Modulation of alpha oscillations by attention is predicted by hemispheric asymmetry of subcortical regions

Reviewer #1 (Public Review):

Summary:
The authors re-analysed the data of a previous study in order to investigate the relation between asymmetries of subcortical brain structures and the hemispheric lateralization of alpha oscillations during visual spatial attention. The visual spatial attention task crossed the factors of target load and distractor salience, which made it possible to also test the specificity of the relation of subcortical asymmetries to lateralized alpha oscillations for specific attentional load conditions. Asymmetry of globus pallidus, caudate nucleus, and thalamus explained inter-individual differences in attentional alpha modulation in the left versus right hemisphere. Multivariate regression analysis revealed that the explanatory potential of these regions' asymmetries varies as a function of target load and distractor salience.

Strengths:
The analysis pipeline is straightforward and follows in large parts what the authors have previously used in Mazzetti et al (2019). The authors use an interesting study design, which allows for testing of effects specific to different dimensions of attentional load (target load/distractor salience). The results are largely convincing and in part replicate what has previously been shown. The article is well-written and easy to follow.

Weaknesses:
While the article is interesting to read for researchers studying alpha oscillations in spatial attention, I am somewhat sceptical about whether this article is of high interest to a broader readership. Although I read the article with interest, the conceptual advance made here can be considered mostly incremental. As the authors describe, the present study's main advance is that it does not include reward associations (as in previous work) and includes different levels of attentional load. While these design features and the obtained results indeed improve our general understanding of how asymmetries of subcortical structures relate to lateralized alpha oscillations, the conceptual advance is somewhat limited.

While the analysis of the relation of individual subcortical structures to alpha lateralization in different attentional load conditions is interesting, I am not convinced that the present analysis is suited to draw strong conclusions about the subcortical regions' specificity. For example, the Thalamus (Fig. 5) shows a significant negative beta estimate only in one condition (low-load target, non-salient distractor) but not in the other conditions. However, the actual specificity of the relation of thalamus asymmetry to lateralized alpha oscillations would require that the beta estimate for this one condition is significantly higher than the beta estimates for the other three conditions, which has not been tested as far as I understand.

Reviewer #2 (Public Review):

Summary:
In this study, Ghafari et al. explored the correlation between hemispheric asymmetry in the volume of various subcortical regions and lateralization of posterior alpha-band oscillations in a spatial attention task with varying cognitive demands. To this end, they combined structural MRI and task MEG to investigate the relationship between hemispheric differences in the volume of basal ganglia, thalamus, hippocampus, and amygdala and hemisphere-specific modulation of alpha-band power. The authors report that differences in the thalamus, caudate nucleus, and globus pallidus volume are linked to the attention-related changes in alpha band oscillations with differential correlations for different regions in different conditions of the design (depending on the salience of the distractor and/or the target).

Strengths:
The manuscript contributes to filling an important gap in current research on attention allocation which commonly focuses exclusively on cortical structures. Because it is not possible to reliably measure subcortical activity with non-invasive electrophysiological methods, they correlate volumetric measurements of the relevant subcortical regions with cortical measurements of alpha band power. Specifically, they build on their own previous finding showing a correlation between hemispheric asymmetry of basal ganglia volumes and alpha lateralization by assessing a task without an explicit reward component. Furthermore, the authors use differences in saliency and perceptual load to disentangle the individual contributions of the subcortical regions.

Weaknesses:
The theoretical bases of several aspects of the design and analyses remain unclear. Specifically, we missed statements in the introduction about why it is reasonable, from a theoretical perspective, to expect:
(i) a link between volumetric measurements and task activity;
(ii) a specific link with hemispheric asymmetry in subcortical structures (While focusing on hemispheric lateralization might circumvent the problem of differences in head size, it would be better to justify this focus theoretically, which requires for example a short review of evidence showing ipsilateral vs contralateral connections between the relevant subcortical and cortical structures);
(iii) effects not only in basal ganglia and thalamus, but also hippocampus and amygdala (a justification of selection of all ROIs);
(iv) effects that depend on distractor versus target salience (a rationale for the specific two-factor design is missing);
(v) effects in the absence of reward (why it is important to show that the effect seen previously in a task with reward is seen also in a task without reward);
(vi) effects on rapid frequency tagging.

Second, the results are not fully reported. The model space and the results from the model comparison are omitted. Behavioral data and rapid frequency tagging results are not shown. Without having access to the data or the results of the analyses, the reader cannot evaluate whether the null effect corresponds to the absence of evidence or (as claimed in the discussion) evidence of absence.

Third, it remains unclear whether the MMS is the best approach to analyzing effects as a function of target and distractor salience. To address the question of whether the effects of subcortical volumes on alpha lateralization vary with task demands (which we assume is the primary research question of interest, given the factorial design), we would like to evaluate some sort of omnibus interaction effect, e.g., by having target and distractor saliency interact with the subcortical volume factors to predict alpha lateralization. Without such analyses, the results are very hard to interpret. What are the implications of finding the differential effects of the different volumes for the different task conditions without directly assessing the effect of the task manipulation? Moreover, the report would benefit from a further breakdown of the effects into simple effects on unattended and attended alpha, to evaluate whether effects as a function of distractor (vs target) salience are indeed accompanied by effects on unattended (vs attended) alpha.

The fourth concern is that the discussion section is not quite ready to help the reader appreciate the implications of key aspects of the findings. What are the implications for our understanding of the roles of different subcortical structures in the various psychological component processes of spatial attention? Why does the volumetric asymmetry of different subcortical structures have diametrically opposite effects on alpha lateralization? Instead, the discussion section highlights that the different subcortical structures are connected in circuits: "Globus pallidus also has wide projections to the thalamus and can thereby impact the dorsal attentional networks by modulating prefrontal activities." If this is true, then why does the effect of the GP dissociate from that of the thalamus? Also, what is it about the current behavioural paradigm that makes the behavioral readout insensitive to variation in subcortical volume (or alpha lateralization?)?