Early uneven ear input induces long-lasting differences in left–right motor function

Michelle W. Antoine, Xiaoxia Zhu, Marianne Dieterich, Thomas Brandt, Sarath Vijayakumar, Nicholas McKeehan, Joseph C. Arezzo, R. Suzanne Zukin, David A. Borkholder, Sherri M. Jones, Robert D. Frisina, Jean M. Hebert

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

How asymmetries in motor behavior become established normally or atypically in mammals remains unclear. An established model for motor asymmetry that is conserved across mammals can be obtained by experimentally inducing asymmetric striatal dopamine activity. However, the factors that can cause motor asymmetries in the absence of experimental manipulations to the brain remain unknown. Here, we show that mice with inner ear dysfunction display a robust left or right rotational preference, and this motor preference reflects an atypical asymmetry in cortico-striatal neurotransmission. By unilaterally targeting striatal activity with an antagonist of extracellular signal-regulated kinase (ERK), a downstream integrator of striatal neurotransmitter signaling, we can reverse or exaggerate rotational preference in these mice. By surgically biasing vestibular failure to one ear, we can dictate the direction of motor preference, illustrating the influence of uneven vestibular failure in establishing the outward asymmetries in motor preference. The inner ear–induced striatal asymmetries identified here intersect with non–ear-induced asymmetries previously linked to lateralized motor behavior across species and suggest that aspects of left–right brain function in mammals can be ontogenetically influenced by inner ear input. Consistent with inner ear input contributing to motor asymmetry, we also show that, in humans with normal ear function, the motor-dominant hemisphere, measured as handedness, is ipsilateral to the ear with weaker vestibular input.

Original languageEnglish (US)
Article numbere2002988
JournalPLoS Biology
Volume16
Issue number3
DOIs
StatePublished - Mar 13 2018

Fingerprint

Corpus Striatum
Ear
ears
Inner Ear
Mammals
Functional Laterality
mammals
Extracellular Signal-Regulated MAP Kinases
Brain
Synaptic Transmission
Neurotransmitter Agents
Dopamine
brain
mice
neurotransmitters
dopamine
mitogen-activated protein kinase
antagonists

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Antoine, M. W., Zhu, X., Dieterich, M., Brandt, T., Vijayakumar, S., McKeehan, N., ... Hebert, J. M. (2018). Early uneven ear input induces long-lasting differences in left–right motor function. PLoS Biology, 16(3), [e2002988]. https://doi.org/10.1371/journal.pbio.2002988

Early uneven ear input induces long-lasting differences in left–right motor function. / Antoine, Michelle W.; Zhu, Xiaoxia; Dieterich, Marianne; Brandt, Thomas; Vijayakumar, Sarath; McKeehan, Nicholas; Arezzo, Joseph C.; Zukin, R. Suzanne; Borkholder, David A.; Jones, Sherri M.; Frisina, Robert D.; Hebert, Jean M.

In: PLoS Biology, Vol. 16, No. 3, e2002988, 13.03.2018.

Research output: Contribution to journalArticle

Antoine, MW, Zhu, X, Dieterich, M, Brandt, T, Vijayakumar, S, McKeehan, N, Arezzo, JC, Zukin, RS, Borkholder, DA, Jones, SM, Frisina, RD & Hebert, JM 2018, 'Early uneven ear input induces long-lasting differences in left–right motor function', PLoS Biology, vol. 16, no. 3, e2002988. https://doi.org/10.1371/journal.pbio.2002988
Antoine MW, Zhu X, Dieterich M, Brandt T, Vijayakumar S, McKeehan N et al. Early uneven ear input induces long-lasting differences in left–right motor function. PLoS Biology. 2018 Mar 13;16(3). e2002988. https://doi.org/10.1371/journal.pbio.2002988
Antoine, Michelle W. ; Zhu, Xiaoxia ; Dieterich, Marianne ; Brandt, Thomas ; Vijayakumar, Sarath ; McKeehan, Nicholas ; Arezzo, Joseph C. ; Zukin, R. Suzanne ; Borkholder, David A. ; Jones, Sherri M. ; Frisina, Robert D. ; Hebert, Jean M. / Early uneven ear input induces long-lasting differences in left–right motor function. In: PLoS Biology. 2018 ; Vol. 16, No. 3.
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