Individual differences in nerve fiber myelination: A methodological study

6.1 Diffusion tensor imaging

6.1.1 Corpus callosum

Positive correlations among age and FA in the genu and body of the CC, along with negative associations among age and RD and MD demonstrated in our study agree with previous findings (e.g., Luders et al., 2010). The results indicate an age-related increase in callosal thickness, which is more pronounced in the anterior and mid regions of the tract. Lack of correlation across the posterior surface (i.e., splenium) of the CC may reflect a greater microstructural variability in this region during the first three decades of life. Congruently, the literature shows greater age-related changes in posterior portion of the CC,than in the anterior parts in individuals aged 4-22 years(Chung et al., 2001; Giedd et al., 1999; Rajapakse et al., 1996). An anterior to posterior (i.e., rostrocaudal) gradient of callosal maturation in 3-15 years old children was proposed (Thompson et al., 2000), whereas based on structural MRI findings, aposterior to anterior gradient of callosal development was suggested(Giedd et al., 1996). Luders et al.(2010) points to the hypothesis of an anterior-to-posterior gradient of callosal maturation and indicates that the age of 9-10 years in girls and 11-12 years in boys is a key period of CC maturation and growth. The switch in callosal maturation profile from retrosplenial to a forward-moving wave of development is known to occur at the age of 15-16 in females and 18-18 in males and a peak of anterior growth of the CC in late adolescence (Luders et al., 2010). This discrepancy may be explained by the difference in age range considered in this study (8-30 years) and in previous studies (4-22 years). Since the callosal maturation was shown to significantly depend on age (Luders et al., 2010), selection of the age range may significantly influencethe outcome of the measurements. In addition, these disagreements may also be a consequence of using different approaches of structural evaluation of the tract and differences in regional specificity. The current findings point to the importance of choosing similar strategies for fiber tract division and highlight the importance of complex methodological approaches in studying white matter maturation.

Our data further demonstratethe differences in FA and RD between the anterior (genu) and mid (body) regions of the CC and the posterior portion of the tract (splenium), which are more pronounced in children and adolescents, and they almost disappear in adults, thus indicating that they may be specific to developmental profile of this fiber tract. A pronounced difference in DTI indices in the splenium of the CC compared to the genu and body (Giedd et al., 1996), and an increase in myelination with maturation(Giedd et al., 1996; Rathee et al., 2016) were demonstrated in earlier studies.

Age-related increase in myelination indicated by an increase in FA and a decrease in RD and MD observed in the body of the CC and, to a lesser extent, in the genu of the CC, reflect a greater dependence of the anterior portion of the tract on age compared to posterior regions. These changes may result not only from axonal myelination, but also redirection of the fibers and pruning(Luders et al., 2010).

The differences between the youngest and the oldest participants were similar in both genders across the anterior and mid surfaces of the CC. The only region which showed gender differences was the splenium. The observed difference in myelination (higher FA and lower RD) in the splenium of the CC between 8-12 years old males and females is consistent with DTI findings of Schmithorst and colleagues(2008) who found that girls (mean age ~12 years) have higher FA in this region than boys. This may indicate an earlier growth rate of CC white matter volume in females. Other authors show no significant gender difference in the microstructural characteristics, as well as the growth rate of callosal regions(Bishop & Wahlsten, 1997; Giedd et al., 1996; Rajapakse et al., 1996), arguing that the observed differences result from differences in the ratio of the size of the CC to the whole brain size.

Overall, results of the present study provided normative values for three subdivisions of the CC for anterior and mid regions and the posterior surface of the CC, and regional differences in maturation ratesacross development.

6.1.2 Inferior fronto-occipital fasciculus

The IFOF is proposed to be the only fiber tract that directly connects the occipital lobe with the frontal regions (Catani, 2007). In addition to its role in semantic and visual processing(Catani & Thiebaut de Schotten, 2008; Rollans et al., 2017)and attention, it is thought to be a part of the mirror system(Catani, 2007). However, there is still no consensus regarding the degree to which its anatomical and structural properties can vary in the healthy brain. Moreover, very few studies investigated this fiber tract in healthy school-age children(Qiu et al., 2007; for review Tamnes et al., 2018).

The analysis of microstructural characteristics of the IFOF revealed a gradual increase in FA and a decrease in RD in both hemispheres across the 8- to 30-year age range, which may indicate a rapid change in myelination in school-age children. The right and left IFOF exhibited a similar trend of increasing FA, while RD and MD revealed fine differences in maturation pattern between the two hemispheres. As such, age-related reduction in RD in the right IFOF was characterized by a linear pattern with a very pronounced effect of age on this variable, which was the highest across all comparisons. Interestingly, the analysis of MD did not reveal changes in the left IFOF and only revealed an age-related decrease in MD in the right hemisphere. Notably, MD was the only metric which detected hemispheric asymmetry in adult participants with MD in the left IFOF to be higher than in the right IFOF. These differences became observable during the transition from adolescence to adulthood, when the MD values in the left hemisphere started growing after the decline observed during the transition from childhood to adolescence, which may indicate reorganization of functional networks in the brain and tuning of language and visual function in late childhood and adulthood.

The asymmetry of the IFOF has not been extensively investigated yet, although some of the previous studies report leftward asymmetry in microstructural properties of this fiber tract(Qiu et al., 2007; Shu et al., 2015; Wu et al., 2016). Critically, Catani et al.(2007) revealed interhemispheric differences in pathways associated with language function in more than half of adult participants (n=50), whereas 17% of the participants exhibited bilateral symmetrical distribution. Although an apparent hemispheric asymmetry was not observed in the current study, there was a pronounced difference in maturation pattern, which may indirectly reflect asymmetry associated with functional roles of each subdivision of the IFOF.

Therefore, the results show that the right IFOF continues to grow at least until adulthood, whereas the left IFOF exhibits cyclic maturation pattern and its microstructural properties change in a nonlinear fashion. Hemispheric asymmetry becomes observable only at later stages of ontogenesis. An increase in RD and MD in the left subdivision of the IFOF between ages 12 and 30 may indicate the change in fiber orientation and pruning, rather than decline in myelin thickness. This, in turn, may be related to the formation of new functional connections between the IFOF and various brain areas as children grow.



6.1.3 Inferior longitudinal fasciculus

The inferior longitudinal fasciculus connects the anterior portion of the temporal lobe with various areas of the occipital lobe and is known to play a critical role in visual object recognition and lexical and semantic processing (Catani, 2007).Theanalysis of DTI indices in the ILF found no changes in FA in both hemispheres. Instead, there was a robust decrease in MD and RD in the right subdivision of the ILF until the age of 12 years, after which the values of these parameters almost did not change. In the left ILF, age-related changes were indicated only by a small difference in RD between adolescents and younger children, which could indicate higher maturation rate and earlier myelination of the left subdivision of the ILF. These findings confirmed the results of earlier studies which indicate that, unlike lateral tracts in dorsal regions, the inferior areas are less affected by aging (Sullivan et al., 2010). The changes in FA are proposed to reflect changes not only in myelination, but in axonal diameter and density, while RD indicates alterations in myelination thickness (Lebel et al., 2012; Tamnes et al., 2018). Therefore, lack of the differences in FA along with a decrease in RD may indicate that the axonal diameter and density remained unchanged, while myelination in the ILF slightly increased. Alternatively, this effect may reflect fine tuning of functions associated with this fiber tract (Tamnes et al., 2018). The microstructural properties of the ILF did not show gender-specific effects.

According to the literature, at the age of 3 month, the ILF can be identified with DTI (Hermoye et al., 2006). It is thought that FA in the ILF reaches its maximum values by the age of 11, and MD decreases to its minimum by the age of 20 (Lebel et al., 2008), although recent studies also suggest that the maturation of the ILF continues into adolescence and by the age of 24, the ILF is still not fully mature (Lebel & Beaulieu, 2011; Lebel & Deoni, 2018), which agrees with the results of the present study.

Our study identified no differences in FA, RD, or MD values between the two hemispheres, although the difference was found in maturation pattern, which may also indirectly indicate functional asymmetry.Several studies show lateralization of the ILF in the right hemisphere (Herbet et al., 2018; Latini et al., 2017), whereas others demonstrate leftward asymmetry of the ILF volume (Shu et al., 2015), attributing it to asymmetry of language networks in the brain.Therefore, the results of this study add to the theoretical knowledge about the maturation pattern of the ILF.

6.2 Myelin proton fraction mapping

This study provided normative MPF values for adult participants. The results of the MPF analysis should be considered in the context of methodological contribution, highlighting the advantageof short scanning time and providing a sensitive measure of myelin content in neural tissue (Yarnykh, Prihod'ko, et al., 2018). Results from children and adolescents point to the importance of applying advanced methods of spacial alignment and fiber tract segmentation, which will be considered in future studies.



Conclusion

The goal of this work was to provide normative data for DTI and MPF from healthy Russian subjects aged 8-30 years and to investigate the maturation pattern in the corpus callosum with its subdivisions, the inferior fronto-occipital fasciculus, and inferior longitudinal fasciculus in relation to age, gender, and hemispheric asymmetry. The results of the study added to existing knowledge on microstructural characteristics of these fiber tracts, which will further help to link white matter maturation with functional and behavioral indices and cognitive development. Future studies will expand the range of fiber tracts associated with complex cognitive functions and will relate microstructural properties of white matter pathways with measurements of behavioral performance. Also, more advanced methods of data processing, including atlas-based tractography approaches for DTI and the application of non-linear methods of coregistration for MPF will be used.



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