Cross-modal interaction of Alpha Activity does not reflect inhibition of early sensory processing: A frequency tagging study using EEG and MEG
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This manuscript addresses the role of alpha oscillations in sensory gain control. The authors use an attention-cuing task in an initial EEG study followed by a separate MEG replication study to demonstrate that whilst (occipital) alpha oscillations are increased when anticipating an auditory target, so is visual responsiveness as assessed with frequency tagging. The authors propose their results demonstrate a general vigilance effect on sensory processing and offer a re-interpretation of the inhibitory role of the alpha rhythm. While these results are valuable, the provided evidence is incomplete.
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Abstract
Selective attention involves prioritizing relevant sensory input while suppressing irrelevant stimuli. It has been proposed that oscillatory alpha-band activity (∼10 Hz) aids this process by functionally inhibiting early sensory regions. However, recent studies have challenged this notion. Our EEG and MEG studies aimed to investigate whether alpha oscillations serve as a ‘gatekeeper’ for downstream signal transmission. We first observed these effects in an EEG study and then replicated them using MEG, which allowed us to localize the sources.We employed a cross-modal paradigm where visual cues indicated whether upcoming targets required visual or auditory discrimination. To assess inhibition, we utilized frequency-tagging, simultaneously flickering the fixation cross at 36 Hz and playing amplitude-modulated white noise at 40 Hz during the cue-to-target interval.Consistent with prior research, we observed an increase in posterior alpha activity following cues signalling auditory targets. However, remarkably, both visual and auditory frequency tagged responses amplified in anticipation of auditory targets, correlating with alpha activity amplitude. Our findings suggest that when attention shifts to auditory processing, the visual stream remains responsive and is not hindered by occipital alpha activity. This implies that alpha modulation does not solely regulate ‘gain control’ in early sensory areas but rather orchestrates signal transmission to later stages of the processing stream.
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eLife Assessment
This manuscript addresses the role of alpha oscillations in sensory gain control. The authors use an attention-cuing task in an initial EEG study followed by a separate MEG replication study to demonstrate that whilst (occipital) alpha oscillations are increased when anticipating an auditory target, so is visual responsiveness as assessed with frequency tagging. The authors propose their results demonstrate a general vigilance effect on sensory processing and offer a re-interpretation of the inhibitory role of the alpha rhythm. While these results are valuable, the provided evidence is incomplete.
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Reviewer #1 (Public review):
In this paper by Brickwedde et al., the authors observe an increase in posterior alpha when anticipating auditory as opposed to visual targets. The authors also observe an enhancement in both visual and auditory steady-state sensory evoked potentials in anticipation of auditory targets, in correlation with enhanced occipital alpha. The authors conclude that alpha does not reflect inhibition of early sensory processing, but rather orchestrates signal transmission to later stages of the sensory processing stream. However, there are several major concerns that need to be addressed in order to draw this conclusion.
First, I am not convinced that the frequency tagging method and the associated analyses are adequate for dissociating visual vs auditory steady-state sensory evoked potentials.
Second, if the authors …
Reviewer #1 (Public review):
In this paper by Brickwedde et al., the authors observe an increase in posterior alpha when anticipating auditory as opposed to visual targets. The authors also observe an enhancement in both visual and auditory steady-state sensory evoked potentials in anticipation of auditory targets, in correlation with enhanced occipital alpha. The authors conclude that alpha does not reflect inhibition of early sensory processing, but rather orchestrates signal transmission to later stages of the sensory processing stream. However, there are several major concerns that need to be addressed in order to draw this conclusion.
First, I am not convinced that the frequency tagging method and the associated analyses are adequate for dissociating visual vs auditory steady-state sensory evoked potentials.
Second, if the authors want to propose a general revision for the function of alpha, it would be important to show that alpha effects in the visual cortex for visual perception are analogous to alpha effects in the auditory cortex for auditory perception.
Third, the authors propose an alternative function for alpha - that alpha orchestrates signal transmission to later stages of the sensory processing stream. However, the supporting evidence for this alternative function is lacking. I will elaborate on these major concerns below.
(1) Potential bleed-over across frequencies in the spectral domain is a major concern for all of the results in this paper. The fact that alpha power, 36Hz and 40Hz frequency-tagged amplitude and 4Hz intermodulation frequency power is generally correlated with one another amplifies this concern. The authors are attaching specific meaning to each of these frequencies, but perhaps there is simply a broadband increase in neural activity when anticipating an auditory target compared to a visual target?
(2) Moreover, 36Hz visual and 40Hz auditory signals are expected to be filtered in the neocortex. Applying standard filters and Hilbert transform to estimate sensory evoked potentials appears to rely on huge assumptions that are not fully substantiated in this paper. In Figure 4, 36Hz "visual" and 40Hz "auditory" signals seem largely indistinguishable from one another, suggesting that the analysis failed to fully demix these signals.
(3) The asymmetric results in the visual and auditory modalities preclude a modality-general conclusion about the function of alpha. However, much of the language seems to generalize across sensory modalities (e.g., use of the term 'sensory' rather than 'visual').
(4) In this vein, some of the conclusions would be far more convincing if there was at least a trend towards symmetry in source-localized analyses of MEG signals. For example, how does alpha power in the primary auditory cortex (A1) compare when anticipating auditory vs visual target? What do the frequency-tagged visual and auditory responses look like when just looking at the primary visual cortex (V1) or A1?
(5) Blinking would have a huge impact on the subject's ability to ignore the visual distractor. The best thing to do would be to exclude from analysis all trials where the subjects blinked during the cue-to-target interval. The authors mention that in the MEG experiment, "To remove blinks, trials with very large eye-movements (> 10 degrees of visual angle) were removed from the data (See supplement Fig. 5)." This sentence needs to be clarified since eye-movements cannot be measured during blinking. In addition, it seems possible to remove putative blink trials from EEG experiments as well, since blinks can be detected in the EEG signals.
(6) It would be interesting to examine the neutral cue trials in this task. For example, comparing auditory vs visual vs neutral cue conditions would be indicative of whether alpha was actively recruited or actively suppressed. In addition, comparing spectral activity during cue-to-target period on neutral-cue auditory correct vs incorrect trials should mimic the comparison of auditory-cue vs visual-cue trials. Likewise, neutral-cue visual correct vs incorrect trials should mimic the attention-related differences in visual-cue vs auditory-cue trials.
(7) In the abstract, the authors state that "This implies that alpha modulation does not solely regulate 'gain control' in early sensory areas but rather orchestrates signal transmission to later stages of the processing stream." However, I don't see any supporting evidence for the latter claim, that alpha orchestrates signal transmission to later stages of the processing stream. If the authors are claiming an alternative function to alpha, this claim should be strongly substantiated.
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Reviewer #2 (Public review):
Brickwedde et al. investigate the role of alpha oscillations in allocating intermodal attention. A first EEG study is followed up with a MEG study that largely replicates the pattern of results (with small to be expected differences). They conclude that a brief increase in the amplitude of auditory and visual stimulus-driven continuous (steady-state) brain responses prior to the presentation of an auditory - but not visual - target speaks to the modulating role of alpha that leads them to revise a prevalent model of gating-by-inhibition.
Overall, this is an interesting study on a timely question, conducted with methods and analysis that are state-of-the-art. I am particularly impressed by the author's decision to replicate the earlier EEG experiment in MEG following the reviewer's comments on the original …
Reviewer #2 (Public review):
Brickwedde et al. investigate the role of alpha oscillations in allocating intermodal attention. A first EEG study is followed up with a MEG study that largely replicates the pattern of results (with small to be expected differences). They conclude that a brief increase in the amplitude of auditory and visual stimulus-driven continuous (steady-state) brain responses prior to the presentation of an auditory - but not visual - target speaks to the modulating role of alpha that leads them to revise a prevalent model of gating-by-inhibition.
Overall, this is an interesting study on a timely question, conducted with methods and analysis that are state-of-the-art. I am particularly impressed by the author's decision to replicate the earlier EEG experiment in MEG following the reviewer's comments on the original submission. Evidently, great care was taken to accommodate the reviewer's suggestions.
Nevertheless, I am struggling with the report for two main reasons: It is difficult to follow the rationale of the study, due to structural issues with the narrative and missing information or justifications for design and analysis decisions, and I am not convinced that the evidence is strong, or even relevant enough for revising the mentioned alpha inhibition theory. Both points are detailed further below.
Strength/relevance of evidence for model revision: The main argument rests on 1) a rather sustained alpha effect following the modality cue, 2) a rather transient effect on steady-state responses just before the expected presentation of a stimulus, and 3) a correlation between those two. Wouldn't the authors expect a sustained effect on sensory processing, as measured by steady-state amplitude irrespective of which of the scenarios described in Figure 1A (original vs revised alpha inhibition theory) applies? Also, doesn't this speak to the role of expectation effects due to consistent stimulus timing? An alternative explanation for the results may look like this: Modality-general increased steady-state responses prior to the expected audio stimulus onset are due to increased attention/vigilance. This effect may be exclusive (or more pronounced) in the attend-audio condition due to higher precision in temporal processing in the auditory sense or, vice versa, too smeared in time due to the inferior temporal resolution of visual processing for the attend-vision condition to be picked up consistently. As expectation effects will build up over the course of the experiment, i.e., while the participant is learning about the consistent stimulus timing, the correlation with alpha power may then be explained by a similar but potentially unrelated increase in alpha power over time.
Structural issues with the narrative and missing information: Here, I am mostly concerned with how this makes the research difficult to access for the reader. I list the major points below:
In the introduction the authors pit the original idea about alpha's role in gating against some recent contradictory results. If it's the aim of the study to provide evidence for either/or, predictions for the results from each perspective are missing. Also, it remains unclear how this relates to the distinction between original vs revised alpha inhibition theory (Fig. 1A). Relatedly if this revision is an outcome rather than a postulation for this study, it shouldn't be featured in the first figure.
The analysis of the intermodulation frequency makes a surprise entrance at the end of the Results section without an introduction as to its relevance for the study. This is provided only in the discussion, but with reference to multisensory integration, whereas the main focus of the study is focussed attention on one sense. (Relatedly, the reference to "theta oscillations" in this sections seems unclear without a reference to the overlapping frequency range, and potentially more explanation.) Overall, if there's no immediate relevance to this analysis, I would suggest removing it.
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Reviewer #3 (Public review):
Brickwedde et al. attempt to clarify the role of alpha in sensory gain modulation by exploring the relationship between attention-related changes in alpha and attention-related changes in sensory-evoked responses, which surprisingly few studies have examined given the prevalence of the alpha inhibition hypothesis. The authors use robust methods and provide novel evidence that alpha likely exhibits inhibitory control over later processing, as opposed to early sensory processing, by providing source-localization data in a cross-modal attention task.
This paper seems very strong, particularly given that the follow-up MEG study both (a) clarifies the task design and separates the effect of distractor stimuli into other experimental blocks, and (b) provides source-localization data to more concretely address …
Reviewer #3 (Public review):
Brickwedde et al. attempt to clarify the role of alpha in sensory gain modulation by exploring the relationship between attention-related changes in alpha and attention-related changes in sensory-evoked responses, which surprisingly few studies have examined given the prevalence of the alpha inhibition hypothesis. The authors use robust methods and provide novel evidence that alpha likely exhibits inhibitory control over later processing, as opposed to early sensory processing, by providing source-localization data in a cross-modal attention task.
This paper seems very strong, particularly given that the follow-up MEG study both (a) clarifies the task design and separates the effect of distractor stimuli into other experimental blocks, and (b) provides source-localization data to more concretely address whether alpha inhibition is occurring at or after the level of sensory processing, and (c) replicates most of the EEG study's key findings.
There are some points that would be helpful to address to bolster the paper. First, the introduction would benefit from a somewhat deeper review of the literature, not just reviewing when the effects of alpha seem to occur, but also addressing how the effect can change depending on task and stimulus design (see review by Morrow, Elias & Samaha (2023). Additionally, the discussion could benefit from more cautionary language around the revision of the alpha inhibition account. For example, it would be helpful to address some of the possible discrepancies between alpha and SSEP measures in terms of temporal specificity, SNR, etc. (see Peylo, Hilla, & Sauseng, 2021). The authors do a good job speculating as to why they found differing results from previous cross-modal attention studies, but I'm also curious whether the authors think that alpha inhibition/modulation of sensory signals would have been different had the distractors been within the same modality or whether the cues indicated target location, rather than just modality, as has been the case in so much prior work?
Overall, the analyses and discussion are quite comprehensive, and I believe this paper to be an excellent contribution to the alpha-inhibition literature.
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Author response:
Public Reviews:
Reviewer #1 (Public review):
In this paper by Brickwedde et al., the authors observe an increase in posterior alpha when anticipating auditory as opposed to visual targets. The authors also observe an enhancement in both visual and auditory steady-state sensory evoked potentials in anticipation of auditory targets, in correlation with enhanced occipital alpha. The authors conclude that alpha does not reflect inhibition of early sensory processing, but rather orchestrates signal transmission to later stages of the sensory processing stream. However, there are several major concerns that need to be addressed in order to draw this conclusion.
First, I am not convinced that the frequency tagging method and the associated analyses are adequate for dissociating visual vs auditory steady-state sensory evoked …
Author response:
Public Reviews:
Reviewer #1 (Public review):
In this paper by Brickwedde et al., the authors observe an increase in posterior alpha when anticipating auditory as opposed to visual targets. The authors also observe an enhancement in both visual and auditory steady-state sensory evoked potentials in anticipation of auditory targets, in correlation with enhanced occipital alpha. The authors conclude that alpha does not reflect inhibition of early sensory processing, but rather orchestrates signal transmission to later stages of the sensory processing stream. However, there are several major concerns that need to be addressed in order to draw this conclusion.
First, I am not convinced that the frequency tagging method and the associated analyses are adequate for dissociating visual vs auditory steady-state sensory evoked potentials.
Second, if the authors want to propose a general revision for the function of alpha, it would be important to show that alpha effects in the visual cortex for visual perception are analogous to alpha effects in the auditory cortex for auditory perception.
Third, the authors propose an alternative function for alpha - that alpha orchestrates signal transmission to later stages of the sensory processing stream. However, the supporting evidence for this alternative function is lacking. I will elaborate on these major concerns below.
(1) Potential bleed-over across frequencies in the spectral domain is a major concern for all of the results in this paper. The fact that alpha power, 36Hz and 40Hz frequency-tagged amplitude and 4Hz intermodulation frequency power is generally correlated with one another amplifies this concern. The authors are attaching specific meaning to each of these frequencies, but perhaps there is simply a broadband increase in neural activity when anticipating an auditory target compared to a visual target?
We appreciate the reviewer’s insightful comment regarding the potential bleed-over across frequencies in the spectral domain. We fully acknowledge that the trade-off between temporal and frequency resolution is a challenge, particularly given the proximity of the frequencies we are examining.
To address this concern, we performed additional analyses to investigate whether there is indeed a broadband increase in neural activity when anticipating an auditory target as compared to a visual target, as opposed to distinct frequency-specific effects. Our results show that the bleed-over between frequencies is minimal and does not significantly affect our findings. Specifically, we repeated the analyses using the same filter and processing steps for the 44 Hz frequency. At this frequency, we did not observe any significant differences between conditions.
These findings suggest that the effects we report are indeed specific to the 40 Hz frequency band and not due to a general broadband increase in neural activity. We hope this addresses the reviewer’s concern and strengthens the validity of our frequency-specific results.
Author response image 1.
Illustration of bleeding over effects over a span of 4 Hz. A, 40 Hz frequency-tagging data over the significant cluster differing between when expecting an auditory versus a visual target (identical to Fig. 9 in the manuscript). B, 44 Hz signal over the same cluster chosen for A. The analysis was identical with the analysis performed in A, apart from the frequency for the band-pass filter.
We do, however, not specifically argue against the possibility of a broadband increase when anticipating an auditory compared to a visual target. But even a broadband-increase would directly contradict the alpha inhibition hypothesis, which poses that an increase in alpha completely disengages the whole cortex. We will clarify this point in the revised manuscript.
(2) Moreover, 36Hz visual and 40Hz auditory signals are expected to be filtered in the neocortex. Applying standard filters and Hilbert transform to estimate sensory evoked potentials appears to rely on huge assumptions that are not fully substantiated in this paper. In Figure 4, 36Hz "visual" and 40Hz "auditory" signals seem largely indistinguishable from one another, suggesting that the analysis failed to fully demix these signals.
We appreciate the reviewer’s insightful concern regarding the filtering and demixing of the 36 Hz visual and 40 Hz auditory signals, and we share the same reservations about the reliance on standard filters and the Hilbert transform method.
To address this, we would like to draw attention to Author response image 1, which demonstrates that a 4 Hz difference is sufficient to effectively demix the signals using our chosen filtering and Hilbert transform approach. We believe that the reason the 36 Hz visual and 40 Hz auditory signals show similar topographies lies not in incomplete demixing but rather in the possibility that this condition difference reflects sensory integration, rather than signal contamination.
This interpretation is further supported by our findings with the intermodulation frequency at 4 Hz, which also suggests cross-modal integration. Furthermore, source localization analysis revealed that the strongest condition differences were observed in the precuneus, an area frequently associated with sensory integration processes. We will expand on this in the discussion section to better clarify this point.
(3) The asymmetric results in the visual and auditory modalities preclude a modality-general conclusion about the function of alpha. However, much of the language seems to generalize across sensory modalities (e.g., use of the term 'sensory' rather than 'visual').
We thank the reviewer for pointing this out and agree that in some cases we have not made a good enough distinction between visual and sensory. We will make sure, that when using ‘sensory’, we either describe overall theories, which are not visual-exclusive or refer to the possibility of a broad sensory increase. However, when directly discussing our results and the interpretation thereof, we will now use ‘visual’ in the revised manuscript.
(4) In this vein, some of the conclusions would be far more convincing if there was at least a trend towards symmetry in source-localized analyses of MEG signals. For example, how does alpha power in the primary auditory cortex (A1) compare when anticipating auditory vs visual target? What do the frequency-tagged visual and auditory responses look like when just looking at the primary visual cortex (V1) or A1?
We thank the reviewer for this important suggestion and have added a virtual channel analysis. We were however, not interested in alpha power in primary auditory cortex, as we were specifically interested in the posterior alpha, which is usually increased when expecting an auditory compared to a visual target (and used to be interpreted as a blanket inhibition of the visual cortex). We will improve upon the clarity concerning this point in the manuscript.
We have however, followed the reviewer’s suggestion of a virtual channel analysis, showing that the condition differences are not observable in primary visual cortex for the 36 Hz visual signal and in primary auditory cortex for the 40 Hz auditory signal. Our data clearly shows that there is an alpha condition difference in V1, while there no condition difference for 36 Hz in V1 and for 40 Hz in Heschl’s Gyrus (see Author response image 2).
Author response image 2.
Virtual channels for V1 and Helschl’s gyrus. A, alpha power for the virtual channel created in V1 (Calcerine_L and Calcerine_R from AAL atlas; Tzourio-Mazoyer et al., 2002, NeuroImage). A cluster permutation analysis over time (between -2 and 0) revealed a significant condition difference between ~ -2 and -1.7 s (p = 0.0449). B, 36 Hz frequency-tagging signal for the virtual channel created in V1 (equivalent to the procedure in A). The same cluster permutation as performed in A revealed no significant condition differences. C, 40 Hz frequency-tagging signal for the virtual channel created in Heschl’s gryrus (Heschl_L and Heschl_R from AAL atlas; Tzourio-Mazoyer et al., 2002, NeuroImage). The same cluster permutation as performed in A revealed no significant condition differences.
(5) Blinking would have a huge impact on the subject's ability to ignore the visual distractor. The best thing to do would be to exclude from analysis all trials where the subjects blinked during the cue-to-target interval. The authors mention that in the MEG experiment, "To remove blinks, trials with very large eye-movements (> 10 degrees of visual angle) were removed from the data (See supplement Fig. 5)." This sentence needs to be clarified since eye-movements cannot be measured during blinking. In addition, it seems possible to remove putative blink trials from EEG experiments as well, since blinks can be detected in the EEG signals.
We thank the reviewer for mentioning that we were making this point confusing. From the MEG-data, we removed eyeblinks using ICA. Alone for the supplementary Fig. 5 analysis, we used the eye-tracking data to confirm that participants were in fact fixating the centre of the screen. For this analysis, we removed trials with blinks (which can be seen in the eye-tracker as huge amplitude movements or as large eye-movements in degrees of visual angle; see Author response image 3 below to show a blink in the MEG data and the according eye-tracker data in degrees of visual angle). We will clarify this in the methods section.
As for the concern closed eyes to ignore visual distractors, in both experiments we can observe highly significant distractor cost in accuracy for visual distractors, which we hope will convince the reviewer that our visual distractors were working as intended.
Author response image 3.
Illustration of eye-tracker data for a trial without and a trial with a blink. All data points recorded during this trial are plottet. A, ICA component 1, which reflects blinks and its according data trace in a trial. No blink is visible. B, eye-tracker data transformed into degrees of visual angle for the trial depicted in A. C, ICA component 1, which reflects blinks and its according data trace in a trial. A clear blink is visible. D, eye-tracker data transformed into degrees of visual angle for the trial depicted in C.
(6) It would be interesting to examine the neutral cue trials in this task. For example, comparing auditory vs visual vs neutral cue conditions would be indicative of whether alpha was actively recruited or actively suppressed. In addition, comparing spectral activity during cue-to-target period on neutral-cue auditory correct vs incorrect trials should mimic the comparison of auditory-cue vs visual-cue trials. Likewise, neutral-cue visual correct vs incorrect trials should mimic the attention-related differences in visual-cue vs auditory-cue trials.
We thank the reviewer for this suggestion. We have analysed the neutral cue trials in the EEG dataset (see suppl. Fig. 1) and will expand this figure to show all conditions. There were no significant differences to auditory or visual cues, but descriptively alpha power was higher for neutral cues compared to visual cues and lower for neutral cues compared to auditory cues. While this may suggest that for visual trials alpha is actively suppressed and for auditory trials actively recruited, we do not feel comfortable to make this claim, as the neutral condition may not reflect a completely neutral state. The neutral task can still be difficult, especially because of the uncertainty of the target modality.
As for the analysis of incorrect versus correct trials, we love the idea, but unfortunately the accuracy rate was quite high so that the number of incorrect trials would not be sufficient to perform a reliable analysis.
(7) In the abstract, the authors state that "This implies that alpha modulation does not solely regulate 'gain control' in early sensory areas but rather orchestrates signal transmission to later stages of the processing stream." However, I don't see any supporting evidence for the latter claim, that alpha orchestrates signal transmission to later stages of the processing stream. If the authors are claiming an alternative function to alpha, this claim should be strongly substantiated.
We thank the reviewer for pointing out, that we have not sufficiently explained our case. The first point refers to gain control akin to the alpha inhibition hypothesis, which claims that increases in alpha disengage a whole cortical area. Since we have confirmed the alpha increase in our data to originate from primary visual cortex through source analysis, this should lead to decreased visual processing. The increase in 36 Hz visual processing therefore directly contradicts the alpha inhibition hypothesis. We propose an alternative explanation for the functionality of alpha activity in this task. Through pulsed inhibition, information packages of relevant visual information could be transmitted down the processing stream, thereby enhancing relevant visual signal transmission. We believe the fact that the enhanced visual 36 Hz signal we found correlated with visual alpha power on a trial-by-trial basis, and did not originate from primary visual cortex, but from areas known for sensory integration supports our claim.
We will make this point clearer in our revised manuscript.
Reviewer #2 (Public review):
Brickwedde et al. investigate the role of alpha oscillations in allocating intermodal attention. A first EEG study is followed up with a MEG study that largely replicates the pattern of results (with small to be expected differences). They conclude that a brief increase in the amplitude of auditory and visual stimulus-driven continuous (steady-state) brain responses prior to the presentation of an auditory - but not visual - target speaks to the modulating role of alpha that leads them to revise a prevalent model of gating-by-inhibition.
Overall, this is an interesting study on a timely question, conducted with methods and analysis that are state-of-the-art. I am particularly impressed by the author's decision to replicate the earlier EEG experiment in MEG following the reviewer's comments on the original submission. Evidently, great care was taken to accommodate the reviewer's suggestions.
We thank the reviewer for the positive feedback and expression of interest in the topic of our manuscript.
Nevertheless, I am struggling with the report for two main reasons: It is difficult to follow the rationale of the study, due to structural issues with the narrative and missing information or justifications for design and analysis decisions, and I am not convinced that the evidence is strong, or even relevant enough for revising the mentioned alpha inhibition theory. Both points are detailed further below.
We thank the reviewer for raising this important point. We will revise our introduction and results in line with the reviewer’s suggestions, hoping that our rationale will then be easier to follow and that our evidence will be more convincing.
Strength/relevance of evidence for model revision: The main argument rests on 1) a rather sustained alpha effect following the modality cue, 2) a rather transient effect on steady-state responses just before the expected presentation of a stimulus, and 3) a correlation between those two. Wouldn't the authors expect a sustained effect on sensory processing, as measured by steady-state amplitude irrespective of which of the scenarios described in Figure 1A (original vs revised alpha inhibition theory) applies? Also, doesn't this speak to the role of expectation effects due to consistent stimulus timing? An alternative explanation for the results may look like this: Modality-general increased steady-state responses prior to the expected audio stimulus onset are due to increased attention/vigilance. This effect may be exclusive (or more pronounced) in the attend-audio condition due to higher precision in temporal processing in the auditory sense or, vice versa, too smeared in time due to the inferior temporal resolution of visual processing for the attend-vision condition to be picked up consistently. As expectation effects will build up over the course of the experiment, i.e., while the participant is learning about the consistent stimulus timing, the correlation with alpha power may then be explained by a similar but potentially unrelated increase in alpha power over time.
We thank the reviewer for raising these insightful questions and suggestions.
It is true that our argument rests on a rather sustained alpha effect and a rather transient effect on steady-state responses and a correlation between the two. However, this connection would not be expected under the alpha inhibition hypothesis, which states that alpha activity would inhibit a whole cortical area (when irrelevant to the task), exerting “gain control”. This notion directly contradicts our results of the “irrelevant” visual information a) being transmitted at all and b) increasing.
However, it has been shown on many occasions that alpha activity exerts pulsed inhibition, so we proposed an alternative theory of an involvement in signal transmission. In this case, the cyclic inhibition would serve as an ordering system, which only allows for high-priority information to pass, resulting in higher signa-to-noise. We do not make a claim about how fast or when these signals are transmitted in relation to alpha power. For instance, it could be that alpha power increases as a preparatory state even before signal is actually transmitted. Zhigalov (2020 Hum. Brain M.) has shown that in V1, frequency-tagging responses were up-and down regulated with attention – independent of alpha activity.
But we do believe that the fact that visual alpha power correlates on a trial-by-trial level with visual 36 Hz frequency-tagging increases and (a relationship which has not been found in V1, see Zhigalov 2020, Hum. Brain Mapp.) suggest a strong connection. Furthermore, the fact that the alpha modulation originates from early visual areas and occurs prior to any frequency-tagging changes, while the increase in frequency-tagging can be observed in areas which are later in the processing stream (such as the precuneus) is strongly indicative for an involvement of alpha power in the transmission of this signal. We cannot fully exclude alternative accounts and mechanisms which effect both alpha power and frequency-tagging responses.
We do believe that the alternative account described by the reviewer does not contradict our theory, as we do believe that the alpha power modulation may reflect an expectation effect (and the idea that it could be related to the resolution of auditory versus visual processing is very interesting!). It is also possible that this expectation is, as the reviewer suggests, related to attention/vigilance and might result in a modality-general signal increase. And indeed, we can observe an increase in the frequency-tagging response in sensory integration areas. Accordingly, we believe that the alternative explanation provided by the reviewer contradicts the alpha inhibition hypothesis, but not necessarily our alternative theory.
We will revise the discussion, which we hope will make our case stronger and easier to follow. Additionally, we will mention the possibility for alternative explanations as well as the possibility, that alpha networks fulfil different roles in different locations/task environments.
Structural issues with the narrative and missing information: Here, I am mostly concerned with how this makes the research difficult to access for the reader. I list the major points below:
In the introduction the authors pit the original idea about alpha's role in gating against some recent contradictory results. If it's the aim of the study to provide evidence for either/or, predictions for the results from each perspective are missing. Also, it remains unclear how this relates to the distinction between original vs revised alpha inhibition theory (Fig. 1A). Relatedly if this revision is an outcome rather than a postulation for this study, it shouldn't be featured in the first figure.
We agree with the reviewer that we have not sufficiently clarified our goal as well as how different functionalities of alpha oscillations would lead to different outcomes. We will revise the introduction and restructure the results and hope that it will be easier to follow.
The analysis of the intermodulation frequency makes a surprise entrance at the end of the Results section without an introduction as to its relevance for the study. This is provided only in the discussion, but with reference to multisensory integration, whereas the main focus of the study is focussed attention on one sense. (Relatedly, the reference to "theta oscillations" in this sections seems unclear without a reference to the overlapping frequency range, and potentially more explanation.) Overall, if there's no immediate relevance to this analysis, I would suggest removing it.
We thank the reviewer for pointing this out and will add information about this frequency to the introduction part. We believe that the intermodulation frequency analysis is important, as it potentially supports the notion that condition differences in the visual-frequency tagging response are related to downstream processing rather than overall visual information processing in V1. We would therefore prefer to leave this analysis in the manuscript.
Reviewer #3 (Public review):
Brickwedde et al. attempt to clarify the role of alpha in sensory gain modulation by exploring the relationship between attention-related changes in alpha and attention-related changes in sensory-evoked responses, which surprisingly few studies have examined given the prevalence of the alpha inhibition hypothesis. The authors use robust methods and provide novel evidence that alpha likely exhibits inhibitory control over later processing, as opposed to early sensory processing, by providing source-localization data in a cross-modal attention task.
This paper seems very strong, particularly given that the follow-up MEG study both (a) clarifies the task design and separates the effect of distractor stimuli into other experimental blocks, and (b) provides source-localization data to more concretely address whether alpha inhibition is occurring at or after the level of sensory processing, and (c) replicates most of the EEG study's key findings.
We are very grateful to the reviewer for their positive feedback and evaluation of our work.
There are some points that would be helpful to address to bolster the paper. First, the introduction would benefit from a somewhat deeper review of the literature, not just reviewing when the effects of alpha seem to occur, but also addressing how the effect can change depending on task and stimulus design (see review by Morrow, Elias & Samaha (2023).
We thank the reviewer for this suggestion and agree. We will add a paragraph to the introduction which refers to missing correlation studies and the impact of task design.
Additionally, the discussion could benefit from more cautionary language around the revision of the alpha inhibition account. For example, it would be helpful to address some of the possible discrepancies between alpha and SSEP measures in terms of temporal specificity, SNR, etc. (see Peylo, Hilla, & Sauseng, 2021). The authors do a good job speculating as to why they found differing results from previous cross-modal attention studies, but I'm also curious whether the authors think that alpha inhibition/modulation of sensory signals would have been different had the distractors been within the same modality or whether the cues indicated target location, rather than just modality, as has been the case in so much prior work?
We thank the reviewer for suggesting these interesting discussion points and will include a paragraph in our discussion which goes deeper into these topics.
Overall, the analyses and discussion are quite comprehensive, and I believe this paper to be an excellent contribution to the alpha-inhibition literature.
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