The present study is the first to measure brain activation with and without preceding training of a visual task during sleep that utilized concurrent fMRI and PSG recordings. The latter allows for precise identification of on-going sleep status. The results revealed significantly increased activation specifically in the trained location of V1 during NREM sleep subsequent to the training of a visual task. This increased activation in the trained region was specific to the sleep status. Notably, the amount of activation in the trained location of V1 during sleep in the post-training fMRI session was highly correlated with performance improvement after sleep. These results indicate that activity enhancement specifically in the trained location of V1 during sleep reflects processing that improves visual perceptual learning and are in accord with the hypothesis that consolidation of learning occurs during sleep after training.
Two models have been proposed to account for performance enhancement after sleep subsequent to training for learning in general; synaptic homeostasis model [15
] and reactivation model [16
]. The reactivation model indicates that neurons that are involved in learning acquisition are covertly reactivated during sleep to strengthen neuronal connections [16
]. For example, firing-rate patterns during training of episodic memory in cortical areas including the hippocampus and the medial prefrontal cortex in rats [19
]. In addition, it has been shown that the brain regions, which were recruited during the training showed enhanced brain activation during sleep in human PET studies [21
]. The reactivation model predicts activation in the area highly related to trained memory/learning during sleep and is in accord with the present finding of BOLD signal enhancement in the trained area of V1 during sleep and performance enhancement after the sleep. The synaptic homeostasis model [15
] indicates that slow-wave activity, which is prominent during early NREM sleep, plays a role in scaling down synapses including those that are excessively increased or strengthened by a learning acquisition process during wakefulness. This model is supported by increased slow-wave activity near the motor and parietal areas in the right hemisphere during sleep after implicit motor learning [23
]. While this model is highly intriguing, from our results, which are not based on any spectral analysis, it is difficult to judge the validity of the homeostasis model. If a downscaling requires an active molecular process (cf. [24
]) resulting in increased metabolism, the present result would be in accordance with synaptic homeostasis model.
In the current study, we had an apriori
anatomical hypothesis that in V1 the sleep consolidation process in visual perceptual learning occurs specifically in the trained region. To test the hypothesis, we made a pre-determined ROI analysis that targeted V1 and obtained results supporting the hypothesis. Although the result was in accord with our hypothesis, note that this does not indicate that other areas are not involved in consolidation of sleep. Some suggest that post-sleep changes on this task have been identified in the later visual cortical regions - both within the occipital, temporal and parietal areas [9
]. In addition, the dramatic connectivity changes during NREM sleep [11
] may suggest that a learned representation during wakefulness may lead to plasticity processes not only in the trained location, but in reciprocal areas connected to it as well. For example, Schwartz et al. indicate that connectivity of other areas including the left frontal cortex, to V1 that was observed at the beginning of training disappeared 24 hours after training of TDT in visual perceptual learning [4
]. Thus, examining connectivity during sleep after training would constitute an important future study. Since location of target presentation was counterbalanced across the subjects in the present experiment, this design is not suitable for analysis of multiple brain areas. However, to obtain some idea, sleep activation in the whole cortex is shown in Supplemental SFig. 6
. This shows enhanced activity in the trained region of V1 that was found to be significant when predetermined ROI analysis was applied as aforementioned. Though less clearly, some activity in the left dorsolateral prefrontal area was also observed (see Supplemental Result 4
for the limitation of this analysis to our data). A future study with an experimental design suitable for multiple areas analyses would clarify whether the left dorsolateral prefrontal area activation is significantly involved in consolidation during sleep.
In the present study, we did not investigate brain activation during REM sleep. While we found trained region specific brain activation in V1 associated with consolidation of visual perceptual learning during NREM sleep, it is possible that REM sleep also plays a role in consolidation of visual perceptual learning [16
]. Previous studies have indicated the involvement of REM sleep in consolidation of the visual task used in the present study [6
]. PET studies in humans have also shown involvement of REM sleep: Activation in the brain regions, which were recruited for the visuomotor training before the sleep was enhanced [21
], with changed connectivity between the frontal and parietal regions [30
] during REM sleep. Thus, it is possible that the trained region specific activation in V1 during NREM sleep, which was found in our study, is just a part of multiple stages of consolidation processing during sleep which usually lasts several hours in adults [11
]. Future studies are required to test this possibility.
In the present study, we measured and compared BOLD signal during sleep with and without preceding visual training with concurrent PSG measurement. For the first time, we observed a significant amount of activation specifically in the trained region of V1 during sleep after training of a visual task that was highly correlated with performance increase after sleep. In this initial study, we utilized ROI analysis and concentrated on examining activation in V1. Future studies should clarify whether brain areas other than V1 are also involved and how cortical connectivity of the trained area of V1 to other areas may change during sleep after training, as well as how REM sleep is involved in sleep consolidation.