A tool for monitoring cell type-specific focused ultrasound neuromodulation and control of chronic epilepsy

Focused ultrasound (FUS) is a powerful tool for noninvasive modulation of deep brain activity with promising therapeutic potential for refractory epilepsy; however, tools for examining FUS effects on specific cell types within the deep brain do not yet exist. Consequently, how cell types within hete...

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 119; no. 46; p. e2206828119
Main Authors:	Murphy, Keith R, Farrell, Jordan S, Gomez, Juan L, Stedman, Quintin G, Li, Ningrui, Leung, Steven A, Good, Cameron H, Qiu, Zhihai, Firouzi, Kamyar, Butts Pauly, Kim, Khuri-Yakub, Butrus Pierre T, Michaelides, Michael, Soltesz, Ivan, de Lecea, Luis
Format:	Journal Article
Language:	English
Published:	United States National Academy of Sciences 15-11-2022
Subjects:	Animals Biological Sciences Brain Brain - diagnostic imaging Brain - physiology Epilepsy Epilepsy - therapy Epilepsy, Temporal Lobe Hippocampus Hippocampus - diagnostic imaging Interneurons Monitoring Neuroimaging Neuromodulation Parameter identification Parvalbumin Photometry Temporal lobe Ultrasonic imaging Ultrasonography Ultrasound epilepsy neuromodulation photometry neuroscience focused ultrasound
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Abstract	Focused ultrasound (FUS) is a powerful tool for noninvasive modulation of deep brain activity with promising therapeutic potential for refractory epilepsy; however, tools for examining FUS effects on specific cell types within the deep brain do not yet exist. Consequently, how cell types within heterogeneous networks can be modulated and whether parameters can be identified to bias these networks in the context of complex behaviors remains unknown. To address this, we developed a fiber Photometry Coupled focused Ultrasound System (PhoCUS) for simultaneously monitoring FUS effects on neural activity of subcortical genetically targeted cell types in freely behaving animals. We identified a parameter set that selectively increases activity of parvalbumin interneurons while suppressing excitatory neurons in the hippocampus. A net inhibitory effect localized to the hippocampus was further confirmed through whole brain metabolic imaging. Finally, these inhibitory selective parameters achieved significant spike suppression in the kainate model of chronic temporal lobe epilepsy, opening the door for future noninvasive therapies.
AbstractList	Focused ultrasound (FUS) is a powerful tool for noninvasive modulation of deep brain activity with promising therapeutic potential for refractory epilepsy; however, tools for examining FUS effects on specific cell types within the deep brain do not yet exist. Consequently, how cell types within heterogeneous networks can be modulated and whether parameters can be identified to bias these networks in the context of complex behaviors remains unknown. To address this, we developed a fiber Photometry Coupled focused Ultrasound System (PhoCUS) for simultaneously monitoring FUS effects on neural activity of subcortical genetically targeted cell types in freely behaving animals. We identified a parameter set that selectively increases activity of parvalbumin interneurons while suppressing excitatory neurons in the hippocampus. A net inhibitory effect localized to the hippocampus was further confirmed through whole brain metabolic imaging. Finally, these inhibitory selective parameters achieved significant spike suppression in the kainate model of chronic temporal lobe epilepsy, opening the door for future noninvasive therapies. Focused ultrasound (FUS) is a powerful tool for noninvasive modulation of deep brain activity with promising therapeutic potential for refractory epilepsy; however, tools for examining FUS effects on specific cell types within the deep brain do not yet exist. Consequently, how cell types within heterogeneous networks can be modulated and whether parameters can be identified to bias these networks in the context of complex behaviors remains unknown. To address this, we developed a fiber Photometry Coupled focused Ultrasound System (PhoCUS) for simultaneously monitoring FUS effects on neural activity of subcortical genetically targeted cell types in freely behaving animals. We identified a parameter set that selectively increases activity of parvalbumin interneurons while suppressing excitatory neurons in the hippocampus. A net inhibitory effect localized to the hippocampus was further confirmed through whole brain metabolic imaging. Finally, these inhibitory selective parameters achieved significant spike suppression in the kainate model of chronic temporal lobe epilepsy, opening the door for future noninvasive therapies.Focused ultrasound (FUS) is a powerful tool for noninvasive modulation of deep brain activity with promising therapeutic potential for refractory epilepsy; however, tools for examining FUS effects on specific cell types within the deep brain do not yet exist. Consequently, how cell types within heterogeneous networks can be modulated and whether parameters can be identified to bias these networks in the context of complex behaviors remains unknown. To address this, we developed a fiber Photometry Coupled focused Ultrasound System (PhoCUS) for simultaneously monitoring FUS effects on neural activity of subcortical genetically targeted cell types in freely behaving animals. We identified a parameter set that selectively increases activity of parvalbumin interneurons while suppressing excitatory neurons in the hippocampus. A net inhibitory effect localized to the hippocampus was further confirmed through whole brain metabolic imaging. Finally, these inhibitory selective parameters achieved significant spike suppression in the kainate model of chronic temporal lobe epilepsy, opening the door for future noninvasive therapies. Ultrasound can be focused through skull onto the deep brain, altering neural activity noninvasively. Despite its broad utility, the action of focused ultrasound on specific cell types is almost entirely unknown. Understanding cell type–specific responses to FUS would allow selection of ultrasound waveforms that engage the intended targets while limiting effects on off-target fields. We developed a system combining FUS targeting and optical recording of virally labeled deep brain cell types in freely behaving animals. We used the tool to identify a protocol for the hippocampus that selectively increases inhibitory neural activity while decreasing excitatory activity with high spatial specificity. The protocol robustly suppressed epileptiforms in a chronic epilepsy model demonstrating the tool’s potential for examining experimental FUS therapies. Focused ultrasound (FUS) is a powerful tool for noninvasive modulation of deep brain activity with promising therapeutic potential for refractory epilepsy; however, tools for examining FUS effects on specific cell types within the deep brain do not yet exist. Consequently, how cell types within heterogeneous networks can be modulated and whether parameters can be identified to bias these networks in the context of complex behaviors remains unknown. To address this, we developed a fiber Photometry Coupled focused Ultrasound System (PhoCUS) for simultaneously monitoring FUS effects on neural activity of subcortical genetically targeted cell types in freely behaving animals. We identified a parameter set that selectively increases activity of parvalbumin interneurons while suppressing excitatory neurons in the hippocampus. A net inhibitory effect localized to the hippocampus was further confirmed through whole brain metabolic imaging. Finally, these inhibitory selective parameters achieved significant spike suppression in the kainate model of chronic temporal lobe epilepsy, opening the door for future noninvasive therapies.
Author	de Lecea, Luis Firouzi, Kamyar Gomez, Juan L Soltesz, Ivan Farrell, Jordan S Butts Pauly, Kim Leung, Steven A Khuri-Yakub, Butrus Pierre T Michaelides, Michael Murphy, Keith R Qiu, Zhihai Stedman, Quintin G Good, Cameron H Li, Ningrui
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Copyright	Copyright National Academy of Sciences Nov 15, 2022 Copyright © 2022 the Author(s). Published by PNAS. 2022
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Keywords	epilepsy neuromodulation photometry neuroscience focused ultrasound
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contributions: K.R.M., J.S.F., J.L.G., C.H.G., Z.Q., K.B.P., B.P.T.K.-Y., M.M., I.S., and L.d.L. designed research; K.R.M., J.S.F., J.L.G., N.L., S.A.L., C.H.G., and K.F. performed research; K.R.M., Q.G.S., B.P.T.K.-Y., and L.d.L. contributed new reagents/analytic tools; K.R.M., J.S.F., J.L.G., N.L., S.A.L., and K.F. analyzed data; and K.R.M., J.S.F., J.L.G., Q.G.S., C.H.G., K.B.P., B.P.T.K.-Y., M.M., I.S., and L.d.L. wrote the paper. Edited by Marcus Raichle, Washington University of School of Medicine, Mallinckrodt Institute of Radiology and Department of Neurology, St. Louis, MO; received April 19, 2022; accepted September 16, 2022
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Snippet	Focused ultrasound (FUS) is a powerful tool for noninvasive modulation of deep brain activity with promising therapeutic potential for refractory epilepsy;... Ultrasound can be focused through skull onto the deep brain, altering neural activity noninvasively. Despite its broad utility, the action of focused...
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SubjectTerms	Animals Biological Sciences Brain Brain - diagnostic imaging Brain - physiology Epilepsy Epilepsy - therapy Epilepsy, Temporal Lobe Hippocampus Hippocampus - diagnostic imaging Interneurons Monitoring Neuroimaging Neuromodulation Parameter identification Parvalbumin Photometry Temporal lobe Ultrasonic imaging Ultrasonography Ultrasound
Title	A tool for monitoring cell type-specific focused ultrasound neuromodulation and control of chronic epilepsy
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