We used a texture discrimination task, a standard task in studies of visual perceptual learning (Censor et al., 2006
; Karni and Sagi, 1991
; Karni et al., 1994
; Mednick et al., 2002
; Ofen et al., 2007
; Schwartz et al., 2002
; Stickgold et al., 2000
; Walker et al., 2005
). As illustrated in , the study involved six behavioral training sessions (black bars) and four fMRI sessions (gray bars) in Experiment 1. In each training trial, we presented a textured display along with a target array that was consistently displayed in the same visual field quadrant (i.e. the upper left visual field). Subjects (n=6) performed two types of tasks. One was to identify a letter presented at the central fixation point, whether the letter ‘T’ or the letter ‘L’. This task was used primarily to ensure subjects’ eye fixation. The other task was to report the orientation of a target array presented in a peripheral position for short duration. Performance in this second task was subject to learning. The subjects were asked to respond first to the letter task and then to the orientation task. There, a mask appeared at an interval after target array presentation. We refer to the interval as stimulus-to-mask-onset asynchrony, or SOA. We employed various SOAs in the training sessions in order to obtain a psychometric function for determining an 80% threshold SOA. Shortening of the threshold after repetitive performance was considered an indication that PL had taken place ().
Figure 1 Experimental design. We conducted four fMRI sessions. Experiment 1 (n=6) involved six training sessions conducted until post 2 (each session is represented as a black bar). The average time intervals (± standard errors) between the initial training (more ...)
Figure 2 Results. (A) The averaged threshold SOA (± standard errors) across all subjects in Experiment 1. (B) Mean performance (± standard errors) in the trained (circles) and untrained (squares) locations in Experiment 1. (C, D) Mean location-specific (more ...)
Four separate measurements of each subject’s brain activation with 3 Tesla fMRI and assessment of task performance during the fMRI acquisition (for details, see Experimental procedures
) were made before the start of training (pre-training), 10–25 hours (next day) after initial training (post-training 1), 10–14 days after initial training (post-training 2), and 4 weeks after initial training (post-training 3) (see ). Each fMRI session involved two conditions for the location of stimulus presentation (for detail see Experimental procedures
). The texture discrimination task is known to have location specificity (Karni and Sagi, 1991
). To estimate a location specific training effect in V1, we presented the target arrays not only in the trained location (upper left visual field), but also in an untrained location (lower right visual field) only
in the fMRI sessions. While the two location conditions were presented from trial to trial in a random order in an event-related fMRI paradigm, SOA was constant at 100 msec, as determined from our preliminary data.
shows the threshold SOAs observed in the behavioral training sessions. The threshold SOA reached asymptotes in 5–6 days, corresponding to the original literature (Karni and Sagi, 1991
). indicates that while performance improvement is observed in the trained condition (ANOVA with repeated measurement, F(3,15)=17.28, p<0.001; post-hoc t-tests, post 2 vs pre-training, p<0.003; post 3 vs pre-training, p<0.03), no significant improvement was observed in the untrained condition. shows location-specific performance or fMRI activation that are defined as f(1, j
)/f(1, 0) −f(0, j
)/f(0, 0), where f(i
) represents fMRI performance or BOLD signal in a location i
(0=untrained location, 1=trained location) and in post j
(post 0=pre-training phase, post 1, 2, 3=post-training phases), respectively (see Supplementary Figure 1
for BOLD signal changes).
Phase effects in both performance and fMRI activation were significant (ANOVA, p<0.01, p<0.05, respectively) in Experiment 1. The location-specific performance in posts 2 and 3 was significantly higher than in the pre-training stage (post-hoc t-tests, p<0.01, p<0.05, respectively).
To our surprise, however, location-specific fMRI activation in V1 (), which was boosted at posts 1 and 2 (post-hoc t-test; p<0.01 and p<0.05 for pre- vs post 1-training and pre- and post 2- training, respectively), decreased to the baseline level (defined as the location-specific activation in V1 in the pre-training phase) at post 3 (p<0.70 for pre- and post 3- training). A significant quadratic trend (F(1,5)=8.9, p<0.05) was obtained. Thus, there are two distinctive patterns of dynamic relations between performance enhancement and neural activation changes in V1 in different stages of the time course of PL. For the initial few weeks after the onset of training, performance improvement and activation increase in V1 occurred. After that period, the V1 activation enhancement vanishes while the improved performance is maintained.
Note that a consistent SOA (100 msec) was used throughout fMRI phases to evaluate and compare brain activation and performance in the sessions. A relatively short or difficult SOA had to be used to avoid a ceiling effect in later phases such as post 2 and 3. The 100 msec SOA might have been so short that learning effects, if any, were not shown until thresholds became below 100 msec. Thus, although the correct response ratio was low in the trained location in the post 1 fMRI session (), this does not necessarily indicate that learning did not occur from the pre-training to post 1 phases. indicates that the 80% threshold SOA in the Day 2 training phase was significantly lower than in the Day 1 training phase but still higher than the 100 msec SOA. This indicates significant learning indeed occurred from the Day1 to Day2 training phases, as originally shown (Karni and Sagi, 1991
). There was a high correlation (r=0.82) between the amount of SOA threshold improvement from the Day 1 to Day 2 training phases (Day1 –Day 2 thresholds) and the amount of changes in location-specific fMRI activation from the pre-training to post1 phases (see Supplementary Fig. 2
for correlations between threshold changes and MRI signal changes).
The V1 activation reduction in Experiment 1 occurred after training was terminated. One hypothesis for the reduction is that the enhancement in V1 activation in posts 1 and 2 is related to training and the reduction in post 3 is due to the termination of training. If this is the case, additional training until post 3 will produce enhanced V1 index at post 3. The counter-hypothesis is that the reduction in post 3 is not due to the termination of training. To test which hypothesis is correct, we conducted a control experiment, Experiment 2, in which a new group of subjects (n=5) received continued
training between posts 2 and 3; all other conditions were identical to those of the Experiment 1. The subject participated in 14 behavioral training sessions over a span of four weeks (black and white bars in , see Supplementary Fig. 3
for the threshold SOA in the behavioral training sessions and fMRI sessions in Experiment 2). indicates generally the same tendency as those in Experiment 1, allowing us to thus conclude that the V1 activation reduction is not due to termination of training. Note that the mean V1 and performance indices in post 1 in Experiment 2 were higher than in Experiment 1. This may be attributed to initially better performance with the subjects overall in Experiment 2 (See Supplementary Fig. 3A
). The 80% thresholds in the initial training phase (Day 1) with control subjects were lower than with the subjects in Experiment 1. The initially higher individual performance in Experiment 2 than in Experiment 1 may have led the onsets of both performance saturation (post 1) and the V1 index drop (post 2) in Experiment 2 to occur more early than in Experiment 1. That is, the onsets of learning saturation and the V1 index drop may be influenced by individual differences to some degree.
We analyzed the reaction times in the trained and untrained locations in the fMRI experiments. shows results on reaction time to the texture orientation task in Experiment 1. The results of 2-way ANOVA (phase and location) with repeated measurement showed a significant phase effect (p<0.01) but did not show a significant effect in location. Post-hoc t-tests showed that there were significant differences between the pre-training and post 2 for both the trained location (p< 0.01) and the untrained location (p< 0.01), between the pre-training and post 3 for both the trained location (p<0.001) and the untrained location (p< 0.002). The same tendency was seen with the reaction times in Experiment 2, shown in Supplementary Fig. 4A
Figure 3 Reaction time to the orientation task, activated region size, and correct response ratio for the fixational letter task in Experiment 1. (A) The reaction time to the orientation task was defined as the time interval from the onset of the target stimulus (more ...)
Did activated size in V1 in Experiment 1 change over time? shows the activated region size in V1. The results of 2-way ANOVA with repeated measurement (phase and location) showed no significant difference in either factor. The activated size in V1 in Experiment 2 is shown in Supplementary Fig. 4B
, indicating that there were no significant phase and location effects, either.
Did the subjects improve the fixation task? We analyzed the performance for the fixation letter task over time. shows the correct response ratio for the fixational letter task in Experiment 1. The results of 1-way ANOVA with repeated measurement showed no significant effects in the phase factor. The ratios were consistently high throughout the training, indicating that the subjects fixated very well during experiments. The correct response ratio for the fixational letter task in Experiment 2 (Supplementary Fig. 4C
) showed the same tendency. Furthermore, we conducted Experiment 3 in which reaction times as well as accuracy to the letter task were measured with 4 subjects and “fMRI sessions” were conducted in a mock scanner so that only performance was obtained, with the otherwise same procedure as in Experiment 1. The results of one-way ANOVA with repeated measurement applied separately to the RTs and accuracy data in Experiment 3 did not show any significant effects of either RTs or accuracy (Supplementary Fig. 5
). These results suggest that performance for the central task remained constant and that the performance benefit for the peripheral task was not due to a differential allocation of attentional resources throughout the different sessions.
Do other brain areas including the visual areas such as V2 and V3 and higher cognitive areas such as the intraparietal sulcus, superior parietal gyrus, and middle frontal gyrus show similar activation changes during the time course of learning like V1 where a novel dynamic activation during the time course of perceptual learning was found? We combined the data from Experiments 1 and 2, since there was no significant difference between the two experiments as a result of ANOVA. First, we applied ANOVA with repeated measurement (phase) to indices for each of these areas. No significant differences were found in any of the areas except for V1 (). The V1 indices at post 1 and post 2 were both significantly higher than the baseline (t-tests, p<0.001, p<0.005, respectively). The amount of difference between the V1 indices in posts 2 and 3 was significantly larger than that between posts 1 and 3 (t(10)=2.281, p<0.05). Second, we applied a trend analysis to each of the areas. V1 showed a significant quadratic trend (F(1,10)=12.06, p<0.001). In contract, none of the other areas showed any of linear, quadratic, or cubic trends. Third, correlation coefficients between V1 and each of V2, V3, the intraparietal sulcus, superior parietal gyrus and the middle frontal gyrus across the subjects were rather small, 0.33, 0.12, 0.07, −0.15 and 0.09, respectively. At the same time, the results of two-way ANOVA with repeated measurement (phase and area) to each combination of V1 and one of the five other areas indicated that except for area as a factor for V1 vs the middle-frontal gyrus (F(1, 10)=7.49, p<0.021) with no significant interaction between the phase and area factors, no other significant effect was found in any combination between V1 and one of the five areas. These results seem to be due to much larger standard errors across the subjects in the five areas than V1 (). Thus, we conclude to state that no clear result was obtained to discuss a tendency in the analyzed areas other than V1.
Figure 4 The mean activation indices (± standard errors) for fMRI responses in V1 (A), V2 and V3 (B), and IPS (the intraparietal sulcus), SPG (the superior parietal gyrus) and MFG (the middle frontal gyrus) (C), from the results from Experiment 1 combined (more ...)
Can the fMRI activation drop in V1 from posts 2 and 3 be attributed to modified attention? There were no significant differences in either correct response ratios () or reaction times for orientation tasks () between posts 2 and 3 (therefore, no evidence for task-load change). Furthermore, as aforementioned, there was no significant fMRI activation change in the time course of learning in other analyzed areas than V1. Thus, there is no clear evidence that the activation drop in V1 from posts 2 to 3 was due to modified attention.