Different properties of visual relearning after damage to early versus higher-level visual cortical areas

Abstract

The manipulation of visual perceptual learning is emerging as an important rehabilitation tool following visual system damage. Specificity of visual learning for training stimulus and task attributes has been used in prior work to infer a differential contribution of higher-level versus lower-level visual cortical areas to this process. The present study used a controlled experimental paradigm in felines to examine whether relearning of motion discrimination and the specificity of such relearning are differently influenced by damage at lower versus higher levels of the visual cortical hierarchy. Cats with damage to either early visual areas 17,18, and 19, or to higher-level, motion-processing lateral suprasylvian (LS) cortex were trained to perform visual tasks with controlled fixation. Animals with either type of lesion could relearn to discriminate the direction of motion of both drifting gratings and random dot stimuli in their impaired visual field. However, two factors emerged as critical for allowing transfer of learning to untrained motion stimuli: (1) an intact LS cortex and (2) more complex visual stimuli. Thus, while the hierarchical level of visual cortex damage did not seem to limit the ability to relearn motion discriminations, generalizability of relearning with a damaged visual system appeared to be influenced by both the areas damaged and the nature of the stimulus used during training.

Figures

Figure 1.

Experimental timeline. The thin black lines at the beginning of the trace indicate that eight cats were first trained to perform the required direction discrimination tasks (initial training) and then lesioned, while three cats received a cortical lesion first and then underwent initial behavioral training in intact regions of their visual field. The rest of the experimental timeline pertains to all 11 cats, which first underwent mapping of their visual deficit and pretraining tests. The cats were then trained at a first location in their impaired hemifields for 15–40 sessions at the rate of 1 session/d. This was followed by testing for transfer. Additional rounds of training at other locations within the impaired hemifield were performed in some of the animals, also followed by tests of transfer. Postmortem histology was performed at the end of experiment.

Figure 2.

Behavioral paradigm. A, During behavioral training and testing, cats were required to perform a left–right direction discrimination task that began when they precisely fixated a centrally placed target on a computer monitor in front of them for 1000 ms. A stimulus then appeared at a selected location in the central 40° of their visual field, drifting either leftward or rightward for 500 ms. Cats were required to maintain fixation on the central target during stimulus presentation. After 500 ms, the stimulus and fixation target disappeared and was replaced by two “response” spots. The cats were required to saccade to the rightmost spot on the monitor if the direction of motion of the stimulus had been to the right, and to the leftmost spot if the direction of motion had been to the left. This was immediately followed by auditory feedback that indicated the correctness of the response. B, Stimuli used for direction discrimination task in A included luminance-modulated, vertical sinewave gratings drifting either left or right. By varying luminance contrast, we measured contrast thresholds for discriminating left–right motion direction. Light gray dots randomly distributed within a circular aperture over a black background and drifting in a range of direction centered around the leftward or rightward vector were used to measure DR thresholds. Finally, light gray dots randomly distributed within a circular aperture over a black background and drifting either to the left or right (signal dots) or randomly (noise dots) were used to measure coherence thresholds.

Figure 3.

Anatomy of brain lesions. A, Coronal brain sections from one cat with a lesion of areas 17/18/19 (cat 6–010) in the left hemisphere. Sections shown were sampled at regular intervals between a region 7 mm posterior (P7) to 9 mm anterior (A9) to the interaural line. They were stained for cytochrome oxidase reactivity to show areas of intact gray matter (brown) and, by inference, the location and extent of the lesion (arrows). The lesion can be recognized in comparison with the intact hemisphere (right in this cat), as a region of missing gray matter. B, Coronal brain sections from one of the cats with a lesion of LS cortex, showing a large region of missing gray matter in the right hemisphere. Note, however, that the areas of early visual cortex damaged in cat 6–010 (A) are intact in cat 165, and vice versa.

Figure 4.

Effect of cortical lesions on DR thresholds: a mapping study. Maps of visual field space illustrating the location, size, and shape of visual stimuli used to measure DR threshold performance at different, nonoverlapping, visual field locations in each cat. Animals are separated according to lesion type (A, cats with 17/18/19 lesions and B, cats with LS lesions). Axes are labeled in degrees of visual angle. As defined previously, normal DR thresholds in the cat range from 11 to 35% (white circles). DR thresholds >35% were only seen contralateral to the brain lesion (right or left impaired hemifields denoted by light gray shading) in both groups. Deficits varied from mild (DR thresholds between 36 and 57%, gray circles) to severe (DR thresholds between 58 and 100%, black circles). The area of visual field covered by the most severe deficits differed among animals, and was largely consistent with the physical size of the brain lesion. For instance, cat 6–010 had one of the smallest areas of brain damage in corresponding regions of areas 17, 18, and 19 (Fig. 3A) and exhibited only a quadrant deficit. In contrast, cat 165 (Fig. 3B), who exhibited abnormal DR thresholds over practically his entire left hemifield of vision, had an almost complete destruction of LS cortex in his right hemisphere (Fig. 3B).

Figure 5.

Illustrative examples of postlesion testing and training in the impaired hemifield. A, Experimental timeline illustrating the time points at which data in B and C were collected. B, Postlesion contrast threshold performance of one cat with a lesion of areas 17/18/19. The map of the visual field identifies the exact locations where data shown in the adjacent two graphs were collected. T, Location that was subsequently trained, as shown in the associated scatter plot. The bar graph shows postlesion contrast thresholds before the onset of training in the impaired hemifield. Thresholds collected centrally (gray bar) and in the intact (left) hemifield (white bar) are normal and not significantly different from each other. However, contrast thresholds in the impaired hemifield (black bar) are significantly worse. The scatter plot illustrates how contrast thresholds improve as a function of repetitive, direction discrimination training with gratings whose contrast was varied in a staircase procedure at location T in the impaired hemifield of this cat. C, Postlesion DR threshold performance of one cat with a lesion of left LS cortex (cat 2–007). The map of the visual field illustrates the exact locations where data shown in the adjacent two graphs were collected. T, Location that was subsequently trained as shown in the associated scatter plot. The bar graph shows postlesion DR thresholds before the onset of training. Thresholds collected centrally (gray bar) and in the intact (left) hemifield (white bar) are normal and not significantly different from each other. However, DR thresholds in the impaired hemifield (black bar) are significantly worse. The scatter plot illustrates how these DR thresholds improve as a function of repetitive, direction discrimination training with random dot stimuli in which the range of dot directions was varied in a staircase procedure at location T in the impaired hemifield of this cat. Error bars = SEM. *p < 0.05, paired Student's t tests relative to intact hemifield values.

Figure 6.

Training improves discrimination thresholds for trained stimuli, regardless of lesion type. A, In this first experiment, cats were trained to discriminate the left–right direction of motion of sinewave gratings at 0.3 cycles/degree spatial frequency and drifting at 6 Hz. A staircase was used to progressively decrease stimulus contrast in each training session. B, Plot of contrast threshold in cats with 17/18/19 lesions in the intact hemifield (good field), in the impaired hemifield before training (bad field initial), and at the same location post-training (bad field post-training). Training gradually improved contrast thresholds at the trained locations in the contralesional visual hemifield (Fig. 5) until contrast thresholds were no longer significantly different from those in the intact hemifield of vision. C, Cats with LS lesions did not exhibit a significant deficit in contrast sensitivity for direction (compare black and white bars) and additional practice of this task in the impaired hemifield did not further improve the animals' contrast thresholds (gray bar). D, At a different, nonoverlapping location in their impaired hemifield, the same cats were trained to discriminate the left–right direction of motion of random dot stimuli in which the range of dot directions was varied from easier to harder levels in each session. E, Before training, cats with 17/18/19 lesions exhibited significantly raised DR thresholds (black bars). Training improved these abnormal thresholds back to normal levels (gray bars). F, A very similar pattern of postlesion deficit and training-induced recovery of DR thresholds was seen in cats with LS lesions. G, Finally, at yet another location in the impaired hemifield of vision, cats were trained to discriminate the left–right direction of motion of random dot stimuli in which the proportion of coherently moving dots was varied using a staircase procedure in each session. H, Before the onset of training, cats with lesions of areas 17/18/19 exhibited significantly higher coherence thresholds in the contralesional (black bars) versus the ipsilesional hemifield (white bars). Just as in B and E, specific training gradually improved impaired coherence thresholds back to normal levels (gray bars) at the trained locations. I, A similar pattern of postlesion deficit and training-induced recovery of coherence thresholds was seen in cats with LS lesions. The number of cats used in each portion of the experiment is shown as N. All values given are means ± SEM. *p < 0.05, paired Student's t tests relative to intact hemifield values. CS, Contrast sensitivity; Coh, coherence.

Figure 7.

Training to discriminate direction of sinewave gratings does not improve global motion thresholds. A, In this experiment, postlesion cats were retrained to discriminate the left–right direction of motion of drifting sinewave gratings at one location in their impaired (contralesional) hemifield of vision. Once contrast thresholds had stabilized at normal levels of performance in each animal, DR and/or coherence thresholds were remeasured at the trained locations. B, Effect of contrast sensitivity training on DR thresholds in cats with 17/18/19 lesions, showing a lack of transfer of learning. C, Practicing the contrast sensitivity task also failed to improve DR thresholds in the impaired hemifield of cats with LS lesions. D, Contrast sensitivity training also failed to transfer to coherence thresholds in cats with 17/18/19 lesions. E, Practicing the contrast sensitivity task failed to improve coherence thresholds in the impaired hemifield of cats with LS lesions. Values are means ± SEM; *p < 0.05, two-tailed Student's t test relative to intact hemifield performance (white bars). Other conventions are the same as those in Figure 6.

Figure 8.

Global motion training improves contrast sensitivity for direction following lesions of areas 17/18/19. A, Schematic diagram of experiment in which cats were trained to discriminate the left–right direction of motion of random dot stimuli in which the DR was varied from easier to harder levels in each session. After recovering normal DR thresholds, contrast thresholds were measured using drifting gratings and coherence thresholds were measured using random dot stimuli. B, Plot of contrast thresholds in cats with 17/18/19 lesions either in the intact hemifield (white bar), the impaired hemifield before training (black bar), or at the same impaired hemifield locations after DR training (gray bar). DR training with random dot stimuli not only recovered DR thresholds (see Fig. 6) but also contrast sensitivity at trained locations in the impaired hemifield. C, Plot of coherence thresholds in cats with 17/18/19 lesions in the intact hemifield, the impaired hemifield before DR training, and after DR training, showing that DR training also improved coherence thresholds in these cats. This was in contrast with data obtained in five of the cats with LS lesions and shown in D, in which DR training did not improve coherence thresholds relative to pretraining levels. All values are means ± SEM; *p < 0.05, two-tailed Student's t test relative to the intact hemifield values. Other conventions are the same as those in Figures 6 and 7.

Figure 9.

Retinotopic specificity of learning. A, Plot of DR thresholds in prelesion cats following initial behavioral training centrally. Once learning occurred and DR thresholds stabilized centrally, there was no significant drop in performance out to ∼16° eccentricity in visually intact animals. Note that distance from trained location (TL) here is equivalent to eccentricity, with training location center coordinates 0,0. B, Equivalent plot to that shown in A, but with data collected postlesion in the center of the visual field (0,0) and in the intact hemifield of six of the LS lesioned cats (white symbols) and all three of the cats with lesions of areas 17/18/19 (black symbols). Even postlesion, there was no significant correlation between DR thresholds and distance from the originally trained location at 0,0 in intact regions of the visual field. C, Retinotopic specificity of DR relearning postlesion in the same animals whose data are plotted in B. Here, the magnitude of improvement in DR thresholds is plotted relative to pretraining (postlesion) values in cats with lesions of areas 17/18/19 (black dots) or LS cortex (white dots) as a function of distance from the trained (in this case, peripheral) impaired hemifield locations. Trained locations are always plotted at a distance of 0°. The magnitude of improvements decreased with increasing distance from the TLs. This decrease was significantly greater in cats with early visual cortex lesions than in cats with LS lesions. R2 = 0.42 for LS lesions and 0.50 for 17/18/19 lesions. D, Plot of change in DR thresholds relative to pretraining (postlesion) values versus eccentricity (degree), showing no significant correlation between training-induced improvement and eccentricity in either lesion group. R2 = 0.00002 for LS lesions and 0.064 for 17/18/19 lesions.