Distinct neurochemical influences on fMRI response polarity in the striatum
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 and
Yen-Yu Ian Shih ()
Additional contact information
Domenic H. Cerri: the University of North Carolina at Chapel Hill
Daniel L. Albaugh: the University of North Carolina at Chapel Hill
Lindsay R. Walton: the University of North Carolina at Chapel Hill
Brittany Katz: the University of North Carolina at Chapel Hill
Tzu-Wen Wang: the University of North Carolina at Chapel Hill
Tzu-Hao Harry Chao: the University of North Carolina at Chapel Hill
Weiting Zhang: the University of North Carolina at Chapel Hill
Randal J. Nonneman: the University of North Carolina at Chapel Hill
Jing Jiang: Stanford University
Sung-Ho Lee: the University of North Carolina at Chapel Hill
Amit Etkin: Stanford University
Catherine N. Hall: University of Sussex
Garret D. Stuber: University of Washington
Yen-Yu Ian Shih: the University of North Carolina at Chapel Hill
Nature Communications, 2024, vol. 15, issue 1, 1-23
Abstract:
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.
Date: 2024
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DOI: 10.1038/s41467-024-46088-z
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