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Single-trial decoding of movement intentions using functional ultrasound neuroimaging

Norman, Sumner L. and Maresca, David and Christopoulos, Vasileios N. and Griggs, Whitney S. and Demené, Charlie and Tanter, Mickaël and Shapiro, Mikhail G. and Andersen, Richard A. (2021) Single-trial decoding of movement intentions using functional ultrasound neuroimaging. Neuron, 109 (9). pp. 1554-1566. ISSN 0896-6273. PMCID PMC8105283. doi:10.1016/j.neuron.2021.03.003. https://resolver.caltech.edu/CaltechAUTHORS:20200515-085712838

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Abstract

New technologies are key to understanding the dynamic activity of neural circuits and systems in the brain. Here, we show that a minimally invasive approach based on ultrasound can be used to detect the neural correlates of movement planning, including directions and effectors. While non-human primates (NHPs) performed memory-guided movements, we used functional ultrasound (fUS) neuroimaging to record changes in cerebral blood volume with 100 μm resolution. We recorded from outside the dura above the posterior parietal cortex, a brain area important for spatial perception, multisensory integration, and movement planning. We then used fUS signals from the delay period before movement to decode the animals’ intended direction and effector. Single-trial decoding is a prerequisite to brain-machine interfaces, a key application that could benefit from this technology. These results are a critical step in the development of neuro-recording and brain interface tools that are less invasive, high resolution, and scalable.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.neuron.2021.03.003DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8105283PubMed CentralArticle
https://doi.org/10.1101/2020.05.12.086132DOIDiscussion Paper
ORCID:
AuthorORCID
Norman, Sumner L.0000-0001-9945-697X
Maresca, David0000-0002-4921-6406
Christopoulos, Vasileios N.0000-0002-0541-8700
Griggs, Whitney S.0000-0003-2941-6803
Demené, Charlie0000-0002-5329-700X
Tanter, Mickaël0000-0001-7739-8051
Shapiro, Mikhail G.0000-0002-0291-4215
Andersen, Richard A.0000-0002-7947-0472
Additional Information:© 2021 Elsevier Inc. Received 2 July 2020, Revised 29 December 2020, Accepted 1 March 2021, Available online 22 March 2021. We thank Kelsie Pejsa for assistance with animal care, surgeries, and training. We thank Thomas Deffieux for his contributions to the ultrasound neuroimaging methods that made this work possible. We thank Igor Kagan for assisting in implantation planning. We thank Charles Liu and Claire Rabut for helpful discussions. Finally, we thank Krissta Passanante for her illustrations. S.N. was supported by a Della Martin Postdoctoral Fellowship. D.M. was supported by a Human Frontiers Science Program Cross-Disciplinary Postdoctoral Fellowship (award LT000637/2016). W.G. was supported by the UCLA-Caltech MSTP (NIGMS T32 GM008042). This research was supported by the National Institute of Health BRAIN Initiative (grant U01NS099724 to M.G.S.), the T&C Chen Brain-machine Interface Center, and the Boswell Foundation (R.A.A.). Related research in the Shapiro lab is supported by the Heritage Medical Research Institute. Author contributions: S.L.N., D.M., V.N.C., M.T., M.G.S., and R.A.A. conceived the study; D.M. and C.D. established the imaging sequences; S.L.N., V.N.C., and W.G. trained the animals; S.L.N., V.N.C., D.M., and W.G. acquired the data; S.L.N., D.M., and V.N.C. performed the data processing; S.L.N., D.M., and V.N.C. drafted the manuscript with substantial contribution from M.G.S. and R.A.A., and all authors edited and approved the final version of the manuscript; M.T., M.G.S., and R.A.A. supervised the research. Declaration of interests: M.T. is a co-founder and shareholder of Iconeus Company, which commercializes ultrasonic neuroimaging scanners. D.M. is now affiliated with T.U. Delft, Netherlands. V.C. is now affiliated with University of California, Riverside.
Group:Heritage Medical Research Institute, Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
Della Martin FoundationUNSPECIFIED
Human Frontier Science ProgramLT000637/2016
NIH Predoctoral FellowshipT32 GM008042
NIHU01NS099724
Tianqiao and Chrissy Chen Institute for NeuroscienceUNSPECIFIED
James G. Boswell FoundationUNSPECIFIED
Heritage Medical Research InstituteUNSPECIFIED
Subject Keywords:functional ultrasound neuroimaging; single-trial decoding; movement planning; Brain-machine interface; Posterior parietal Cortex; Saccade; Reach; Non-human primate
Issue or Number:9
PubMed Central ID:PMC8105283
DOI:10.1016/j.neuron.2021.03.003
Record Number:CaltechAUTHORS:20200515-085712838
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200515-085712838
Official Citation:Sumner L. Norman, David Maresca, Vassilios N. Christopoulos, Whitney S. Griggs, Charlie Demene, Mickael Tanter, Mikhail G. Shapiro, Richard A. Andersen, Single-trial decoding of movement intentions using functional ultrasound neuroimaging, Neuron, Volume 109, Issue 9, 2021, Pages 1554-1566.e4, ISSN 0896-6273, https://doi.org/10.1016/j.neuron.2021.03.003.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:103226
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:15 May 2020 16:16
Last Modified:11 May 2022 21:17

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