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Distinct neurochemical influences on fMRI response polarity in the striatum
Journal article   Open access   Peer reviewed

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, …
Nature communications, Vol.15(1), 1916
03/01/2024
DOI: 10.1038/s41467-024-46088-z
PMCID: PMC10907631
PMID: 38429266
url
https://doi.org/10.1038/s41467-024-46088-zView
Published (Version of record) Open Access

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.

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