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«Published in final edited form as: Brain and Language, 2013 DOI: 10.1016/j.bandl.2013.03.001 Dorsal and ventral pathways in language development Jens ...»

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The inclusion of these most posterior frontal connections is in accordance with ex vivo dissection data (Martino et al., 2010 and Sarubbo et al., 2011).

Besides the undetectable dorsal D2 connection, our newborn data revealed that also the white matter in the ventral fronto-temporal connections is delayed in its maturation. While adults and also children (though not yet on adult level) show higher FA in these pathways than in mean FA across the cerebral white matter, this is not the case for newborns. This result is consistent with previous findings on white matter maturation that showed slower myelination in language-related frontotemporal regions compared to sensory or motor related white matter (Pujol et al., 2006).

For both, the dorsal and the ventral stream, the core language-relevant tracts terminating in Broca’s area in the IFG can be considered as subcomponents of the two streams, i.e. as specific pathways or tracts within the streams (Rauschecker & Scott, 2009). It is the ventral pathway connecting the ventral part of the IFG and BA 45 to the temporo-parietal region of the language network that is in place very early.

This result argues for an initial prominence of the ventral pathway (together with the dorsal pathway D1 connecting to the premotor cortex) in the language processing network during ontogeny. The dorsal pathway D2 connecting to Broca’s area unfolds its involvement in higher language functions only during further development and is evident in 7-year-old children but not in newborn infants. On the basis of the present data, we cannot specify from what exact age this pathway connecting to BA 44 is in place. We argue that dorsal pathway D2 is necessary for more complex linguistic processes and would therefore be observable in early childhood, but not in infancy. It is important to note, however, that not delineating a fiber tract in DWI data by tractography does not imply this tract is missing in the brain. But compared to all other fiber pathways investigated in the present study that could be tracked in newborns, this tracking was not possible for dorsal pathway D2. This suggests that D2 in newborns conveys properties that differ from other age groups and also from other pathways in newborns. We argue that the underlying reason is the pathway’s immaturity as reflected in low FA.

Information exchange between frontal and temporal language regions can be guaranteed via the ventral pathway in cases where the dorsal pathway is not fully available, either due to brain lesions (Wilson et al., 2011), or due to structural immaturity in development (Brauer et al., 2011). The relevance of the ventral pathway for language processing has further been evidenced by a study with healthy adults that revealed that individual FA differences in the extreme and external capsule region of the ventral pathway correspond to individual abilities in word segmentation and grammar rule-learning under articulatory suppression which was used to tax the dorsal phonological memory system (Lopez-Barroso et al., 2011).

Additional evidence for an involvement of the ventral pathway in language learning comes from a study in 8-10 year old children which reported higher FA in the ventral pathway along the IFOF in bilingual compared to monolingual children (Mohades et al., 2012).

The strong reliance on the ventral pathway during language development might also yield particular processing strategies. The involvement of the ventral inferior frontal areas in semantic processes was described in functional imaging studies for adults (Vigneau et al., 2006) and also for children (Sakai, 2005). The connection from the ventral IFG to the temporal cortex via the IFOF that was proposed to serve as a route for semantic processes (Duffau et al., 2005). The observed dominance of semantic strategies in sentence comprehension during early language development (Bates et al., 1984) is in line with the idea that the ventral pathway is a primary connection within the language network during early development. However, these functional consequences of white matter maturation were not directly testable within the present pure anatomical study.

Bringing together results from studies on a ventral connection between the temporal lobe and the IFG requires some consideration of findings concerning the ECFS and IFOF. The IFOF runs via the EmC/EC and is widely accepted to include terminations in the ventral IFG (Catani et al., 2002; Forkel et al.; Thiebaut de Schotten et al., 2012 and Vandermosten et al., 2012). This connectivity is identical to the connectivity of the superficial tract V1, as defined by ex vivo dissection (Martino et al., 2010 and Sarubbo et al., 2011). The ECFS is suggested to run via the EmC connecting the IFG to the temporal lobe. In DTI data it is difficult to clearly separate the EC and EmC because of their size and proximity. Even in ex vivo dissection there is not always a clear cut between the two capsules and the fibers of the IFOF tracts probably run in both the EmC and EC (Sarubbo et al., 2011).

The present report comparing data from two studies has some limitations that deserve further discussion. The newborns’ data were obtained at a different scanner than the children and adults’ data. In order to ensure the reliability of the observed group differences in FA, we compared the infant data with data from a control group of adolescents and young adults obtained at the same scanner and using a very similar protocol adapted for adults. This comparison confirmed the findings from the original analysis (for details, see Suppl. Content). In the present comparison, grouplevel tracking was confirmed on the individual level. For instance, dorsal pathway D2 was absent in all of the newborn brains: conversely, it was present in the tracking results of every one of the child and adult brains (see Suppl. Content).

5 Conclusions

Our results support the view of a change in the fronto-temporal network from infancy to childhood with a later maturation of the dorsal compared to the ventral connection.

Given the important role of the two connecting streams in the language network as shown in previous studies, we postulate an association between the time course of language development and the maturation of the fronto-temporal pathways, particularly the late maturation of the dorsal one. Tract V1 of the ventral pathway is the first one in the developing brain that connects the temporal and ventral inferior frontal language-relevant regions and is observable in newborn infants. For the dorsal pathways, pathway D1 terminating in PMC is already in place at birth. This pathway is likely to support auditory-to-motor mapping, which is necessary for auditory-motor feedback during babbling and language learning in infancy. Dorsal pathway D2 matures later and is evident in children, but, due to scarce myelination, not yet observable in newborns. This tract of the dorsal connection terminates in the dorsal IFG and is assumed to play a role in the development of more complex language functions.

6 Acknowledgements We thank Paola Scifo for support of MRI data acquisition. Part of this work was supported by a grant from the European Research Council to A.F. (ERC-2010-AdG 20100407, NeuroSyntax).

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