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Alteration of functional connectivity in the cortex and major brain networks of non-human primates following focused ultrasound exposure.

ABSTRACT: Focused ultrasound (FUS) is a non-invasive neuromodulation technology that is being investigated for potential treatment of neurological and psychiatric disorders. Focused ultrasound combined with microbubbles can temporarily open the intact blood-brain barrier (BBB) of animals and humans, and facilitate drug delivery. FUS exposure, either with or without microbubbles, has been demonstrated to alter the behavior of non-human primates, and previous work has demonstrated transient and long-term effects of FUS neuromodulation on functional connectivity using resting state functional MRI. However, it is unknown whether opening the BBB affects functional connectivity differently than FUS alone. Thus we applied FUS alone (neuromodulation) and FUS with microbubbles (BBB opening) in the dorsal striatum of lightly anesthetized non-human primates, and compared changes in functional connectivity in major brain networks. We found different alteration patterns between FUS neuromodulation and FUS-mediated BBB opening in several cortical areas, and we also found that applying FUS to a deep brain structure can alter functional connectivity in the default mode network and frontotemporal network.

SUBMITTER: Liu D

PROVIDER: S-EPMC9949083 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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Alteration of functional connectivity in the cortex and major brain networks of non-human primates following focused ultrasound exposure.

Liu D D Munoz F F Sanatkhani S S Pouliopoulos A N AN Konofagou E E Grinband J J Vp Ferrera F

bioRxiv : the preprint server for biology 20230216

Focused ultrasound (FUS) is a non-invasive neuromodulation technology that is being investigated for potential treatment of neurological and psychiatric disorders. Focused ultrasound combined with microbubbles can temporarily open the intact blood-brain barrier (BBB) of animals and humans, and facilitate drug delivery. FUS exposure, either with or without microbubbles, has been demonstrated to alter the behavior of non-human primates, and previous work has demonstrated transient and long-term ef ...[more]

PMID: 36824864

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Project description:BackgroundFocused ultrasound (FUS) is a non-invasive neuromodulation technology that is being investigated for potential treatment of neurological and psychiatric disorders. FUS combined with microbubbles can temporarily open the intact blood-brain barrier (BBB) of animals and humans, and facilitate drug delivery. FUS exposure, either with or without microbubbles, has been demonstrated to alter the behavior of non-human primates (NHP), and previous studies have demonstrated the transient and long-term effects of FUS neuromodulation on functional connectivity using resting state functional MRI. The behavioral effects of FUS vary depending on whether or not it is applied in conjunction with microbubbles to open the BBB, but it is unknown whether opening the BBB affects functional connectivity differently than FUS alone.ObjectiveTo compare the effects of applying FUS alone (FUS neuromodulation) and FUS with microbubbles (FUS-BBB opening) on changes of resting state functional connectivity in NHP.MethodsWe applied 2 min FUS exposure without (neuromodulation) and with microbubbles (BBB opening) in the dorsal striatum of lightly anesthetized non-human primates, and acquired resting state functional MRI 40 min respectively after FUS exposure. The functional connectivity (FC) in the cortex and major brain networks between the two approaches were measured and compared.ResultsWhen applying FUS exposure to the caudate nucleus of NHP, we found that both FUS neuromodulation can activate FC between caudate and insular cortex, while inhibiting the FC between caudate and motor cortex. FUS-BBB opening can activate FC between the caudate and medial prefrontal cortex, and within the frontotemporal network (FTN). We also found both FUS and FUS-BBB opening can significantly activate FC within the default mode network (DMN).ConclusionThe results suggest applying FUS to a deep brain structure can alter functional connectivity in the DMN and FTN, and that FUS neuromodulation and FUS-mediated BBB opening can have different effects on patterns of functional connectivity.

Project description:Pain engages multiple brain networks, with the thalamus serving as a critical subcortical hub. This study aims to explore the effects of low-intensity transcranial focused ultrasound-induced suppression on the organization of thalamocortical nociceptive networks. We employed MR-guided focused ultrasound, a potential non-invasive therapy, with real-time ultrasound beam localization feedback and fMRI monitoring. We first functionally identified the focused ultrasound target at the thalamic ventroposterior lateral nucleus by mapping the whole-brain blood oxygenation level-dependent responses to nociceptive heat stimulation of the hand using fMRI in each individual macaque monkey under light anaesthesia. The blood oxygenation level-dependent fMRI signals from the heat-responsive thalamic ventroposterior lateral nucleus were analysed to derive thalamocortical effective functional connectivity network using the psychophysical interaction method. Nineteen cortical regions across sensorimotor, cognitive, associative and limbic networks exhibited strong effective functional connectivity to the thalamic ventroposterior lateral during heat nociceptive processing. Focused ultrasound-induced suppression of heat activity in the thalamic ventroposterior lateral nucleus altered nociceptive responses in most of the 19 regions. Data-driven hierarchical clustering analyses of blood oxygenation level-dependent time courses across all thalamocortical region-of-interest pairs identified two effective functional connectivity subnetworks. The concurrent suppression of thalamic heat response with focused ultrasound reorganized these subnetworks and modified thalamocortical connection strength. Our findings suggest that the thalamic ventroposterior lateral nucleus has extensive and causal connections to a wide array of cortical areas during nociceptive processing. The combination of MR-guided focused ultrasound with fMRI enables precise dissection and modulation of nociceptive networks in the brain, a capability that no other device-based neuromodulation methods have achieved. This presents a promising non-invasive tool for modulating pain networks with profound clinical relevance. The robust modulation of nociceptive effective functional connectivity networks by focused ultrasound strongly supports the thalamic ventroposterior lateral as a viable target for pain management strategies.

Dataset Information

Alteration of functional connectivity in the cortex and major brain networks of non-human primates following focused ultrasound exposure.

Publications

Alteration of functional connectivity in the cortex and major brain networks of non-human primates following focused ultrasound exposure.

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