Functional specialization within the inferior parietal lobes across cognitive domains
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Summary: Overall the reviewers felt that the manuscript had a fair amount of promise but raised some issues about the specific tasks used and some details of the analysis. One reviewer in particular felt that the manuscript should be reworked around the functional connectivity results, which would strengthen the manuscript. I tend to agree with this assessment, particularly as concerns the lateralization framing which is not very well explored by these tasks.
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Abstract
The inferior parietal lobe (IPL) is a key neural substrate underlying diverse mental processes, from basic attention to language and social cognition, that define human interactions. Its putative domain-global role appears to tie into poorly understood differences between cognitive domains in both hemispheres. Across attentional, semantic, and social cognitive tasks, our study explored functional specialization within the IPL. The task specificity of IPL subregion activity was substantiated by distinct predictive signatures identified by multivariate pattern-learning algorithms. Moreover, the left and right IPL exerted domain-specific modulation of effective connectivity among their subregions. Task-evoked functional interactions of the anterior and posterior IPL subregions involved recruitment of distributed cortical partners. While anterior IPL subregions were engaged in strongly lateralized coupling links, both posterior subregions showed more symmetric coupling patterns across hemispheres. Our collective results shed light on how under-appreciated functional specialization in the IPL supports some of the most distinctive human mental capacities.
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Reviewer #2:
In this paper, Numssen and co-workers focus on the functional differences between hemispheres to investigate the "domain-role" of IPL in different types of mental processes. They employ multivariate pattern-learning algorithms to assess the specific involvement of two IPL subregions in three tasks: an attentional task (Attention), a semantic task (Semantics) and a social task (Social cognition). The authors describe how, when involved in different tasks, each right and left IPL subregion recruits a different pattern of connected areas.
The employed tasks are "well established", and the results confirm previous findings. However, the novelty of the paper lies in the fact that the authors use these results as a tool to observe IPL activity when involved in different domains of cognition.
The methodology is sound, well …
Reviewer #2:
In this paper, Numssen and co-workers focus on the functional differences between hemispheres to investigate the "domain-role" of IPL in different types of mental processes. They employ multivariate pattern-learning algorithms to assess the specific involvement of two IPL subregions in three tasks: an attentional task (Attention), a semantic task (Semantics) and a social task (Social cognition). The authors describe how, when involved in different tasks, each right and left IPL subregion recruits a different pattern of connected areas.
The employed tasks are "well established", and the results confirm previous findings. However, the novelty of the paper lies in the fact that the authors use these results as a tool to observe IPL activity when involved in different domains of cognition.
The methodology is sound, well explained in the method section, the analyses are appropriate, and the results clear and well explained in the text and in graphic format.
However, a solid experimental design is required to provide strong results. To the reviewer's view, the employed design can provide interesting results about functional connectivity, but not about the functional role of IPL in the investigated functions.
I think the study would be correct and much more interesting if only based on functional connectivity data. Note that rewriting the paper accordingly would lead to a thorough discussion about how anatomical circuits are differently recruited based on different cognitive demands and about the variable role of cortical regions in functional tasks. This issue is neglected in the present discussion, and this concept is in disagreement with the main results, suggesting (probably beyond the intention of the authors) that different parts of the right and left IPL are the areas responsible for the studied functions.
Major points:
The 3 chosen tasks explore functions that are widespread in the brain, and are not specifically aimed at investigating IPL. The results (see. e.g. fig 1) confirm this idea, but the authors specifically focus on IPL. This seems a rather arbitrary and not justified choice. If they want to explore the lateralization issue, they should consider the whole set of involved areas or use tasks showing all their maximal activation in IPL.
The authors aims to study lateralization using an attentional task, considering the violation of a prevision (invalid>valid), a linguistic task, looking for an activation related to word identification (word>pseudoword) and a social task, considering correct perspective taking (false belief>true belief), but they do not consider that in all cases a movement (key press) is required. It is well known that IPL is a key area also for creating motor commands and guiding movements. Accordingly, the lateralization bias observed could be due more to the unbalance between effectors while issuing the motor command, than to a different involvement of IPL regions in the specific tasks functions.
Like point 2, the position of keys is also crucial if the authors want to explore lateralization. This is especially important if one considers that IPL plays a major role in spatial attention (e.g. Neglect syndrome). In the Methods, the authors simply say "Button assignments were randomized across subjects and kept identical across sessions", this should be explained in more detail.
The authors show to know well the anatomical complexity of IPL, however their results are referred to two large-multiareal-regions. This seems to the reader at odds with all the descriptions related to fig.2. If they don't find any more subtle distinction within these 2 macro-regions, they should at least discuss this discrepancy.
The part about Task-specific network connectivity is indeed very interesting, I would suggest to the authors to focus exclusively on this part. (Note that the results of this part seems to confirm that only the linguistic task is able to show a clear lateralization).
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Reviewer #1:
The authors have performed a rare feat in the study of the posterior parietal cortex, which is to achieve a functional parcellation of this crucial area on the basis of its response during a diverse set of tasks. The variety of tasks and the analytical approach married to it are very strong and lead to a division that agrees well with data from patients with lesions and studies in homologous areas of non-human primates.
Readers are encouraged to note the analytical approach, with particular regard for the permutation testing that establishes the differences between the tasks in the functional connectivity of the area.
Conceptually, this paper is another strong argument for understanding the broad role of the posterior parietal across tasks and point at the flexibility of its functional response in supporting those roles.
Thi…
Reviewer #1:
The authors have performed a rare feat in the study of the posterior parietal cortex, which is to achieve a functional parcellation of this crucial area on the basis of its response during a diverse set of tasks. The variety of tasks and the analytical approach married to it are very strong and lead to a division that agrees well with data from patients with lesions and studies in homologous areas of non-human primates.
Readers are encouraged to note the analytical approach, with particular regard for the permutation testing that establishes the differences between the tasks in the functional connectivity of the area.
Conceptually, this paper is another strong argument for understanding the broad role of the posterior parietal across tasks and point at the flexibility of its functional response in supporting those roles.
This manuscript lays out a series of fMRI investigations and analyses centered on examining the response of the IPL during three different tasks (attention, semantics, social cognition). The analyses are largely data-driven and examine functional response and connectivity, to make the argument for a functional parcellation of the IPL into at least two distinct subregions. The manuscript is well-written and the analyses well described. There are some concerns about the analyses that dampen enthusiasm slightly and a lack of consideration of the associated literature in non-human primates, but these problems seem imminently correctable.
The analyses begin with a data-driven cluster analysis across an anatomically constrained IPL ROI, searching for cluster solutions that efficiently parcellate IPL on the basis of the response of voxels across the three tasks. This analysis is fine, but does constrain the average activity in the identified clusters to differ across the tasks. That makes the univariate activation in 3b a bit circular and hard to interpret. Either the error bars should be removed and a note added that the univariate activity is purely descriptive or the univariate data should be displayed from a slice of the data that did not contribute to the derivation of the clusters. The strongest version of this analysis would hold out entire participants.
The predictive coding analysis is potentially informative but the details were a bit unclear. In the one versus rest analysis the strongest test would be to build the model on the data from n-1 participants and then test it on the trials of the held-out participant. If this was not done, some justification for not doing it would be in order.
Finally, the authors should also consider integrating some of the non-human primate literature as it only strengthens their case. In the human literature the IPL has proved a tough nut to crack, but the single unit physiology has revealed strong differences in the homologous areas of macaque, some of which directly map onto the division argued for here.
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Summary: Overall the reviewers felt that the manuscript had a fair amount of promise but raised some issues about the specific tasks used and some details of the analysis. One reviewer in particular felt that the manuscript should be reworked around the functional connectivity results, which would strengthen the manuscript. I tend to agree with this assessment, particularly as concerns the lateralization framing which is not very well explored by these tasks.
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