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Structural and Functional Brain Rewiring Clarifies Preserved Interhemispheric Transfer in Humans Born Without the Corpus Callosum

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Structural and Functional Brain Rewiring Clarifies Preserved Interhemispheric Transfer in Humans Born Without the Corpus Callosum Structural and functional brain rewiring clarifies preserved interhemispheric transfer in humans born without the corpus callosum Fernanda Tovar-Molla,b,c,d,1, Myriam Monteiroa,b, Juliana Andradea,b, Ivanei E. Bramatia,b, Rodrigo Vianna-Barbosaa,b, Theo Marinsa,b, Erika Rodriguesa,e, Natalia Dantasa,b, Timothy E. J. Behrensf, Ricardo de Oliveira-Souzaa, Jorge Molla,c, and Roberto Lenta,b,c,1 aD’Or Institute for Research and Education (IDOR), 22281-032, Rio de Janeiro, Brazil; bInstitute of Biomedical Sciences (ICB) and dNational Center of Structural Biology and Bioimaging (CENABIO), Federal University of Rio de Janeiro, 21941-902, Rio de Janeiro, Brazil; cNational Institute for Translational Neuroscience (INNT), Ministry of Science and Technology, Brazil; eAugusto Motta University (Unisuam), 21041-020, Rio de Janeiro, Brazil; and fCentre for Functional Magnetic Resonance Imaging of the Brain, Oxford University, Oxford OX3 9DU, United Kingdom Edited by Giovanni Berlucchi, Universita di Verona, Verona, Italy, and accepted by the Editorial Board April 17, 2014 (received for review January 15, 2014) Why do humans born without the corpus callosum, the major in- humans and monkeys (14, 15). None of the anomalous tracts in terhemispheric commissure, lack the disconnection syndrome classically CD, however, has been proven to explain the disconnection par- described in callosotomized patients? This paradox was discovered by adox observed in these patients, which has remained unsolved Nobel laureate Roger Sperry in 1968, and has remained unsolved since since its discovery by Sperry and his collaborators (6, 7). then. To tackle the hypothesis that alternative neural pathways could To approach this puzzle, we followed the hypothesis that the explain this puzzle, we investigated patients with callosal dysgenesis early infliction of the callosal defect would provide the developing using structural and functional neuroimaging, as well as neuropsycho- brain with a set of anomalous connections that might preserve the logical assessments. We identified two anomalous white-matter tracts crossed transfer of information between cortical areas, and thus by deterministic and probabilistic tractography, and provide sup- assume—at least in part—the functions of the CC. We used porting resting-state functional neuroimaging and neuropsycholog- multiple neuroimaging techniques and neuropsychological tests ical evidence for their functional role in preserved interhemispheric on subjects with total (agenesis) and partial CD, and compared transfer of complex tactile information, such as object recognition. them with normal controls. In addition to confirming the pres- These compensatory pathways connect the homotopic posterior ence of the previously known long, aberrant tracts of the white parietal cortical areas (Brodmann areas 39 and surroundings) via the matter, the Probst and the sigmoid bundles (10–12), we describe posterior and anterior commissures. We propose that anomalous the trajectory of two so-far unreported homotopic interhemi- brain circuitry of callosal dysgenesis is determined by long-distance plasticity, a set of hardware changes occurring in the developing spheric tracts that course through the posterior or anterior brain after pathological interference. So far unknown, these patho- commissures, and provide evidence suggestive of their functional logical changes somehow divert growing axons away from the dorsal midline, creating alternative tracts through the ventral fore- Significance brain and the dorsal midbrain midline, with partial compensatory effects to the interhemispheric transfer of cortical function. Individuals subjected to surgical transection of the corpus cal- losum (“split-brains”) fail to transfer information between the callosal agenesis | callosal plasticity | human connectome cerebral hemispheres, a condition known as “disconnection syndrome.” On the other hand, subjects born without the cal- he human brain connectome is sculpted out of intensive in- losum (callosal dysgenesis, CD) typically show preserved in- Tteraction between genes and environment during devel- terhemispheric communication. To clarify this paradox, which opment (1). Subtle interference in this lengthy interactive has defied neuroscientists for decades, we investigated CD process generates individual differences and peculiarities within subjects using functional and structural neuroimaging and the normal range of human variation (2). However, more drastic neuropsychological tests. Results demonstrated the existence developmental disturbances impose changes that will greatly of anomalous interhemispheric tracts that cross through the modify adult brain circuits, with adverse consequences for cog- midbrain and ventral forebrain, linking the parietal cortices nition and behavior (3). This is the case of callosal dysgenesis bilaterally. These findings provide an explanation for the pre- (CD), a condition well-known for generating gross morphologi- served cross-transfer of tactile information between hemi- NEUROSCIENCE cal changes in the brain, and pronounced cognitive and behav- spheres in CD. We suggest that this condition is associated with ioral consequences to the patients (4). extensive brain rewiring, generating a new circuitry that pro- CD differs greatly from callosotomy, however, because the vides functional compensatory interhemispheric integration. latter is characterized by a clear disconnection syndrome (5), whereas the former displays a considerable degree of inter- Author contributions: F.T.-M., R.d.O.-S., and R.L. designed research; M.M., J.A., I.E.B., R.V.-B., hemispheric communication, despite absence of the corpus T.M., E.R., N.D., and R.d.O.-S. performed research; F.T.-M., M.M., J.A., I.E.B., R.V.-B., T.M., E.R., T.E.J.B., R.d.O.-S., J.M., and R.L. analyzed data; F.T.-M. and R.L. coordinated the callosum (CC) (6, 7). The clinical presentation of CD is highly general strategy of the project; M.M. and R.d.O.-S. conceived the neuropsychological variable, ranging from subtle, subnormal, cognitive symptoms to battery and performed the tests; I.E.B., R.V.-B., T.M., and E.R. conceived and performed severe mental retardation, epilepsy, and somatic deficits (4). the neuroimaging experiments; T.E.J.B. contributed to neuroimaging data analysis; and Strikingly, however, all cases maintain some degree of inter- F.T.-M., J.M., and R.L. wrote the paper. hemispheric transfer (8), possibly mediated by compensatory The authors declare no conflict of interest. pathways (9) that would—at least partially—replace the role of This article is a PNAS Direct Submission. G.B. is a guest editor invited by the Editorial the (absent or defective) CC. In fact, some evidence for white- Board. matter circuit reorganization in CD has been produced (10–12), 1To whom correspondence may be addressed. E-mail: [email protected] or but no rewiring of any kind has been identified in adults sub- [email protected]. jected to callosal transection (13), although failure to interrupt This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. interhemispheric transfer has been reported after callosotomy in 1073/pnas.1400806111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1400806111 PNAS | May 27, 2014 | vol. 111 | no. 21 | 7843–7848 Downloaded by guest on September 28, 2021 role in enabling crossed-transfer of complex tactile function be- fractional anisotropy (FA) DTI maps, however, showed a more tween the hemispheres of these subjects. organized (higher FA) posterior commissure in CD subjects, compared with controls. In addition, DTI and FACT tractog- Results raphy revealed an aberrant interhemispheric tract crossing the Longitudinal and Crossed Heterotopic Abnormal Circuits. Anatomical midline at the level of the posterior commissure (heretofore MRI showed the typical morphological features of CD, including referred to as the “aberrant midbrain bundle”) in four patients parallel, enlarged lateral ventricles, downward displacement of with CD (Fig. 1A, Fig. S3 A–D, and Table S1), and another the cingulate gyrus, and radial sulci on the medial brain surface. bundle crossing through the anterior commissure in one CD A summary of the main characteristics and experimental approaches patient (referred to as the “aberrant ventral forebrain bundle”) for CD subjects are listed in Table S1. (Fig. 1B, Fig. S3E, and Table S1). Both bundles were shown to Aberrant fibers forming the Probst bundles were identified interconnect the dorsolateral parietal cortices homotopically. In by diffusion tensor imaging (DTI/deterministic tractography) addition, it is remarkable that they follow a trajectory parallel (Materials and Methods) in all individuals with CD in our sample and adjacent to the corticospinal tract, as shown in Fig. S3 A–D. (Fig. S1 and Table S1), as described in previous studies (11, 12). rs-fMRI data (using independent component analyses) sup- Another abnormal interhemispheric, heterotopic, white-matter ported these tractographic findings by showing that CD brains pathway (the sigmoid bundle) has also been described in CD (11, exhibited a robust, bilaterally symmetric functional connectivity 12, 16). DTI tractography analysis showed that this aberrant bun- corresponding to the posterior parietal cortex component of the dle crosses the midline and connects the occipitoparietal region default mode network (DMN) (Fig. 2A), in close resemblance to with the contralateral frontal pole through the rostral remnant of controls (Fig. 2B).
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