Control of species-dependent cortico-motoneuronal connections underlying manual dexterity

Zirong Gu; John Kalamboglas; Shin Yoshioka; Wenqi Han; Zhuo Li; Yuka Imamura Kawasawa; Sirisha Pochareddy; Zhen Li; Fuchen Liu; Xuming Xu; Sagara Wijeratne; Masaki Ueno; Emily Blatz; Joseph Salomone; Atsushi Kumanogoh; Mladen Roko Rasin; Brian Gebelein; Matthew T. Weirauch; Nenad Sestan; John H. Martin; Yutaka Yoshida

doi:10.1126/science.aan3721

Control of species-dependent cortico-motoneuronal connections underlying manual dexterity

Zirong Gu, John Kalamboglas, Shin Yoshioka, Wenqi Han, Zhuo Li, Yuka Imamura Kawasawa, Sirisha Pochareddy, Zhen Li, Fuchen Liu, Xuming Xu, Sagara Wijeratne, Masaki Ueno, Emily Blatz, Joseph Salomone, Atsushi Kumanogoh, Mladen Roko Rasin, Brian Gebelein, Matthew T. Weirauch, Nenad Sestan, John H. MartinYutaka Yoshida

Research output: Contribution to journal › Article › peer-review

80 Scopus citations

Abstract

Superior manual dexterity in higher primates emerged together with the appearance of cortico-motoneuronal (CM) connections during the evolution of the mammalian corticospinal (CS) system. Previously thought to be specific to higher primates, we identified transient CM connections in early postnatal mice, which are eventually eliminated by Sema6D-PlexA1 signaling. PlexA1 mutant mice maintain CM connections into adulthood and exhibit superior manual dexterity as compared with that of controls. Last, differing PlexA1 expression in layer 5 of the motor cortex, which is strong in wild-type mice but weak in humans, may be explained by FEZF2-mediated cis-regulatory elements that are found only in higher primates. Thus, species-dependent regulation of PlexA1 expression may have been crucial in the evolution of mammalian CS systems that improved fine motor control in higher primates.

Original language	English (US)
Pages (from-to)	400-404
Number of pages	5
Journal	Science
Volume	357
Issue number	6349
DOIs	https://doi.org/10.1126/science.aan3721
State	Published - Jul 28 2017

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Gu, Z., Kalamboglas, J., Yoshioka, S., Han, W., Li, Z., Kawasawa, Y. I., Pochareddy, S., Li, Z., Liu, F., Xu, X., Wijeratne, S., Ueno, M., Blatz, E., Salomone, J., Kumanogoh, A., Rasin, M. R., Gebelein, B., Weirauch, M. T., Sestan, N., ... Yoshida, Y. (2017). Control of species-dependent cortico-motoneuronal connections underlying manual dexterity. Science, 357(6349), 400-404. https://doi.org/10.1126/science.aan3721

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title = "Control of species-dependent cortico-motoneuronal connections underlying manual dexterity",

abstract = "Superior manual dexterity in higher primates emerged together with the appearance of cortico-motoneuronal (CM) connections during the evolution of the mammalian corticospinal (CS) system. Previously thought to be specific to higher primates, we identified transient CM connections in early postnatal mice, which are eventually eliminated by Sema6D-PlexA1 signaling. PlexA1 mutant mice maintain CM connections into adulthood and exhibit superior manual dexterity as compared with that of controls. Last, differing PlexA1 expression in layer 5 of the motor cortex, which is strong in wild-type mice but weak in humans, may be explained by FEZF2-mediated cis-regulatory elements that are found only in higher primates. Thus, species-dependent regulation of PlexA1 expression may have been crucial in the evolution of mammalian CS systems that improved fine motor control in higher primates.",

author = "Zirong Gu and John Kalamboglas and Shin Yoshioka and Wenqi Han and Zhuo Li and Kawasawa, {Yuka Imamura} and Sirisha Pochareddy and Zhen Li and Fuchen Liu and Xuming Xu and Sagara Wijeratne and Masaki Ueno and Emily Blatz and Joseph Salomone and Atsushi Kumanogoh and Rasin, {Mladen Roko} and Brian Gebelein and Weirauch, {Matthew T.} and Nenad Sestan and Martin, {John H.} and Yutaka Yoshida",

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doi = "10.1126/science.aan3721",

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Gu, Z, Kalamboglas, J, Yoshioka, S, Han, W, Li, Z, Kawasawa, YI, Pochareddy, S, Li, Z, Liu, F, Xu, X, Wijeratne, S, Ueno, M, Blatz, E, Salomone, J, Kumanogoh, A, Rasin, MR, Gebelein, B, Weirauch, MT, Sestan, N, Martin, JH & Yoshida, Y 2017, 'Control of species-dependent cortico-motoneuronal connections underlying manual dexterity', Science, vol. 357, no. 6349, pp. 400-404. https://doi.org/10.1126/science.aan3721

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AU - Gu, Zirong

AU - Kalamboglas, John

AU - Yoshioka, Shin

AU - Han, Wenqi

AU - Li, Zhuo

AU - Kawasawa, Yuka Imamura

AU - Pochareddy, Sirisha

AU - Li, Zhen

AU - Liu, Fuchen

AU - Xu, Xuming

AU - Wijeratne, Sagara

AU - Ueno, Masaki

AU - Blatz, Emily

AU - Salomone, Joseph

AU - Kumanogoh, Atsushi

AU - Rasin, Mladen Roko

AU - Gebelein, Brian

AU - Weirauch, Matthew T.

AU - Sestan, Nenad

AU - Martin, John H.

AU - Yoshida, Yutaka

PY - 2017/7/28

Y1 - 2017/7/28

N2 - Superior manual dexterity in higher primates emerged together with the appearance of cortico-motoneuronal (CM) connections during the evolution of the mammalian corticospinal (CS) system. Previously thought to be specific to higher primates, we identified transient CM connections in early postnatal mice, which are eventually eliminated by Sema6D-PlexA1 signaling. PlexA1 mutant mice maintain CM connections into adulthood and exhibit superior manual dexterity as compared with that of controls. Last, differing PlexA1 expression in layer 5 of the motor cortex, which is strong in wild-type mice but weak in humans, may be explained by FEZF2-mediated cis-regulatory elements that are found only in higher primates. Thus, species-dependent regulation of PlexA1 expression may have been crucial in the evolution of mammalian CS systems that improved fine motor control in higher primates.

AB - Superior manual dexterity in higher primates emerged together with the appearance of cortico-motoneuronal (CM) connections during the evolution of the mammalian corticospinal (CS) system. Previously thought to be specific to higher primates, we identified transient CM connections in early postnatal mice, which are eventually eliminated by Sema6D-PlexA1 signaling. PlexA1 mutant mice maintain CM connections into adulthood and exhibit superior manual dexterity as compared with that of controls. Last, differing PlexA1 expression in layer 5 of the motor cortex, which is strong in wild-type mice but weak in humans, may be explained by FEZF2-mediated cis-regulatory elements that are found only in higher primates. Thus, species-dependent regulation of PlexA1 expression may have been crucial in the evolution of mammalian CS systems that improved fine motor control in higher primates.

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Control of species-dependent cortico-motoneuronal connections underlying manual dexterity

Abstract

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