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 journalArticle

20 Citations (Scopus)

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 languageEnglish (US)
Pages (from-to)400-404
Number of pages5
JournalScience
Volume357
Issue number6349
DOIs
StatePublished - Jul 28 2017

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Primates
Motor Cortex

All Science Journal Classification (ASJC) codes

  • General

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Gu, Z., Kalamboglas, J., Yoshioka, S., Han, W., Li, Z., Kawasawa, Y. I., ... 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
Gu, Zirong ; Kalamboglas, John ; Yoshioka, Shin ; Han, Wenqi ; Li, Zhuo ; Kawasawa, Yuka Imamura ; Pochareddy, Sirisha ; Li, Zhen ; Liu, Fuchen ; Xu, Xuming ; Wijeratne, Sagara ; Ueno, Masaki ; Blatz, Emily ; Salomone, Joseph ; Kumanogoh, Atsushi ; Rasin, Mladen Roko ; Gebelein, Brian ; Weirauch, Matthew T. ; Sestan, Nenad ; Martin, John H. ; Yoshida, Yutaka. / Control of species-dependent cortico-motoneuronal connections underlying manual dexterity. In: Science. 2017 ; Vol. 357, No. 6349. pp. 400-404.
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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.",
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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

Control of species-dependent cortico-motoneuronal connections underlying manual dexterity. / Gu, Zirong; Kalamboglas, John; Yoshioka, Shin; Han, Wenqi; Li, Zhuo; Kawasawa, Yuka Imamura; Pochareddy, Sirisha; Li, Zhen; Liu, Fuchen; Xu, Xuming; Wijeratne, Sagara; Ueno, Masaki; Blatz, Emily; Salomone, Joseph; Kumanogoh, Atsushi; Rasin, Mladen Roko; Gebelein, Brian; Weirauch, Matthew T.; Sestan, Nenad; Martin, John H.; Yoshida, Yutaka.

In: Science, Vol. 357, No. 6349, 28.07.2017, p. 400-404.

Research output: Contribution to journalArticle

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AU - Gu, Zirong

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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

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Gu Z, Kalamboglas J, Yoshioka S, Han W, Li Z, Kawasawa YI et al. Control of species-dependent cortico-motoneuronal connections underlying manual dexterity. Science. 2017 Jul 28;357(6349):400-404. https://doi.org/10.1126/science.aan3721