Distinct neurochemical influences on fMRI response polarity in the striatum
Abstract The striatum, known as the input nucleus of the basal ganglia, is extensively studied for its diverse behavioral roles. However, the relationship between its neuronal and vascular activity, vital for interpreting functional magnetic resonance imaging (fMRI) signals, has not received compreh...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-03-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-46088-z |
| _version_ | 1827326792469315584 |
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| author | Domenic H. Cerri Daniel L. Albaugh Lindsay R. Walton Brittany Katz Tzu-Wen Wang Tzu-Hao Harry Chao Weiting Zhang Randal J. Nonneman Jing Jiang Sung-Ho Lee Amit Etkin Catherine N. Hall Garret D. Stuber Yen-Yu Ian Shih |
| author_facet | Domenic H. Cerri Daniel L. Albaugh Lindsay R. Walton Brittany Katz Tzu-Wen Wang Tzu-Hao Harry Chao Weiting Zhang Randal J. Nonneman Jing Jiang Sung-Ho Lee Amit Etkin Catherine N. Hall Garret D. Stuber Yen-Yu Ian Shih |
| author_sort | Domenic H. Cerri |
| collection | DOAJ |
| description | Abstract The striatum, known as the input nucleus of the basal ganglia, is extensively studied for its diverse behavioral roles. However, the relationship between its neuronal and vascular activity, vital for interpreting functional magnetic resonance imaging (fMRI) signals, has not received comprehensive examination within the striatum. Here, we demonstrate that optogenetic stimulation of dorsal striatal neurons or their afferents from various cortical and subcortical regions induces negative striatal fMRI responses in rats, manifesting as vasoconstriction. These responses occur even with heightened striatal neuronal activity, confirmed by electrophysiology and fiber-photometry. In parallel, midbrain dopaminergic neuron optogenetic modulation, coupled with electrochemical measurements, establishes a link between striatal vasodilation and dopamine release. Intriguingly, in vivo intra-striatal pharmacological manipulations during optogenetic stimulation highlight a critical role of opioidergic signaling in generating striatal vasoconstriction. This observation is substantiated by detecting striatal vasoconstriction in brain slices after synthetic opioid application. In humans, manipulations aimed at increasing striatal neuronal activity likewise elicit negative striatal fMRI responses. Our results emphasize the necessity of considering vasoactive neurotransmission alongside neuronal activity when interpreting fMRI signal. |
| first_indexed | 2024-03-07T14:50:38Z |
| format | Article |
| id | doaj.art-7f2843290a2d4421b7c9e76dab4e7dfd |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-07T14:50:38Z |
| publishDate | 2024-03-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-7f2843290a2d4421b7c9e76dab4e7dfd2024-03-05T19:41:57ZengNature PortfolioNature Communications2041-17232024-03-0115112310.1038/s41467-024-46088-zDistinct neurochemical influences on fMRI response polarity in the striatumDomenic H. Cerri0Daniel L. Albaugh1Lindsay R. Walton2Brittany Katz3Tzu-Wen Wang4Tzu-Hao Harry Chao5Weiting Zhang6Randal J. Nonneman7Jing Jiang8Sung-Ho Lee9Amit Etkin10Catherine N. Hall11Garret D. Stuber12Yen-Yu Ian Shih13Center for Animal MRI, the University of North Carolina at Chapel HillCenter for Animal MRI, the University of North Carolina at Chapel HillCenter for Animal MRI, the University of North Carolina at Chapel HillCenter for Animal MRI, the University of North Carolina at Chapel HillCenter for Animal MRI, the University of North Carolina at Chapel HillCenter for Animal MRI, the University of North Carolina at Chapel HillCenter for Animal MRI, the University of North Carolina at Chapel HillCenter for Animal MRI, the University of North Carolina at Chapel HillDepartment of Psychiatry and Behavioral Sciences, Stanford UniversityCenter for Animal MRI, the University of North Carolina at Chapel HillDepartment of Psychiatry and Behavioral Sciences, Stanford UniversitySussex Neuroscience, University of SussexCenter for Neurobiology of Addiction, Pain, and Emotion, University of WashingtonCenter for Animal MRI, the University of North Carolina at Chapel HillAbstract The striatum, known as the input nucleus of the basal ganglia, is extensively studied for its diverse behavioral roles. However, the relationship between its neuronal and vascular activity, vital for interpreting functional magnetic resonance imaging (fMRI) signals, has not received comprehensive examination within the striatum. Here, we demonstrate that optogenetic stimulation of dorsal striatal neurons or their afferents from various cortical and subcortical regions induces negative striatal fMRI responses in rats, manifesting as vasoconstriction. These responses occur even with heightened striatal neuronal activity, confirmed by electrophysiology and fiber-photometry. In parallel, midbrain dopaminergic neuron optogenetic modulation, coupled with electrochemical measurements, establishes a link between striatal vasodilation and dopamine release. Intriguingly, in vivo intra-striatal pharmacological manipulations during optogenetic stimulation highlight a critical role of opioidergic signaling in generating striatal vasoconstriction. This observation is substantiated by detecting striatal vasoconstriction in brain slices after synthetic opioid application. In humans, manipulations aimed at increasing striatal neuronal activity likewise elicit negative striatal fMRI responses. Our results emphasize the necessity of considering vasoactive neurotransmission alongside neuronal activity when interpreting fMRI signal.https://doi.org/10.1038/s41467-024-46088-z |
| spellingShingle | Domenic H. Cerri Daniel L. Albaugh Lindsay R. Walton Brittany Katz Tzu-Wen Wang Tzu-Hao Harry Chao Weiting Zhang Randal J. Nonneman Jing Jiang Sung-Ho Lee Amit Etkin Catherine N. Hall Garret D. Stuber Yen-Yu Ian Shih Distinct neurochemical influences on fMRI response polarity in the striatum Nature Communications |
| title | Distinct neurochemical influences on fMRI response polarity in the striatum |
| title_full | Distinct neurochemical influences on fMRI response polarity in the striatum |
| title_fullStr | Distinct neurochemical influences on fMRI response polarity in the striatum |
| title_full_unstemmed | Distinct neurochemical influences on fMRI response polarity in the striatum |
| title_short | Distinct neurochemical influences on fMRI response polarity in the striatum |
| title_sort | distinct neurochemical influences on fmri response polarity in the striatum |
| url | https://doi.org/10.1038/s41467-024-46088-z |
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