Non-feature-specific elevated responses and feature-specific backward replay in human brain induced by visual sequence exposure
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eLife Assessment
This valuable study investigates both online responses to, and offline replay of, visual motion sequences. Sophisticated EEG analyses provide solid evidence for both feature-specific and non-specific sequence representations, though the explanation of the statistical methods used is currently incomplete.
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Abstract
The ability of cortical circuits to adapt in response to experience is a fundamental property of the brain. After exposure to a moving dot sequence, flashing a dot as cue at the starting point of the sequence can induce successive elevated responses even in the absence of the sequence. This cue-triggered elevated responses have been demonstrated to play a crucial role in predicting future events in dynamic environments. However, temporal sequences we are exposed usually contain rich feature information. It remains unknown whether the elevated responses are feature specific and, more crucially, how the brain organizes this sequence information after exposure. To address these questions, participants were exposed to a predefined sequence of four motion directions for about 30 min and subsequently presented with the start or end motion direction of the sequence as a cue. Surprisingly, we found that the cue-triggered elevated responses were not specific to a particular motion direction. Interestingly, the motion direction information was spontaneously reactivated and the motion sequence was backward replayed in a time-compressed manner. These effects were marginally significant even with brief exposure. Notably, no replay events were observed when the second or third motion direction of the sequence served as a cue. Further analyses revealed that activity in the medial temporal lobe (MTL) preceded the ripple power increase in visual cortex at replay onset, implying a coordinated relationship between the activities in the MTL and visual cortex. Together, we demonstrate that visual sequence exposure could induce two-fold brain plasticity that may simultaneously serve for different functional purposes. The non-feature-specific elevated responses may facilitate general processing of upcoming stimuli, whereas the feature-specific backward replay may underpin passive learning of visual sequence.
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eLife Assessment
This valuable study investigates both online responses to, and offline replay of, visual motion sequences. Sophisticated EEG analyses provide solid evidence for both feature-specific and non-specific sequence representations, though the explanation of the statistical methods used is currently incomplete.
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Reviewer #1 (Public review):
Summary:
The study identifies two types of activation: one that is cue-triggered and non-specific to motion directions, and another that is specific to the exposed motion directions but occurs in a reversed manner. The finding that activity in the medial temporal lobe (MTL) preceded that in the visual cortex suggests that the visual cortex may serve as a platform for the manifestation of replay events, which potentially enhance visual sequence learning.
Strengths:
Identifying the two types of activation after exposure to a sequence of motion directions is very interesting. The experimental design, procedures, and analyses are solid. The findings are interesting and novel.
Weaknesses:
It was not immediately clear to me why the second type of activation was suggested to occur spontaneously. The procedural …
Reviewer #1 (Public review):
Summary:
The study identifies two types of activation: one that is cue-triggered and non-specific to motion directions, and another that is specific to the exposed motion directions but occurs in a reversed manner. The finding that activity in the medial temporal lobe (MTL) preceded that in the visual cortex suggests that the visual cortex may serve as a platform for the manifestation of replay events, which potentially enhance visual sequence learning.
Strengths:
Identifying the two types of activation after exposure to a sequence of motion directions is very interesting. The experimental design, procedures, and analyses are solid. The findings are interesting and novel.
Weaknesses:
It was not immediately clear to me why the second type of activation was suggested to occur spontaneously. The procedural differences in the analyses that distinguished between the two types of activation need to be a little better clarified.
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Reviewer #2 (Public review):
This paper shows and analyzes an interesting phenomenon. It shows that when people are exposed to sequences of moving dots (that is moving dots in one direction, followed by another direction, etc.), showing either the starting movement direction or ending movement direction causes a coarse-grained brain response that is similar to that elicited by the complete sequence of 4 directions. However, they show by decoding the sensor responses that this brain activity actually does not carry information about the actual sequence and the motion directions, at least not on the time scale of the initial sequence. They also show a reverse reply on a highly compressed time scale, which is elicited during the period of elevated activity, and activated by the first and last elements of the sequence, but not others. …
Reviewer #2 (Public review):
This paper shows and analyzes an interesting phenomenon. It shows that when people are exposed to sequences of moving dots (that is moving dots in one direction, followed by another direction, etc.), showing either the starting movement direction or ending movement direction causes a coarse-grained brain response that is similar to that elicited by the complete sequence of 4 directions. However, they show by decoding the sensor responses that this brain activity actually does not carry information about the actual sequence and the motion directions, at least not on the time scale of the initial sequence. They also show a reverse reply on a highly compressed time scale, which is elicited during the period of elevated activity, and activated by the first and last elements of the sequence, but not others. Additionally, these replays seem to occur during periods of cortical ripples, similar to what is found in animal studies.
These results are intriguing. They are based on MEG recordings in humans, and finding such replays in humans is novel. Also, this is based on what seems to be sophisticated statistical analysis. However, this is the main problem with this paper. The statistical analysis is not explained well at all, and therefore its validity is hard to evaluate. I am not at all saying it is incorrect; what I am saying is that given how it is explained, it cannot be evaluated.
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