TY - JOUR
T1 - Evolution of the brainstem orofacial motor system in primates
T2 - A comparative study of trigeminal, facial, and hypoglossal nuclei
AU - Sherwood, Chet C.
AU - Hof, Patrick R.
AU - Holloway, Ralph L.
AU - Samendeferi, Katerina
AU - Gannon, Patrick J.
AU - Frahm, Heiko D.
AU - Zilles, Karl
N1 - Funding Information:
We thank Drs. J.K. Rilling, C.J. Terranova, C.J. Vinyard, S.C. McFarlin, and the anonymous reviewers for helpful suggestions that improved this manuscript. We thank Dr. J.M. Erwin for constant interest and support. Dr. C.E. MacLeod generously shared shrinkage correction factor data. This work was supported by the Leakey Foundation, the Wenner-Gren Foundation for Anthropological Research, NSF BCS-0121286, NSF SBE-SBR-9617262, NSF IBN-9905402, NSF DBI-9602234 (to NYCEP), and the Mount Sinai School of Medicine. Part of this work was supported by a grant to K.Z. (Human Brain Project/Neuroinformatics research funded by the National Institute of Biomedical Imaging and Bioengineering, the National Institute of Neurological Disorders and Stroke, and the National Institute of Mental Health). P.R.H. is the Regenstreif Professor of Neuroscience.
PY - 2005/1
Y1 - 2005/1
N2 - The trigeminal motor (Vmo), facial (VII), and hypoglossal (XII) nuclei of the brainstem comprise the final common output for neural control of most orofacial muscles. Hence, these cranial motor nuclei are involved in the production of adaptive behaviors such as feeding, facial expression, and vocalization. We measured the volume and Grey Level Index (GLI) of Vmo, VII, and XII in 47 species of primates and examined these nuclei for scaling patterns and phylogenetic specializations. Allometric regression, using medulla volume as an independent variable, did not reveal a significant difference between strepsirrhines and haplorhines in the scaling of Vmo volume. In addition, correlation analysis using independent contrasts did not find a relationship between Vmo size or GLI and the percent of leaves in the diet. The scaling trajectory of VII volume, in contrast, differed significantly between suborders. Great ape and human VII volumes, furthermore, were significantly larger than predicted by the haplorhine regression. Enlargement of VII in these taxa may reflect increased differentiation of the facial muscles of expression and greater utilization of the visual channel in social communication. The independent contrasts of VII volume and GLI, however, were not correlated with social group size. To examine whether the human hypoglossal motor system is specialized to control the tongue for speech, we tested human XII volume and GLI for departures from nonhuman haplorhine prediction lines. Although human XII volumes were observed above the regression line, they did not exceed prediction intervals. Of note, orang-utan XII volumes had greater residuals than humans. Human XII GLI values also did not differ from allometric prediction. In sum, these findings indicate that the cranial orofacial motor nuclei evince a mosaic of phylogenetic specializations for innervation of the facial muscles of expression in the context of a generally conservative scaling relationship with respect to medulla size.
AB - The trigeminal motor (Vmo), facial (VII), and hypoglossal (XII) nuclei of the brainstem comprise the final common output for neural control of most orofacial muscles. Hence, these cranial motor nuclei are involved in the production of adaptive behaviors such as feeding, facial expression, and vocalization. We measured the volume and Grey Level Index (GLI) of Vmo, VII, and XII in 47 species of primates and examined these nuclei for scaling patterns and phylogenetic specializations. Allometric regression, using medulla volume as an independent variable, did not reveal a significant difference between strepsirrhines and haplorhines in the scaling of Vmo volume. In addition, correlation analysis using independent contrasts did not find a relationship between Vmo size or GLI and the percent of leaves in the diet. The scaling trajectory of VII volume, in contrast, differed significantly between suborders. Great ape and human VII volumes, furthermore, were significantly larger than predicted by the haplorhine regression. Enlargement of VII in these taxa may reflect increased differentiation of the facial muscles of expression and greater utilization of the visual channel in social communication. The independent contrasts of VII volume and GLI, however, were not correlated with social group size. To examine whether the human hypoglossal motor system is specialized to control the tongue for speech, we tested human XII volume and GLI for departures from nonhuman haplorhine prediction lines. Although human XII volumes were observed above the regression line, they did not exceed prediction intervals. Of note, orang-utan XII volumes had greater residuals than humans. Human XII GLI values also did not differ from allometric prediction. In sum, these findings indicate that the cranial orofacial motor nuclei evince a mosaic of phylogenetic specializations for innervation of the facial muscles of expression in the context of a generally conservative scaling relationship with respect to medulla size.
KW - Brain evolution
KW - Communication
KW - Comparative neuroanatomy
KW - Facial expression
KW - Language evolution
KW - Muscles of mastication
KW - Speech
KW - Tongue
KW - Vocalization
UR - http://www.scopus.com/inward/record.url?scp=12144281635&partnerID=8YFLogxK
U2 - 10.1016/j.jhevol.2004.10.003
DO - 10.1016/j.jhevol.2004.10.003
M3 - Article
C2 - 15656936
AN - SCOPUS:12144281635
SN - 0047-2484
VL - 48
SP - 45
EP - 84
JO - Journal of Human Evolution
JF - Journal of Human Evolution
IS - 1
ER -