Microstructural asymmetries of the planum temporale predict functional lateralization of auditory-language processing

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    The authors studied the relationship between structural and functional lateralization in the planum temporale region of the brain, whilst also considering the morphological presentation of a single or duplicated Heschl's gyrus. The analyses are convincing due to a large sample size, inter-rater reliability, and corrections for multiple comparisons. The associations in this valuable work might serve as a reference for future targeted-studies on brain lateralization.

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Abstract

Structural hemispheric asymmetry has long been assumed to guide functional asymmetry of the human brain, but empirical evidence for this compelling hypothesis remains scarce. Recently, it has been suggested that microstructural asymmetries may be more relevant to functional asymmetries than macrostructural asymmetries. To investigate the link between microstructure and function, we analyzed multimodal MRI data in 907 participants. We quantified structural and functional asymmetries of the planum temporale (PT), a cortical area crucial for auditory-language processing. We found associations of functional PT asymmetries and several microstructural asymmetries, such as intracortical myelin content, neurite density, and neurite orientation dispersion. The PT microstructure per se also showed hemispheric-specific coupling with PT functional activity. All these functional-structural associations are highly specific to within-PT functional activity during auditory-language processing. These results suggest that structural asymmetry guides functional lateralization of the same brain area and highlight a critical role of microstructural PT asymmetries in auditory-language processing.

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  1. eLife assessment

    The authors studied the relationship between structural and functional lateralization in the planum temporale region of the brain, whilst also considering the morphological presentation of a single or duplicated Heschl's gyrus. The analyses are convincing due to a large sample size, inter-rater reliability, and corrections for multiple comparisons. The associations in this valuable work might serve as a reference for future targeted-studies on brain lateralization.

  2. Reviewer #1 (Public Review):

    Summary:

    Qin and colleagues analysed data from the Human Connectome Project on four right-handed subgroups with different gyrification patterns in Heschl's gyrus. Based on these groups, the authors highlight the structure-function relationship of planum temporale asymmetry in lateralised language processing at the group level and next at the individual level. In particular, the authors propose that especially microstructural asymmetries are related to functional auditory language asymmetries in the planum temporale.

    Strengths:

    The study is interesting because of an ongoing and long-standing debate about the relationship between structural and functional brain asymmetries, and in particular whether structural brain asymmetries can be seen as markers of functional language brain lateralisation.

    In this debate, the relationship between Heschl's gyrus asymmetry and planum temporale asymmetry is rare and therefore valuable here. A large sample size and inter-rater reliability support the findings.

    Weaknesses:

    In this case of multiple brain measures, it would be important to provide the reader with some sort of effect size (e.g. Cohen's d) to help interpret the results. In addition, the authors highlight the microstructural results in spite of the macrostructural results. However, the macrostructural surface results are also strong. I would suggest either reducing the emphasis on micro vs macrostructural results or adding information to justify the microstructural importance.

  3. Reviewer #2 (Public Review):

    Summary:

    The authors assessed the link between structural and functional lateralization in area PT, one of the brain areas that is known to exhibit strong structural lateralization, and which is known to be implicated in speech processing. Importantly, they included the sulcal configuration of Heschl's gyrus (HG), presenting either as a single or duplicated HG, in their analysis. They found several significant associations between microstructural indices and task-based functional lateralization, some of which depended on the sulcal configuration.

    Strengths:

    A clear strength is the large sample size (n=907), an openly available database, and the fact that HG morphology was manually classified in each individual. This allows for robust statistical testing of the effects across morphological categories, which is not often seen in the literature.

    Weaknesses:

    - Unfortunately, no left-handers were included in the study. It would have been a valuable addition to the literature, to study the effect of handedness on the observed associations, as many previous studies on this topic were not adequately powered. The fact that only right-handers were studied should be pointed out clearly in the introduction or even the abstract.

    - The tasks to quantify functional lateralization were not specifically designed to pick up lateralization. In the interest of the sample size, it is understandable that the authors used the available HCP-task-battery results, however, it would have been feasible to access another dataset for validation. A targeted subset of results, concerning for example the relationship between sulcal morphology and task-based functional lateralization, could be re-assessed using other open-access fMRI datasets.

    - The study is mainly descriptive and the general discussion of the findings in the larger context of brain lateralization comes a bit short. For example, are the observed effects in line with what we know from other 'language-relevant' areas? What could be the putative mechanisms that give rise to functional lateralization based on the microstructural markers observed? And which mechanisms might be underlying the formation of a duplicated HG?