Connectivity-Based Functional Analysis of Dopamine Release in the Striatum Using Diffusion-Weighted MRI and Positron Emission Tomography
The striatum acts in conjunction with the cortex to control and execute functions that are impaired by abnormal dopamine neurotransmission in disorders such as Parkinson's and schizophrenia. To date, in vivo quantification of striatal dopamine has been restricted to structure-based striatal sub...
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| Published in | Cerebral cortex (New York, N.Y. 1991) Vol. 24; no. 5; pp. 1165 - 1177 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Oxford University Press
01.05.2014
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1047-3211 1460-2199 1460-2199 |
| DOI | 10.1093/cercor/bhs397 |
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| Abstract | The striatum acts in conjunction with the cortex to control and execute functions that are impaired by abnormal dopamine neurotransmission in disorders such as Parkinson's and schizophrenia. To date, in vivo quantification of striatal dopamine has been restricted to structure-based striatal subdivisions. Here, we present a multimodal imaging approach that quantifies the endogenous dopamine release following the administration of d-amphetamine in the functional subdivisions of the striatum of healthy humans with [(11)C]PHNO and [(11)C]Raclopride positron emission tomography ligands. Using connectivity-based (CB) parcellation, we subdivided the striatum into functional subregions based on striato-cortical anatomical connectivity information derived from diffusion magnetic resonance imaging (MRI) and probabilistic tractography. Our parcellation showed that the functional organization of the striatum was spatially coherent across individuals, congruent with primate data and previous diffusion MRI studies, with distinctive and overlapping networks. d-amphetamine induced the highest dopamine release in the limbic followed by the sensory, motor, and executive areas. The data suggest that the relative regional proportions of D2-like receptors are unlikely to be responsible for this regional dopamine release pattern. Notably, the homogeneity of dopamine release was significantly higher within the CB functional subdivisions in comparison with the structural subdivisions. These results support an association between local levels of dopamine release and cortical connectivity fingerprints. |
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| AbstractList | The striatum acts in conjunction with the cortex to control and execute functions that are impaired by abnormal dopamine neurotransmission in disorders such as Parkinson's and schizophrenia. To date, in vivo quantification of striatal dopamine has been restricted to structure-based striatal subdivisions. Here, we present a multimodal imaging approach that quantifies the endogenous dopamine release following the administration of d-amphetamine in the functional subdivisions of the striatum of healthy humans with [(11)C]PHNO and [(11)C]Raclopride positron emission tomography ligands. Using connectivity-based (CB) parcellation, we subdivided the striatum into functional subregions based on striato-cortical anatomical connectivity information derived from diffusion magnetic resonance imaging (MRI) and probabilistic tractography. Our parcellation showed that the functional organization of the striatum was spatially coherent across individuals, congruent with primate data and previous diffusion MRI studies, with distinctive and overlapping networks. d-amphetamine induced the highest dopamine release in the limbic followed by the sensory, motor, and executive areas. The data suggest that the relative regional proportions of D2-like receptors are unlikely to be responsible for this regional dopamine release pattern. Notably, the homogeneity of dopamine release was significantly higher within the CB functional subdivisions in comparison with the structural subdivisions. These results support an association between local levels of dopamine release and cortical connectivity fingerprints.The striatum acts in conjunction with the cortex to control and execute functions that are impaired by abnormal dopamine neurotransmission in disorders such as Parkinson's and schizophrenia. To date, in vivo quantification of striatal dopamine has been restricted to structure-based striatal subdivisions. Here, we present a multimodal imaging approach that quantifies the endogenous dopamine release following the administration of d-amphetamine in the functional subdivisions of the striatum of healthy humans with [(11)C]PHNO and [(11)C]Raclopride positron emission tomography ligands. Using connectivity-based (CB) parcellation, we subdivided the striatum into functional subregions based on striato-cortical anatomical connectivity information derived from diffusion magnetic resonance imaging (MRI) and probabilistic tractography. Our parcellation showed that the functional organization of the striatum was spatially coherent across individuals, congruent with primate data and previous diffusion MRI studies, with distinctive and overlapping networks. d-amphetamine induced the highest dopamine release in the limbic followed by the sensory, motor, and executive areas. The data suggest that the relative regional proportions of D2-like receptors are unlikely to be responsible for this regional dopamine release pattern. Notably, the homogeneity of dopamine release was significantly higher within the CB functional subdivisions in comparison with the structural subdivisions. These results support an association between local levels of dopamine release and cortical connectivity fingerprints. The striatum acts in conjunction with the cortex to control and execute functions that are impaired by abnormal dopamine neurotransmission in disorders such as Parkinson's and schizophrenia. To date, in vivo quantification of striatal dopamine has been restricted to structure-based striatal subdivisions. Here, we present a multimodal imaging approach that quantifies the endogenous dopamine release following the administration of d -amphetamine in the functional subdivisions of the striatum of healthy humans with [ 11 C]PHNO and [ 11 C]Raclopride positron emission tomography ligands. Using connectivity-based (CB) parcellation, we subdivided the striatum into functional subregions based on striato-cortical anatomical connectivity information derived from diffusion magnetic resonance imaging (MRI) and probabilistic tractography. Our parcellation showed that the functional organization of the striatum was spatially coherent across individuals, congruent with primate data and previous diffusion MRI studies, with distinctive and overlapping networks. d -amphetamine induced the highest dopamine release in the limbic followed by the sensory, motor, and executive areas. The data suggest that the relative regional proportions of D2-like receptors are unlikely to be responsible for this regional dopamine release pattern. Notably, the homogeneity of dopamine release was significantly higher within the CB functional subdivisions in comparison with the structural subdivisions. These results support an association between local levels of dopamine release and cortical connectivity fingerprints. The striatum acts in conjunction with the cortex to control and execute functions that are impaired by abnormal dopamine neurotransmission in disorders such as Parkinson's and schizophrenia. To date, in vivo quantification of striatal dopamine has been restricted to structure-based striatal subdivisions. Here, we present a multimodal imaging approach that quantifies the endogenous dopamine release following the administration of d-amphetamine in the functional subdivisions of the striatum of healthy humans with [ super(11)C]PHNO and [ super(11)C]Raclopride positron emission tomography ligands. Using connectivity-based (CB) parcellation, we subdivided the striatum into functional subregions based on striato-cortical anatomical connectivity information derived from diffusion magnetic resonance imaging (MRI) and probabilistic tractography. Our parcellation showed that the functional organization of the striatum was spatially coherent across individuals, congruent with primate data and previous diffusion MRI studies, with distinctive and overlapping networks. d-amphetamine induced the highest dopamine release in the limbic followed by the sensory, motor, and executive areas. The data suggest that the relative regional proportions of D2-like receptors are unlikely to be responsible for this regional dopamine release pattern. Notably, the homogeneity of dopamine release was significantly higher within the CB functional subdivisions in comparison with the structural subdivisions. These results support an association between local levels of dopamine release and cortical connectivity fingerprints. The striatum acts in conjunction with the cortex to control and execute functions that are impaired by abnormal dopamine neurotransmission in disorders such as Parkinson's and schizophrenia. To date, in vivo quantification of striatal dopamine has been restricted to structure-based striatal subdivisions. Here, we present a multimodal imaging approach that quantifies the endogenous dopamine release following the administration of d-amphetamine in the functional subdivisions of the striatum of healthy humans with [(11)C]PHNO and [(11)C]Raclopride positron emission tomography ligands. Using connectivity-based (CB) parcellation, we subdivided the striatum into functional subregions based on striato-cortical anatomical connectivity information derived from diffusion magnetic resonance imaging (MRI) and probabilistic tractography. Our parcellation showed that the functional organization of the striatum was spatially coherent across individuals, congruent with primate data and previous diffusion MRI studies, with distinctive and overlapping networks. d-amphetamine induced the highest dopamine release in the limbic followed by the sensory, motor, and executive areas. The data suggest that the relative regional proportions of D2-like receptors are unlikely to be responsible for this regional dopamine release pattern. Notably, the homogeneity of dopamine release was significantly higher within the CB functional subdivisions in comparison with the structural subdivisions. These results support an association between local levels of dopamine release and cortical connectivity fingerprints. |
| Author | Tsoumpas, Charalampos Douaud, Gwenaelle Rabiner, Eugenii A. Searle, Graham E. Jenkinson, Mark Long, Christopher J. Haber, Suzanne N. Shotbolt, Paul Behrens, Timothy E. J. Tziortzi, Andri C. Jbabdi, Saad Gunn, Roger N. |
| AuthorAffiliation | 3 GlaxoSmithKline Clinical Imaging Centre , Hammersmith Hospital , London , UK 1 FMRIB Centre, Nuffield Department of Clinical Neurosciences 4 School of Medicine and Dentistry , University of Rochester , Rochester , USA 6 Department of Medicine , Imperial College London , London , UK 5 Division of Imaging Sciences and Biomedical Engineering , King's College London , London , UK and 2 Department of Engineering Science , University of Oxford , Oxford , UK |
| AuthorAffiliation_xml | – name: 5 Division of Imaging Sciences and Biomedical Engineering , King's College London , London , UK and – name: 2 Department of Engineering Science , University of Oxford , Oxford , UK – name: 3 GlaxoSmithKline Clinical Imaging Centre , Hammersmith Hospital , London , UK – name: 4 School of Medicine and Dentistry , University of Rochester , Rochester , USA – name: 1 FMRIB Centre, Nuffield Department of Clinical Neurosciences – name: 6 Department of Medicine , Imperial College London , London , UK |
| Author_xml | – sequence: 1 givenname: Andri C. surname: Tziortzi fullname: Tziortzi, Andri C. – sequence: 2 givenname: Suzanne N. surname: Haber fullname: Haber, Suzanne N. – sequence: 3 givenname: Graham E. surname: Searle fullname: Searle, Graham E. – sequence: 4 givenname: Charalampos surname: Tsoumpas fullname: Tsoumpas, Charalampos – sequence: 5 givenname: Christopher J. surname: Long fullname: Long, Christopher J. – sequence: 6 givenname: Paul surname: Shotbolt fullname: Shotbolt, Paul – sequence: 7 givenname: Gwenaelle surname: Douaud fullname: Douaud, Gwenaelle – sequence: 8 givenname: Saad surname: Jbabdi fullname: Jbabdi, Saad – sequence: 9 givenname: Timothy E. J. surname: Behrens fullname: Behrens, Timothy E. J. – sequence: 10 givenname: Eugenii A. surname: Rabiner fullname: Rabiner, Eugenii A. – sequence: 11 givenname: Mark surname: Jenkinson fullname: Jenkinson, Mark – sequence: 12 givenname: Roger N. surname: Gunn fullname: Gunn, Roger N. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23283687$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com 2012 |
| Copyright_xml | – notice: The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com 2012 |
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| SubjectTerms | Adult Brain Mapping Corpus Striatum - diagnostic imaging Corpus Striatum - drug effects Corpus Striatum - metabolism Diffusion Tensor Imaging Dopamine - metabolism Dopamine Antagonists - pharmacokinetics Dopamine Antagonists - pharmacology Executive Function - physiology Humans Male Middle Aged Nerve Net - diagnostic imaging Nerve Net - drug effects Nerve Net - metabolism Positron-Emission Tomography Primates Probability Raclopride - pharmacokinetics Raclopride - pharmacology |
| Title | Connectivity-Based Functional Analysis of Dopamine Release in the Striatum Using Diffusion-Weighted MRI and Positron Emission Tomography |
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