Combining Brain Perturbation and Neuroimaging in Non-human Primates

P Christiaan Klink; Jean-François Aubry; Vincent P Ferrera; Andrew S Fox; Sean Froudist-Walsh; Bechir Jarraya; Elisa Konofagou; Richard Krauzlis; Adam Messinger; Anna S Mitchell; Michael Ortiz-Rios; Hiroyuki Oya; Angela C Roberts; Anna Wang Roe; Matthew F S Rushworth; Jérôme Sallet; Michael Christoph Schmid; Charles E Schroeder; Jordy Tasserie; Doris Tsao; Lynn Uhrig; Wim Vanduffel; Melanie Wilke; Igor Kagan; Christopher I Petkov

doi:10.1016/j.neuroimage.2021.118017

Combining Brain Perturbation and Neuroimaging in Non-human Primates

P Christiaan Klink, Jean-François Aubry, Vincent P Ferrera, Andrew S Fox, Sean Froudist-Walsh, Bechir Jarraya, Elisa Konofagou, Richard Krauzlis, Adam Messinger, Anna S Mitchell, Michael Ortiz-Rios, Hiroyuki Oya, Angela C Roberts, Anna Wang Roe, Matthew F S Rushworth, Jérôme Sallet, Michael Christoph Schmid, Charles E Schroeder, Jordy Tasserie, Doris TsaoLynn Uhrig, Wim Vanduffel, Melanie Wilke, Igor Kagan, Christopher I Petkov

Netherlands Institute for Neuroscience (NIN)

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Abstract

Brain perturbation studies allow detailed causal inferences of behavioral and neural processes. Because the combination of brain perturbation methods and neural measurement techniques is inherently challenging, research in humans has predominantly focused on non-invasive, indirect brain perturbations, or neurological lesion studies. Non-human primates have been indispensable as a neurobiological system that is highly similar to humans while simultaneously being more experimentally tractable, allowing visualization of the functional and structural impact of systematic brain perturbation. This review considers the state of the art in non-human primate brain perturbation with a focus on approaches that can be combined with neuroimaging. We consider both non-reversible (lesions) and reversible or temporary perturbations such as electrical, pharmacological, optical, optogenetic, chemogenetic, pathway-selective, and ultrasound based interference methods. Method-specific considerations from the research and development community are offered to facilitate research in this field and support further innovations. We conclude by identifying novel avenues for further research and innovation and by highlighting the clinical translational potential of the methods.

Original language	English
Pages (from-to)	118017
Journal	NeuroImage
Volume	235
DOIs	https://doi.org/10.1016/j.neuroimage.2021.118017
Publication status	Published - Mar 2021

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Klink, P. C., Aubry, J-F., Ferrera, V. P., Fox, A. S., Froudist-Walsh, S., Jarraya, B., Konofagou, E., Krauzlis, R., Messinger, A., Mitchell, A. S., Ortiz-Rios, M., Oya, H., Roberts, A. C., Roe, A. W., Rushworth, M. F. S., Sallet, J., Schmid, M. C., Schroeder, C. E., Tasserie, J., ... Petkov, C. I. (2021). Combining Brain Perturbation and Neuroimaging in Non-human Primates. NeuroImage, 235, 118017. https://doi.org/10.1016/j.neuroimage.2021.118017

Klink, P Christiaan ; Aubry, Jean-François ; Ferrera, Vincent P ; Fox, Andrew S ; Froudist-Walsh, Sean ; Jarraya, Bechir ; Konofagou, Elisa ; Krauzlis, Richard ; Messinger, Adam ; Mitchell, Anna S ; Ortiz-Rios, Michael ; Oya, Hiroyuki ; Roberts, Angela C ; Roe, Anna Wang ; Rushworth, Matthew F S ; Sallet, Jérôme ; Schmid, Michael Christoph ; Schroeder, Charles E ; Tasserie, Jordy ; Tsao, Doris ; Uhrig, Lynn ; Vanduffel, Wim ; Wilke, Melanie ; Kagan, Igor ; Petkov, Christopher I. / Combining Brain Perturbation and Neuroimaging in Non-human Primates. In: NeuroImage. 2021 ; Vol. 235. pp. 118017.

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title = "Combining Brain Perturbation and Neuroimaging in Non-human Primates",

abstract = "Brain perturbation studies allow detailed causal inferences of behavioral and neural processes. Because the combination of brain perturbation methods and neural measurement techniques is inherently challenging, research in humans has predominantly focused on non-invasive, indirect brain perturbations, or neurological lesion studies. Non-human primates have been indispensable as a neurobiological system that is highly similar to humans while simultaneously being more experimentally tractable, allowing visualization of the functional and structural impact of systematic brain perturbation. This review considers the state of the art in non-human primate brain perturbation with a focus on approaches that can be combined with neuroimaging. We consider both non-reversible (lesions) and reversible or temporary perturbations such as electrical, pharmacological, optical, optogenetic, chemogenetic, pathway-selective, and ultrasound based interference methods. Method-specific considerations from the research and development community are offered to facilitate research in this field and support further innovations. We conclude by identifying novel avenues for further research and innovation and by highlighting the clinical translational potential of the methods.",

author = "Klink, {P Christiaan} and Jean-Fran{\c c}ois Aubry and Ferrera, {Vincent P} and Fox, {Andrew S} and Sean Froudist-Walsh and Bechir Jarraya and Elisa Konofagou and Richard Krauzlis and Adam Messinger and Mitchell, {Anna S} and Michael Ortiz-Rios and Hiroyuki Oya and Roberts, {Angela C} and Roe, {Anna Wang} and Rushworth, {Matthew F S} and J{\'e}r{\^o}me Sallet and Schmid, {Michael Christoph} and Schroeder, {Charles E} and Jordy Tasserie and Doris Tsao and Lynn Uhrig and Wim Vanduffel and Melanie Wilke and Igor Kagan and Petkov, {Christopher I}",

note = "Copyright {\textcopyright} 2021. Published by Elsevier Inc.",

year = "2021",

month = mar,

doi = "10.1016/j.neuroimage.2021.118017",

language = "English",

volume = "235",

pages = "118017",

journal = "NeuroImage",

issn = "1053-8119",

publisher = "Academic Press",

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Klink, PC, Aubry, J-F, Ferrera, VP, Fox, AS, Froudist-Walsh, S, Jarraya, B, Konofagou, E, Krauzlis, R, Messinger, A, Mitchell, AS, Ortiz-Rios, M, Oya, H, Roberts, AC, Roe, AW, Rushworth, MFS, Sallet, J, Schmid, MC, Schroeder, CE, Tasserie, J, Tsao, D, Uhrig, L, Vanduffel, W, Wilke, M, Kagan, I & Petkov, CI 2021, 'Combining Brain Perturbation and Neuroimaging in Non-human Primates', NeuroImage, vol. 235, pp. 118017. https://doi.org/10.1016/j.neuroimage.2021.118017

Combining Brain Perturbation and Neuroimaging in Non-human Primates. / Klink, P Christiaan; Aubry, Jean-François; Ferrera, Vincent P; Fox, Andrew S; Froudist-Walsh, Sean; Jarraya, Bechir; Konofagou, Elisa; Krauzlis, Richard; Messinger, Adam; Mitchell, Anna S; Ortiz-Rios, Michael; Oya, Hiroyuki; Roberts, Angela C; Roe, Anna Wang; Rushworth, Matthew F S; Sallet, Jérôme; Schmid, Michael Christoph; Schroeder, Charles E; Tasserie, Jordy; Tsao, Doris; Uhrig, Lynn; Vanduffel, Wim; Wilke, Melanie; Kagan, Igor; Petkov, Christopher I.

In: NeuroImage, Vol. 235, 03.2021, p. 118017.

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

TY - JOUR

T1 - Combining Brain Perturbation and Neuroimaging in Non-human Primates

AU - Klink, P Christiaan

AU - Aubry, Jean-François

AU - Ferrera, Vincent P

AU - Fox, Andrew S

AU - Froudist-Walsh, Sean

AU - Jarraya, Bechir

AU - Konofagou, Elisa

AU - Krauzlis, Richard

AU - Messinger, Adam

AU - Mitchell, Anna S

AU - Ortiz-Rios, Michael

AU - Oya, Hiroyuki

AU - Roberts, Angela C

AU - Roe, Anna Wang

AU - Rushworth, Matthew F S

AU - Sallet, Jérôme

AU - Schmid, Michael Christoph

AU - Schroeder, Charles E

AU - Tasserie, Jordy

AU - Tsao, Doris

AU - Uhrig, Lynn

AU - Vanduffel, Wim

AU - Wilke, Melanie

AU - Kagan, Igor

AU - Petkov, Christopher I

PY - 2021/3

Y1 - 2021/3

N2 - Brain perturbation studies allow detailed causal inferences of behavioral and neural processes. Because the combination of brain perturbation methods and neural measurement techniques is inherently challenging, research in humans has predominantly focused on non-invasive, indirect brain perturbations, or neurological lesion studies. Non-human primates have been indispensable as a neurobiological system that is highly similar to humans while simultaneously being more experimentally tractable, allowing visualization of the functional and structural impact of systematic brain perturbation. This review considers the state of the art in non-human primate brain perturbation with a focus on approaches that can be combined with neuroimaging. We consider both non-reversible (lesions) and reversible or temporary perturbations such as electrical, pharmacological, optical, optogenetic, chemogenetic, pathway-selective, and ultrasound based interference methods. Method-specific considerations from the research and development community are offered to facilitate research in this field and support further innovations. We conclude by identifying novel avenues for further research and innovation and by highlighting the clinical translational potential of the methods.

AB - Brain perturbation studies allow detailed causal inferences of behavioral and neural processes. Because the combination of brain perturbation methods and neural measurement techniques is inherently challenging, research in humans has predominantly focused on non-invasive, indirect brain perturbations, or neurological lesion studies. Non-human primates have been indispensable as a neurobiological system that is highly similar to humans while simultaneously being more experimentally tractable, allowing visualization of the functional and structural impact of systematic brain perturbation. This review considers the state of the art in non-human primate brain perturbation with a focus on approaches that can be combined with neuroimaging. We consider both non-reversible (lesions) and reversible or temporary perturbations such as electrical, pharmacological, optical, optogenetic, chemogenetic, pathway-selective, and ultrasound based interference methods. Method-specific considerations from the research and development community are offered to facilitate research in this field and support further innovations. We conclude by identifying novel avenues for further research and innovation and by highlighting the clinical translational potential of the methods.

U2 - 10.1016/j.neuroimage.2021.118017

DO - 10.1016/j.neuroimage.2021.118017

M3 - Article

C2 - 33794355

VL - 235

SP - 118017

JO - NeuroImage

JF - NeuroImage

SN - 1053-8119

ER -

Combining Brain Perturbation and Neuroimaging in Non-human Primates

Abstract

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