Mapping functional gradients of the striatal circuit using simultaneous microelectric stimulation and ultrahigh-field fMRI in non-human primates

Mapping functional gradients of the striatal circuit using simultaneous microelectric stimulation and ultrahigh-field fMRI in non-human primates

Advances in functional magnetic resonance imaging (fMRI) have significantly enhanced our understanding of the striatal system of both humans and non-human primates (NHP) over the last few decades. However, its circuit-level functional anatomy remains poorly understood, partly because in-vivo fMRI ca...

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Bibliographic Details
Published in:NeuroImage (Orlando, Fla.) Vol. 236; p. 118077
Main Authors: Han, Min-Jun, Park, Chan-Ung, Kang, Sangyun, Kim, Byounghoon, Nikolaidis, Aki, Milham, Michael P., Hong, Seok Jun, Kim, Seong-Gi, Baeg, Eunha
Format: Journal Article
Language:English
Published: United States Elsevier Inc 01-08-2021
Elsevier Limited
Elsevier
Subjects:
7 tesla
Animals
Blood
Brain mapping
Brain Mapping - methods
CBV-fMRI
Corpus Striatum - diagnostic imaging
Corpus Striatum - physiology
Electric Stimulation
Electrical microstimulation
Electrodes
Embedding
Functional anatomy
Functional magnetic resonance imaging
Gradient
Laboratory animals
Macaca mulatta - physiology
Magnetic Resonance Imaging
Male
Neostriatum
Neural networks
Neuroimaging
Non-human primates
Oxygen saturation
Putamen
Spatial discrimination
Striatum
Surgery
Thalamus
United States > US
Germany
CBV-fMRI
Striatum
Gradient
Electrical microstimulation
Non-human primates
7 tesla
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Summary:Advances in functional magnetic resonance imaging (fMRI) have significantly enhanced our understanding of the striatal system of both humans and non-human primates (NHP) over the last few decades. However, its circuit-level functional anatomy remains poorly understood, partly because in-vivo fMRI cannot directly perturb a brain system and map its casual input-output relationship. Also, routine 3T fMRI has an insufficient spatial resolution. We performed electrical microstimulation (EM) of the striatum in lightly-anesthetized NHPs while simultaneously mapping whole-brain activation, using contrast-enhanced fMRI at ultra-high-field 7T. By stimulating multiple positions along the striatum's main (dorsal-to-ventral) axis, we revealed its complex functional circuit concerning mutually connected subsystems in both cortical and subcortical areas. Indeed, within the striatum, there were distinct brain activation patterns across different stimulation sites. Specifically, dorsal stimulation revealed a medial-to-lateral elongated shape of activation in upper caudate and putamen areas, whereas ventral stimulation evoked areas confined to the medial and lower caudate. Such dorsoventral gradients also appeared in neocortical and thalamic activations, indicating consistent embedding profiles of the striatal system across the whole brain. These findings reflect different forms of within-circuit and inter-regional neuronal connectivity between the dorsal and ventromedial striatum. These patterns both shared and contrasted with previous anatomical tract-tracing and in-vivo resting-state fMRI studies. Our approach of combining microstimulation and whole-brain fMRI mapping in NHPs provides a unique opportunity to integrate our understanding of a targeted brain area's meso- and macro-scale functional systems.
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ISSN:1053-8119
1095-9572
DOI:10.1016/j.neuroimage.2021.118077