Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learning
Despite evidence that dopamine neurotransmission in the striatum is critical for learning as well as for movement control, little is yet known about how the learning-related dynamics of striatal activity are affected by dopamine depletion, a condition faced in Parkinson's disease. We made local...
| Autores: | , , , , , |
|---|---|
| Tipo de recurso: | artículo |
| Fecha de publicación: | 2013 |
| País: | España |
| Institución: | Universidad Camilo José Cela (UCJC) |
| Repositorio: | Depósito Digital e-UCJC |
| OAI Identifier: | oai:repositorio.ucjc.edu:20.500.12020/1228 |
| Acceso en línea: | https://www.jneurosci.org/content/33/11/4782 http://hdl.handle.net/20.500.12020/1228 https://doi.org/10.1523/JNEUROSCI.3746-12.2013 |
| Access Level: | acceso abierto |
| Palabra clave: | Biología Celular y Molecular Ciencias Biomédicas Dopamine Parkinson’s disease Striatum 24 Ciencias de la Vida 2490 Neurociencias |
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Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learningF. Hernandez, LediaKubota, YasuoHu, DanHowe, Mark WLemaire, NuneGraybiel, Ann MBiología Celular y MolecularCiencias BiomédicasDopamineParkinson’s diseaseStriatum24 Ciencias de la Vida2490 NeurocienciasDespite evidence that dopamine neurotransmission in the striatum is critical for learning as well as for movement control, little is yet known about how the learning-related dynamics of striatal activity are affected by dopamine depletion, a condition faced in Parkinson's disease. We made localized intrastriatal 6-hydroxydopamine lesions in rats and recorded within the dopamine-depleted sensorimotor striatal zone and its contralateral correspondent as the animals learned a conditional maze task. Rather than producing global, nonspecific elevations in firing rate across the task, the dopamine depletion altered striatal projection neuron activity and fast-spiking interneuron activity selectively, with sharply task-specific and cell type-specific effects, and often, with learning-stage selective effects as well. Striatal projection neurons with strong responses during the maze runs had especially elevated responsiveness during the maze runs. Projection neurons that, instead, fired most strongly before maze running showed elevated pre-start firing rates, but not during maze running, as learning progressed. The intrastriatal dopamine depletion severely affected the learning-related patterning of fast-spiking interneuron ensembles, especially during maze running and after extended training. Remarkably, L-DOPA treatment almost entirely reversed the depletion-induced elevations in pre-run firing of the projection neurons, and elevated their responses around start and end of maze runs. By contrast, L-DOPA failed to normalize fast-spiking interneuron activity. Thus the effects of striatal dopamine depletion and restoration on striatal activity are highly dependent not only on cell type, as previously shown, but also on the behavioral activity called for and the state of behavioral learning achieved.This work was funded by National Institutes of Health–National Institute of Neurological Disorders and Stroke P50 NS-38372, National Parkinson Foundation and Stanley H. and Sheila G. Sydney Fund to A.M.G., and Parkinson Disease Foundation Fellowship and Fulbright Fellowship to L.F.H.Society for Neuroscience2013info:eu-repo/semantics/articlehttps://www.jneurosci.org/content/33/11/4782https://www.jneurosci.org/content/33/11/4782http://hdl.handle.net/20.500.12020/1228https://doi.org/10.1523/JNEUROSCI.3746-12.2013reponame:Depósito Digital e-UCJCinstname:Universidad Camilo José Cela (UCJC)InglésNational Institutes of Health–National Institute of Neurological Disorders and Stroke P50 NS-38372info:eu-repo/semantics/openAccessoai:repositorio.ucjc.edu:20.500.12020/12282026-05-27T07:36:51Z |
| dc.title.none.fl_str_mv |
Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learning |
| title |
Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learning |
| spellingShingle |
Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learning F. Hernandez, Ledia Biología Celular y Molecular Ciencias Biomédicas Dopamine Parkinson’s disease Striatum 24 Ciencias de la Vida 2490 Neurociencias |
| title_short |
Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learning |
| title_full |
Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learning |
| title_fullStr |
Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learning |
| title_full_unstemmed |
Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learning |
| title_sort |
Selective effects of dopamine depletion on neuronal subpopulations in the sensorimotor striatum during procedural learning |
| dc.creator.none.fl_str_mv |
F. Hernandez, Ledia Kubota, Yasuo Hu, Dan Howe, Mark W Lemaire, Nune Graybiel, Ann M |
| author |
F. Hernandez, Ledia |
| author_facet |
F. Hernandez, Ledia Kubota, Yasuo Hu, Dan Howe, Mark W Lemaire, Nune Graybiel, Ann M |
| author_role |
author |
| author2 |
Kubota, Yasuo Hu, Dan Howe, Mark W Lemaire, Nune Graybiel, Ann M |
| author2_role |
author author author author author |
| dc.subject.none.fl_str_mv |
Biología Celular y Molecular Ciencias Biomédicas Dopamine Parkinson’s disease Striatum 24 Ciencias de la Vida 2490 Neurociencias |
| topic |
Biología Celular y Molecular Ciencias Biomédicas Dopamine Parkinson’s disease Striatum 24 Ciencias de la Vida 2490 Neurociencias |
| description |
Despite evidence that dopamine neurotransmission in the striatum is critical for learning as well as for movement control, little is yet known about how the learning-related dynamics of striatal activity are affected by dopamine depletion, a condition faced in Parkinson's disease. We made localized intrastriatal 6-hydroxydopamine lesions in rats and recorded within the dopamine-depleted sensorimotor striatal zone and its contralateral correspondent as the animals learned a conditional maze task. Rather than producing global, nonspecific elevations in firing rate across the task, the dopamine depletion altered striatal projection neuron activity and fast-spiking interneuron activity selectively, with sharply task-specific and cell type-specific effects, and often, with learning-stage selective effects as well. Striatal projection neurons with strong responses during the maze runs had especially elevated responsiveness during the maze runs. Projection neurons that, instead, fired most strongly before maze running showed elevated pre-start firing rates, but not during maze running, as learning progressed. The intrastriatal dopamine depletion severely affected the learning-related patterning of fast-spiking interneuron ensembles, especially during maze running and after extended training. Remarkably, L-DOPA treatment almost entirely reversed the depletion-induced elevations in pre-run firing of the projection neurons, and elevated their responses around start and end of maze runs. By contrast, L-DOPA failed to normalize fast-spiking interneuron activity. Thus the effects of striatal dopamine depletion and restoration on striatal activity are highly dependent not only on cell type, as previously shown, but also on the behavioral activity called for and the state of behavioral learning achieved. |
| publishDate |
2013 |
| dc.date.none.fl_str_mv |
2013 |
| dc.type.none.fl_str_mv |
info:eu-repo/semantics/article |
| format |
article |
| dc.identifier.none.fl_str_mv |
https://www.jneurosci.org/content/33/11/4782 https://www.jneurosci.org/content/33/11/4782 http://hdl.handle.net/20.500.12020/1228 https://doi.org/10.1523/JNEUROSCI.3746-12.2013 |
| url |
https://www.jneurosci.org/content/33/11/4782 http://hdl.handle.net/20.500.12020/1228 https://doi.org/10.1523/JNEUROSCI.3746-12.2013 |
| dc.language.none.fl_str_mv |
Inglés |
| language_invalid_str_mv |
Inglés |
| dc.relation.none.fl_str_mv |
National Institutes of Health–National Institute of Neurological Disorders and Stroke P50 NS-38372 |
| dc.rights.none.fl_str_mv |
info:eu-repo/semantics/openAccess |
| eu_rights_str_mv |
openAccess |
| dc.publisher.none.fl_str_mv |
Society for Neuroscience |
| publisher.none.fl_str_mv |
Society for Neuroscience |
| dc.source.none.fl_str_mv |
reponame:Depósito Digital e-UCJC instname:Universidad Camilo José Cela (UCJC) |
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Universidad Camilo José Cela (UCJC) |
| reponame_str |
Depósito Digital e-UCJC |
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Depósito Digital e-UCJC |
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1869425037699710976 |
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15.301603 |