Direct interhemispheric cortical communication via thalamic commissures: a new white matter pathway in the primate brain

Author:

Szczupak Diego1ORCID,Schaeffer David J1ORCID,Tian Xiaoguang1ORCID,Choi Sang-Ho1ORCID,Fang-Cheng 2ORCID,Iack Pamela Meneses3ORCID,Campos Vinicius P4ORCID,Mayo J Patrick5ORCID,Patsch Janina6ORCID,Mitter Christian6ORCID,Haboosheh Amit7,Kwon Ha Seung1ORCID,Vieira Marcelo A C4ORCID,Reich Daniel S8ORCID,Jacobson Steve8ORCID,Kasprian Gregor6ORCID,Tovar-Moll Fernanda9ORCID,Lent Roberto310ORCID,Silva Afonso C1ORCID

Affiliation:

1. University of Pittsburgh Brain Institute, Department of Neurobiology, University of Pittsburgh , 3501 Fifth Avenue, Pittsburgh, PA 15261 , USA

2. Department of Neurological Surgery, University of Pittsburgh , 200 Lothrop Street, Pittsburgh, PA 15261 , USA

3. Biomedical Sciences Institute, Federal University of Rio de Janeiro , 373 Carlos Chagas Filho Avenue, Rio de Janeiro, Rio de Janeiro 21941-853 , Brazil

4. Department of Electrical and Computer Engineering, 400 Trabalhador São-Carlense Avenue, University of São Paulo , São Carlos, SP 13565-905 , Brazil

5. Department of Ophthalmology, University of Pittsburgh , 1622 Locust Street, Pittsburgh, PA 15261 , USA

6. Department of Biomedical Imaging and Image-Guided Therapy of the Medical University of Vienna , 18-20 Währinger Gürtel, 1090, Vienna , Austria

7. Department of Radiology Hadassah Ein Karem Hospital , Kalman Ya'akov Man St, Jerusalem 9112001 , Israel

8. National Institute of Neurological Disorders and Stroke, National Institutes of Health , 10 Center Drive, Bethesda, MD 20814 , USA

9. D’Or Institute of Research and Education, 30 Rua Diniz Cordeiro Street, Rio de Janeiro , Rio de Janeiro 22281-100 , Brazil

10. D’Or Institute of Research and Education, 30 Rua Diniz Cordeiro Street , Rio de Janeiro, Rio de Janeiro 22281-100 , Brazil

Abstract

Abstract Cortical neurons of eutherian mammals project to the contralateral hemisphere, crossing the midline primarily via the corpus callosum and the anterior, posterior, and hippocampal commissures. We recently reported and named the thalamic commissures (TCs) as an additional interhemispheric axonal fiber pathway connecting the cortex to the contralateral thalamus in the rodent brain. Here, we demonstrate that TCs also exist in primates and characterize the connectivity of these pathways with high-resolution diffusion-weighted MRI, viral axonal tracing, and fMRI. We present evidence of TCs in both New World (Callithrix jacchus and Cebus apella) and Old World primates (Macaca mulatta). Further, like rodents, we show that the TCs in primates develop during the embryonic period, forming anatomical and functionally active connections of the cortex with the contralateral thalamus. We also searched for TCs in the human brain, showing their presence in humans with brain malformations, although we could not identify TCs in healthy subjects. These results pose the TCs as a vital fiber pathway in the primate brain, allowing for more robust interhemispheric connectivity and synchrony and serving as an alternative commissural route in developmental brain malformations.

Funder

PA Department of Health

National Institute on Aging

Foundation of the State of Rio de Janeiro

National Council for Scientific and Technological Development

D'Or Institute for Research and Education

Intramural Research Program

National Institutes of Health

National Institute of Neurological Disorders and Stroke

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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