Early uneven ear input induces long-lasting differences in left-right motor function.
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 moto...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2018-03-01
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| Series: | PLoS Biology |
| Online Access: | http://europepmc.org/articles/PMC5849283?pdf=render |
| _version_ | 1818619313005789184 |
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| author | 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 Hébert |
| author_facet | 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 Hébert |
| author_sort | Michelle W Antoine |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-16T17:35:30Z |
| format | Article |
| id | doaj.art-585efff9782148cebaf22e2e325004ed |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-16T17:35:30Z |
| publishDate | 2018-03-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-585efff9782148cebaf22e2e325004ed2022-12-21T22:22:48ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852018-03-01163e200298810.1371/journal.pbio.2002988Early uneven ear input induces long-lasting differences in left-right motor function.Michelle W AntoineXiaoxia ZhuMarianne DieterichThomas BrandtSarath VijayakumarNicholas McKeehanJoseph C ArezzoR Suzanne ZukinDavid A BorkholderSherri M JonesRobert D FrisinaJean M HébertHow 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.http://europepmc.org/articles/PMC5849283?pdf=render |
| spellingShingle | 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 Hébert Early uneven ear input induces long-lasting differences in left-right motor function. PLoS Biology |
| title | Early uneven ear input induces long-lasting differences in left-right motor function. |
| title_full | Early uneven ear input induces long-lasting differences in left-right motor function. |
| title_fullStr | Early uneven ear input induces long-lasting differences in left-right motor function. |
| title_full_unstemmed | Early uneven ear input induces long-lasting differences in left-right motor function. |
| title_short | Early uneven ear input induces long-lasting differences in left-right motor function. |
| title_sort | early uneven ear input induces long lasting differences in left right motor function |
| url | http://europepmc.org/articles/PMC5849283?pdf=render |
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