The length of the thalamo-cortical white matter fibers brings insight into sex differences in sleep spindle frequency
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Evaluation Summary:
This valuable paper addresses an important question about the neuroanatomical markers of individual and sex differences in sleep spindle frequency. The authors report associations between an anatomical marker - the length of the white matter fibre bundles underlying the thalamocortical loop and sleep spindle frequency, and highlight that the length of the white matter projections from the thalamus to the frontal cortex mediates sex differences in the sleep spindle frequency. This work advances the field of sleep and brain research by showing for the first time the association between the anatomy of a specific brain network and specific functional characteristics.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Abstract
Sleep spindles (SS) are crucial to brain functions like memory and learning. SS characteristics result from the propagation of nerve impulses along white matter (WM) projections underlying an intricate loop between the thalamus and the cortex. SS amplitude and density have been associated with WM diffusion microarchitecture but physiological mechanisms underlying individual and sex-related variations in SS frequency are unknown. Here, we tested a model of traveling signals along the thalamo-cortico-thalamic projections to explain individual differences in spindle frequency. We predicted the presence of a relationship between the length of the thalamo-cortical WM bundles and a specific characteristic of this functional network, SS frequency.
Thirty young participants underwent a polysomnographic recording and a 3T MRI including a diffusion sequence. The length of WM fiber bundles between the thalamus and the frontal cortex was derived from probabilistic tractography computed through constrained spherical deconvolution.
Longer WM fiber bundles between the thalamus and specific regions of the frontal cortex (rostral middle frontal gyrus and anterior and middle part of the superior frontal gyrus) were associated with slower SS frequency. Moreover, the length of these WM fiber bundles statistically mediated the sex-related differences in SS frequency.
By providing a neuroanatomical marker of individual and sex-related differences in SS frequency, this study is the first to highlight the association between the anatomy of a specific brain network and a specific functional characteristic of this network, the frequency of oscillations produced during sleep.
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Evaluation Summary:
This valuable paper addresses an important question about the neuroanatomical markers of individual and sex differences in sleep spindle frequency. The authors report associations between an anatomical marker - the length of the white matter fibre bundles underlying the thalamocortical loop and sleep spindle frequency, and highlight that the length of the white matter projections from the thalamus to the frontal cortex mediates sex differences in the sleep spindle frequency. This work advances the field of sleep and brain research by showing for the first time the association between the anatomy of a specific brain network and specific functional characteristics.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested …
Evaluation Summary:
This valuable paper addresses an important question about the neuroanatomical markers of individual and sex differences in sleep spindle frequency. The authors report associations between an anatomical marker - the length of the white matter fibre bundles underlying the thalamocortical loop and sleep spindle frequency, and highlight that the length of the white matter projections from the thalamus to the frontal cortex mediates sex differences in the sleep spindle frequency. This work advances the field of sleep and brain research by showing for the first time the association between the anatomy of a specific brain network and specific functional characteristics.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
The authors tested, in 30 subjects, a model of traveling signals along the thalamo-cortico-thalamic projections to explain individual differences in spindle frequency. As predicted, they showed the presence of a relationship between the length of the thalamocortical white matter bundles and sleep spindle frequency (a specific characteristic of this functional network), and further showed that this neuroanatomical marker mediated the sex-related differences in sleep spindle frequency.
This paper has several strengths, both methodologically and conceptually. The authors leverage the use of polysomnographic/EEG overnight recordings and diffusion MRI data for their analysis, providing a unique dataset in a group of men and women. The focus on understanding the well-established sex difference in sleep spindles is …
Reviewer #1 (Public Review):
The authors tested, in 30 subjects, a model of traveling signals along the thalamo-cortico-thalamic projections to explain individual differences in spindle frequency. As predicted, they showed the presence of a relationship between the length of the thalamocortical white matter bundles and sleep spindle frequency (a specific characteristic of this functional network), and further showed that this neuroanatomical marker mediated the sex-related differences in sleep spindle frequency.
This paper has several strengths, both methodologically and conceptually. The authors leverage the use of polysomnographic/EEG overnight recordings and diffusion MRI data for their analysis, providing a unique dataset in a group of men and women. The focus on understanding the well-established sex difference in sleep spindles is a significant strength and advances knowledge and understanding of neuroanatomical underpinnings for this sex difference. Interestingly, the authors did not find a relationship between this neuroanatomical measure and sleep spindle amplitude, which deserves further comment. The current work can be used as a foundation for future work, for example, examining the relationship between neuroanatomical white matter fiber bundle length between thalamus and frontal cortex and functional sleep spindle outcomes, such as memory consolidation, as well as exploring age-related changes/differences in these measures.
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Reviewer #2 (Public Review):
The authors aimed to explain sleep spindle frequency, and specifically a reason for sex differences in spindle frequency. Although the authors have highlighted other effects explaining these differences before (e.g., Carrier et al., 2017), here they have a very logical argument for why white matter fiber bundle length should inversely predict frequency that relies on the amount of time it takes to travel from cortical to thalamic areas. I believe the authors accomplish this goal, and convincingly show that fiber bundle length mediates this relationship. However, I believe the data could be presented more clearly and the statistics could be possibly simplified/improved.
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