Unique longitudinal contributions of sulcal interruptions to reading acquisition in children

Reviewer #1 (Public review):

Summary:

There is prior literature showing a robust relationship between sulcal interruptions in the posterior occipital temporal sulcus (pOTS) and reading ability. The goals of this study were to extend these findings to children examined longitudinally as they become better readers, and to examine the underlying white matter properties in individuals with and without pOTS sulcal interruptions. To do this, the authors collected longitudinal structural, diffusion, and behavioral data in 51 children (TP1 age 5.5, TP3 age 8.2 years).

First, the authors found that the gyral gap was consistent across time within the subject. This is expected, as they state in the introduction that sulcal patterns are typically established in utero. Next, they found that children with an interrupted pOTS have higher reading scores (across a variety of measures) at timepoint (TP) 3 than children with continuous pOTS, and this was specific to the pOTS, as no associations emerged for the anterior OTS or MFS; this is again expected from prior literature. They then found that the binary presence of this gap, but not anterior OTS or MFS predicted T3 reading performance. Further, they found that a subsample of the lowest readers at TP1 did not have differences in reading score by gyral gap, but that this difference emerged at TP3. Additionally, the gyral gap at TP1 is similar to variance TOWRE 3 reading skills as some behavioral measures at TP1. Examining underlying white matter in a smaller subset of children, the authors found higher MD in children with an interrupted pOTS vs. those with a continuous pOTS, which was contrary to their hypothesis, and higher local connectivity for interrupted, aligning with their hypothesis, but this difference was no longer present when accounting for TP3 reading scores. The authors conclude that structural properties, in this case, the gyral gap, may guide neural plasticity for reading.

Strengths:

This paper has an interesting set of longitudinal data to examine the perhaps changing relationship between sulcal interruptions in the pOTS with reading scores. I commend the authors on data collection and attention to detail in the anatomical analyses.

Weaknesses:

However, my enthusiasm was somewhat dampened after finding numerous prior publications on this very topic and I'm unclear as to how much more this paper adds to the current literature. Would we expect the existence of sulcal interruptions to be aligned with reading skills in older kids but not younger kids? Is the point to see if the interruptions exist prior to reading (but these children are not really prereaders)? What is the alternative- why would these interruptions not exist? After all, this anatomy is determined prenatally. Children who have pOTS interruptions at T1 should also have these interruptions at T3 (and indeed that is what the authors find). So how can this be the mechanism that drives plasticity? The authors also talk about the neuronal recycling hypothesis but their data cannot speak to this because they do not have fMRI data nor does their sample include only prereaders with no reading experience. The conclusions are overall overstated and not supported by the results. I think this paper could add interesting knowledge for the specific subfield of reading and the brain. However, the current state of the results, especially with the inclusion of so many trending results and the comparison of so many different processing pipelines and models, in addition to a conclusion that is not motivated by the work makes it difficult to appreciate the paper.

Reviewer #2 (Public review):

Summary:

This manuscript examined the impact of sulcal morphology on reading development. A very specific feature on the ventral surface of the brain was identified, namely the presence of an interruption in the posterior portion of the left occipitotemporal sulcus (pOTS). Compared to children with a continuous pOTS, children with an interruption at age 5 years had better reading ability at age 8. This was a large effect measured in 43 children. Surprisingly, this morphological feature was a better predictor of reading ability than measures of pre-literacy cognitive skills, such as phonological awareness. The effect was tested and reproduced across several different measures of reading ability. The authors hypothesised that the mechanism underlying this benefit related to greater local connectivity, which confers a computational advantage. This was demonstrated using analysis of diffusion-weighted imaging data in 29 of the children obtained at age 8.

Strengths:

The novelty of the manuscript is threefold: (i) the measure was made in children who were pre-literate (previous work was in older children and adults); (ii) longitudinal brain imaging and behavioural data were analysed; and (iii) diffusion data were analysed to test a hypothesis about the underlying mechanism.

The manuscript is exceptionally well written. The methods are detailed and easily reproduced. The approach is thoughtful and meticulous. All possible alternatives appear to have been considered. Where possible, further analyses have been done to address these alternatives. For example, the testing of the specificity of the sulcal interruption to left pOTS was an important addition. None predicted reading skills.

Weaknesses:

The correlation of the interruption with all kinds of literacy measures and in particular reading comprehension and then PIQ suggest this interruption might confer a more general cognitive advantage rather than specifically a reading one.

It would be interesting to know if the anatomical difference predicts any other cognitive ability or if there might be any cognitive cost (a negative correlation) of this sulcal interruption.
The location of the interruption in the sulcus is quite variable and in some cases, there is more than one interruption. The sample size is probably not big enough to compare these different patterns or to evaluate the influence of the location of the sulcal interruption.

The sample is quite high-functioning and the generalisability of the findings outside of this specific population is inevitably limited.