Predictive encoding of motor behavior in the supplementary motor area is disrupted in parkinsonism Article Swipe
Claudia Hendrix
,
Brett A. Campbell
,
Benjamin Tittle
,
Luke A. Johnson
,
Kenneth B. Baker
,
Matthew D. Johnson
,
Gregory F. Molnar
,
Jerrold L. Vitek
·
YOU?
·
· 2018
· Open Access
·
· DOI: https://doi.org/10.1152/jn.00306.2018
YOU?
·
· 2018
· Open Access
·
· DOI: https://doi.org/10.1152/jn.00306.2018
Many studies suggest that Parkinson’s disease (PD) is associated with changes in neuronal activity patterns throughout the basal ganglia-thalamocortical motor circuit. There are limited electrophysiological data, however, describing how parkinsonism impacts the presupplementary motor area (pre-SMA) and SMA proper (SMAp), cortical areas known to be involved in movement planning and motor control. In this study, local field potentials (LFPs) were recorded in the pre-SMA/SMAp of a nonhuman primate during a visually cued reaching task. Recordings were made in the same subject in both the naive and parkinsonian state using the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of parkinsonism. We found that in the naive animal, well before a go-cue providing instruction of reach onset and direction was given, LFP activity was dynamically modulated in both high (20–30 Hz) and low beta (10–20 Hz) bands, and the magnitude of this modulation (e.g., decrease/increase in beta amplitude for each band, respectively) correlated linearly with reaction time (RT) on a trial-to-trial basis, suggesting it may predictively encode for RT. Consistent with this hypothesis, we observed that this activity was more prominent within the pre-SMA compared with SMAp. In the parkinsonian state, however, pre-SMA/SMAp beta band modulation was disrupted, particularly in the high beta band, such that the predictive encoding of RT was significantly diminished. In addition, the predictive encoding of RT preferentially within pre-SMA over SMAp was lost. These findings add to our understanding of the role of pre-SMA/SMAp in motor behavior and suggest a fundamental role of these cortical areas in early preparatory and premovement processes that are altered in parkinsonism. NEW & NOTEWORTHY Goal-directed movements, such as reaching for an object, necessitate temporal preparation and organization of information processing within the basal ganglia-thalamocortical motor network. Impaired movement in parkinsonism is thought to be the result of pathophysiological activity disrupting information flow within this network. This work provides neurophysiological evidence linking altered motor preplanning processes encoded in pre-SMA/SMAp beta band modulation to the pathogenesis of motor disturbances in parkinsonism.
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- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1152/jn.00306.2018
- https://journals.physiology.org/doi/pdf/10.1152/jn.00306.2018
- OA Status
- bronze
- Cited By
- 17
- References
- 77
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W2807618198
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
-
https://openalex.org/W2807618198Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.1152/jn.00306.2018Digital Object Identifier
- Title
-
Predictive encoding of motor behavior in the supplementary motor area is disrupted in parkinsonismWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2018Year of publication
- Publication date
-
2018-06-06Full publication date if available
- Authors
-
Claudia Hendrix, Brett A. Campbell, Benjamin Tittle, Luke A. Johnson, Kenneth B. Baker, Matthew D. Johnson, Gregory F. Molnar, Jerrold L. VitekList of authors in order
- Landing page
-
https://doi.org/10.1152/jn.00306.2018Publisher landing page
- PDF URL
-
https://journals.physiology.org/doi/pdf/10.1152/jn.00306.2018Direct link to full text PDF
- Open access
-
YesWhether a free full text is available
- OA status
-
bronzeOpen access status per OpenAlex
- OA URL
-
https://journals.physiology.org/doi/pdf/10.1152/jn.00306.2018Direct OA link when available
- Concepts
-
SMA*, Neuroscience, Supplementary motor area, Parkinsonism, Local field potential, Motor area, Psychology, Basal ganglia, Electrophysiology, Primate, Central nervous system, Medicine, Computer science, Disease, Internal medicine, Functional magnetic resonance imaging, AlgorithmTop concepts (fields/topics) attached by OpenAlex
- Cited by
-
17Total citation count in OpenAlex
- Citations by year (recent)
-
2025: 3, 2024: 2, 2023: 1, 2022: 1, 2021: 4Per-year citation counts (last 5 years)
- References (count)
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77Number of works referenced by this work
- Related works (count)
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10Other works algorithmically related by OpenAlex
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| abstract_inverted_index.more | 172 |
| abstract_inverted_index.over | 217 |
| abstract_inverted_index.role | 229, 239 |
| abstract_inverted_index.same | 79 |
| abstract_inverted_index.such | 197, 260 |
| abstract_inverted_index.that | 3, 96, 168, 198, 250 |
| abstract_inverted_index.this | 53, 134, 164, 169, 297 |
| abstract_inverted_index.time | 149 |
| abstract_inverted_index.well | 101 |
| abstract_inverted_index.were | 59, 75 |
| abstract_inverted_index.with | 9, 147, 163, 178 |
| abstract_inverted_index.work | 300 |
| abstract_inverted_index.& | 256 |
| abstract_inverted_index.SMAp. | 179 |
| abstract_inverted_index.There | 21 |
| abstract_inverted_index.These | 221 |
| abstract_inverted_index.areas | 41, 243 |
| abstract_inverted_index.band, | 143, 196 |
| abstract_inverted_index.basal | 17, 276 |
| abstract_inverted_index.data, | 25 |
| abstract_inverted_index.early | 245 |
| abstract_inverted_index.field | 56 |
| abstract_inverted_index.found | 95 |
| abstract_inverted_index.known | 42 |
| abstract_inverted_index.local | 55 |
| abstract_inverted_index.lost. | 220 |
| abstract_inverted_index.model | 91 |
| abstract_inverted_index.motor | 19, 33, 50, 233, 278, 306, 319 |
| abstract_inverted_index.naive | 84, 99 |
| abstract_inverted_index.onset | 109 |
| abstract_inverted_index.reach | 108 |
| abstract_inverted_index.state | 87 |
| abstract_inverted_index.task. | 73 |
| abstract_inverted_index.these | 241 |
| abstract_inverted_index.using | 88 |
| abstract_inverted_index.(LFPs) | 58 |
| abstract_inverted_index.(e.g., | 136 |
| abstract_inverted_index.bands, | 129 |
| abstract_inverted_index.basis, | 154 |
| abstract_inverted_index.before | 102 |
| abstract_inverted_index.during | 68 |
| abstract_inverted_index.encode | 159 |
| abstract_inverted_index.given, | 113 |
| abstract_inverted_index.go-cue | 104 |
| abstract_inverted_index.proper | 38 |
| abstract_inverted_index.result | 289 |
| abstract_inverted_index.state, | 183 |
| abstract_inverted_index.study, | 54 |
| abstract_inverted_index.within | 174, 215, 274, 296 |
| abstract_inverted_index.(SMAp), | 39 |
| abstract_inverted_index.altered | 252, 305 |
| abstract_inverted_index.animal, | 100 |
| abstract_inverted_index.changes | 10 |
| abstract_inverted_index.disease | 5 |
| abstract_inverted_index.encoded | 309 |
| abstract_inverted_index.impacts | 30 |
| abstract_inverted_index.limited | 23 |
| abstract_inverted_index.linking | 304 |
| abstract_inverted_index.object, | 265 |
| abstract_inverted_index.pre-SMA | 176, 216 |
| abstract_inverted_index.primate | 67 |
| abstract_inverted_index.studies | 1 |
| abstract_inverted_index.subject | 80 |
| abstract_inverted_index.suggest | 2, 236 |
| abstract_inverted_index.thought | 285 |
| abstract_inverted_index.(10–20 | 127 |
| abstract_inverted_index.(20–30 | 122 |
| abstract_inverted_index.Impaired | 280 |
| abstract_inverted_index.activity | 13, 115, 170, 292 |
| abstract_inverted_index.behavior | 234 |
| abstract_inverted_index.circuit. | 20 |
| abstract_inverted_index.compared | 177 |
| abstract_inverted_index.control. | 51 |
| abstract_inverted_index.cortical | 40, 242 |
| abstract_inverted_index.encoding | 201, 211 |
| abstract_inverted_index.evidence | 303 |
| abstract_inverted_index.findings | 222 |
| abstract_inverted_index.however, | 26, 184 |
| abstract_inverted_index.involved | 45 |
| abstract_inverted_index.linearly | 146 |
| abstract_inverted_index.movement | 47, 281 |
| abstract_inverted_index.network. | 279, 298 |
| abstract_inverted_index.neuronal | 12 |
| abstract_inverted_index.nonhuman | 66 |
| abstract_inverted_index.observed | 167 |
| abstract_inverted_index.patterns | 14 |
| abstract_inverted_index.planning | 48 |
| abstract_inverted_index.provides | 301 |
| abstract_inverted_index.reaching | 72, 262 |
| abstract_inverted_index.reaction | 148 |
| abstract_inverted_index.recorded | 60 |
| abstract_inverted_index.temporal | 267 |
| abstract_inverted_index.visually | 70 |
| abstract_inverted_index.(pre-SMA) | 35 |
| abstract_inverted_index.addition, | 208 |
| abstract_inverted_index.amplitude | 140 |
| abstract_inverted_index.direction | 111 |
| abstract_inverted_index.magnitude | 132 |
| abstract_inverted_index.modulated | 118 |
| abstract_inverted_index.processes | 249, 308 |
| abstract_inverted_index.prominent | 173 |
| abstract_inverted_index.providing | 105 |
| abstract_inverted_index.Consistent | 162 |
| abstract_inverted_index.NOTEWORTHY | 257 |
| abstract_inverted_index.Recordings | 74 |
| abstract_inverted_index.associated | 8 |
| abstract_inverted_index.correlated | 145 |
| abstract_inverted_index.describing | 27 |
| abstract_inverted_index.disrupted, | 190 |
| abstract_inverted_index.disrupting | 293 |
| abstract_inverted_index.modulation | 135, 188, 314 |
| abstract_inverted_index.movements, | 259 |
| abstract_inverted_index.potentials | 57 |
| abstract_inverted_index.predictive | 200, 210 |
| abstract_inverted_index.processing | 273 |
| abstract_inverted_index.suggesting | 155 |
| abstract_inverted_index.throughout | 15 |
| abstract_inverted_index.diminished. | 206 |
| abstract_inverted_index.dynamically | 117 |
| abstract_inverted_index.fundamental | 238 |
| abstract_inverted_index.hypothesis, | 165 |
| abstract_inverted_index.information | 272, 294 |
| abstract_inverted_index.instruction | 106 |
| abstract_inverted_index.necessitate | 266 |
| abstract_inverted_index.premovement | 248 |
| abstract_inverted_index.preparation | 268 |
| abstract_inverted_index.preparatory | 246 |
| abstract_inverted_index.preplanning | 307 |
| abstract_inverted_index.disturbances | 320 |
| abstract_inverted_index.organization | 270 |
| abstract_inverted_index.parkinsonian | 86, 182 |
| abstract_inverted_index.parkinsonism | 29, 283 |
| abstract_inverted_index.particularly | 191 |
| abstract_inverted_index.pathogenesis | 317 |
| abstract_inverted_index.pre-SMA/SMAp | 63, 185, 231, 311 |
| abstract_inverted_index.predictively | 158 |
| abstract_inverted_index.Goal-directed | 258 |
| abstract_inverted_index.Parkinson’s | 4 |
| abstract_inverted_index.parkinsonism. | 93, 254, 322 |
| abstract_inverted_index.respectively) | 144 |
| abstract_inverted_index.significantly | 205 |
| abstract_inverted_index.understanding | 226 |
| abstract_inverted_index.preferentially | 214 |
| abstract_inverted_index.trial-to-trial | 153 |
| abstract_inverted_index.presupplementary | 32 |
| abstract_inverted_index.decrease/increase | 137 |
| abstract_inverted_index.neurophysiological | 302 |
| abstract_inverted_index.pathophysiological | 291 |
| abstract_inverted_index.electrophysiological | 24 |
| abstract_inverted_index.ganglia-thalamocortical | 18, 277 |
| abstract_inverted_index.1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine | 90 |
| cited_by_percentile_year.max | 97 |
| cited_by_percentile_year.min | 89 |
| corresponding_author_ids | https://openalex.org/A5047447270 |
| countries_distinct_count | 1 |
| institutions_distinct_count | 8 |
| corresponding_institution_ids | https://openalex.org/I130238516 |
| citation_normalized_percentile.value | 0.82958711 |
| citation_normalized_percentile.is_in_top_1_percent | False |
| citation_normalized_percentile.is_in_top_10_percent | False |