure 6.

Effects of coarse discrimination training on fine difference thresholds. A, Schematic of the same–different trial sequence used to measure direction difference thresholds using random dot stimuli in post-training CB subjects (left). Comparison plot (right) of post-training direction difference thresholds (mean ± SEM) in the intact hemifield of vision (white bar, Good field), and at the direction-trained (light gray bar, DR train) and orientation-trained (dark gray bar, Ori train) blind-field locations. Group 1 subjects were not tested on this task because of their difficulty in discriminating global motion direction (Fig. 3C). There was a significant impairment in difference thresholds at both direction-trained and orientation-trained blind-field locations, relative to the good field. B, Schematic of the same–different trial sequence used to measure orientation difference thresholds using static Gabors in post-training CB subjects (left). Comparison plot (right) of post-training direction difference thresholds (mean ± SEM) in the intact hemifield of vision (white bar, Good field), and at the direction-trained (light gray bar, DR train) and orientation-trained (dark gray bar, Ori train) blind-field locations. Data from Groups 1 and 2 are combined for this graph. There was a significant impairment in orientation difference thresholds at both direction-trained and orientation-trained blind-field locations, relative to the good field. Data for this figure were collected in the laboratory with controlled fixation.

Figure 7.

Effects of discrimination training on contrast sensitivity. A–F, CSFs for trained blind-field locations (gray dots) and corresponding locations in the intact hemifield of vision (white dots) for all subjects who underwent this test (total N values are indicated in each graph). Small dots (for Group 2 subjects) and triangles (for Group 1 subjects) indicate individual data points; large dots denote average contrast sensitivity across all subjects and groups at each spatial and temporal frequency (TF). Pretraining CSFs could not be measured in the blind field before the onset of training. As such, all data for this figure were collected after training, in the laboratory, with controlled fixation. Note that in all cases, regardless of the training administered, or whether the testing stimulus was static or moving, post-training CSFs were uniformly worse than those measured in the intact hemifield of vision. Schematics of training stimuli are shown on the left side of the graphs, while test stimuli and tasks are shown on top of the graphs. cpd, Cycles per degree.