TY - JOUR
T1 - A pan-mammalian map of interhemispheric brain connections predates the evolution of the corpus callosum
AU - Suárez, Rodrigo
AU - Paolino, Annalisa
AU - Fenlon, Laura R.
AU - Morcom, Laura R.
AU - Kozulin, Peter
AU - Kurniawan, Nyoman D.
AU - Richards, Linda J.
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank the Queensland Nuclear Magnetic Resonance Network and the Australian National Imaging Facility for the operation of the scanners, the Queensland Brain Institute’s Advanced Microscopy Facility for histology imaging, and the University of Queensland Biological Resources and the Native Wildlife Teaching and Research Facility for all animal help. This work was supported by Australian Research Council Grants DP160103958 (to L.J.R. and R.S.) and DE160101394 (to R.S.), National Health and Medical Research Council Fellowships DP160103958 (to L.J.R. and R.S.) and DE160101394 (to R.S.), the Australian Postgraduate Award (to L.R.F. and L.R.M.), and the UQ-QBI Doctoral Scholarship award (to A.P.).
Publisher Copyright:
© 2018 National Academy of Sciences. All rights reserved.
PY - 2018/9/18
Y1 - 2018/9/18
N2 - The brain of mammals differs from that of all other vertebrates, in having a six-layered neocortex that is extensively interconnected within and between hemispheres. Interhemispheric connections are conveyed through the anterior commissure in egg-laying monotremes and marsupials, whereas eutherians evolved a separate commissural tract, the corpus callosum. Although the pattern of interhemispheric connectivity via the corpus callosum is broadly shared across eutherian species, it is not known whether this pattern arose as a consequence of callosal evolution or instead corresponds to a more ancient feature ofmammalian brain organization. Here we show that, despite cortical axons using an ancestral commissural route, monotremes and marsupials share features of interhemispheric connectivity with eutherians that likely predate the origin of the corpus callosum. Based on ex vivo magnetic resonance imaging and tractography, we found that connections through the anterior commissure in both fat-tailed dunnarts (Marsupialia) and duck-billed platypus (Monotremata) are spatially segregated according to cortical area topography. Moreover, cell-resolution retrograde and anterograde interhemispheric circuit mapping in dunnarts revealed several features shared with callosal circuits of eutherians. These include the layered organization of commissural neurons and terminals, a broad map of connections between similar (homotopic) regions of each hemisphere, and regions connected to different areas (heterotopic), including hyperconnected hubs along the medial and lateral borders of the cortex, such as the cingulate/motor cortex and claustrum/insula. We therefore propose that an interhemispheric connectome originated in early mammalian ancestors, predating the evolution of the corpus callosum. Because these features have been conserved throughout mammalian evolution, they likely represent key aspects of neocortical organization.
AB - The brain of mammals differs from that of all other vertebrates, in having a six-layered neocortex that is extensively interconnected within and between hemispheres. Interhemispheric connections are conveyed through the anterior commissure in egg-laying monotremes and marsupials, whereas eutherians evolved a separate commissural tract, the corpus callosum. Although the pattern of interhemispheric connectivity via the corpus callosum is broadly shared across eutherian species, it is not known whether this pattern arose as a consequence of callosal evolution or instead corresponds to a more ancient feature ofmammalian brain organization. Here we show that, despite cortical axons using an ancestral commissural route, monotremes and marsupials share features of interhemispheric connectivity with eutherians that likely predate the origin of the corpus callosum. Based on ex vivo magnetic resonance imaging and tractography, we found that connections through the anterior commissure in both fat-tailed dunnarts (Marsupialia) and duck-billed platypus (Monotremata) are spatially segregated according to cortical area topography. Moreover, cell-resolution retrograde and anterograde interhemispheric circuit mapping in dunnarts revealed several features shared with callosal circuits of eutherians. These include the layered organization of commissural neurons and terminals, a broad map of connections between similar (homotopic) regions of each hemisphere, and regions connected to different areas (heterotopic), including hyperconnected hubs along the medial and lateral borders of the cortex, such as the cingulate/motor cortex and claustrum/insula. We therefore propose that an interhemispheric connectome originated in early mammalian ancestors, predating the evolution of the corpus callosum. Because these features have been conserved throughout mammalian evolution, they likely represent key aspects of neocortical organization.
KW - Anterior commissure
KW - Claustrum
KW - Corpus callosum
KW - Cortical connectome
KW - Diffusion tensor MRI
UR - http://www.scopus.com/inward/record.url?scp=85053477349&partnerID=8YFLogxK
U2 - 10.1073/pnas.1808262115
DO - 10.1073/pnas.1808262115
M3 - Article
C2 - 30181276
AN - SCOPUS:85053477349
SN - 0027-8424
VL - 115
SP - 9622
EP - 9627
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 38
ER -