Potentiation of cortico-spinal output via targeted electrical stimulation of the motor thalamus

Jonathan C. Ho, Erinn M. Grigsby, Arianna Damiani, Lucy Liang, Josep-Maria Balaguer, Sridula Kallakuri, Lilly W. Tang, Jessica Barrios-Martinez, Vahagn Karapetyan, Daryl Fields, Peter C. Gerszten, T. Kevin Hitchens, Theodora Constantine, Gregory M. Adams, Donald J. Crammond, Marco Capogrosso, Jorge A. Gonzalez-Martinez and Elvira Pirondini ()
Additional contact information
Jonathan C. Ho: University of Pittsburgh
Erinn M. Grigsby: University of Pittsburgh
Arianna Damiani: University of Pittsburgh
Lucy Liang: University of Pittsburgh
Josep-Maria Balaguer: University of Pittsburgh
Sridula Kallakuri: University of Pittsburgh
Lilly W. Tang: University of Pittsburgh
Jessica Barrios-Martinez: University of Pittsburgh
Vahagn Karapetyan: University of Pittsburgh
Daryl Fields: University of Pittsburgh
Peter C. Gerszten: University of Pittsburgh
T. Kevin Hitchens: University of Pittsburgh
Theodora Constantine: University of Pittsburgh
Gregory M. Adams: University of Pittsburgh
Donald J. Crammond: University of Pittsburgh
Marco Capogrosso: University of Pittsburgh
Jorge A. Gonzalez-Martinez: University of Pittsburgh
Elvira Pirondini: University of Pittsburgh

Nature Communications, 2024, vol. 15, issue 1, 1-21

Abstract: Abstract Cerebral white matter lesions prevent cortico-spinal descending inputs from effectively activating spinal motoneurons, leading to loss of motor control. However, in most cases, the damage to cortico-spinal axons is incomplete offering a potential target for therapies aimed at improving volitional muscle activation. Here we hypothesize that, by engaging direct excitatory connections to cortico-spinal motoneurons, stimulation of the motor thalamus could facilitate activation of surviving cortico-spinal fibers thereby immediately potentiating motor output. To test this hypothesis, we identify optimal thalamic targets and stimulation parameters that enhance upper-limb motor-evoked potentials and grip forces in anesthetized monkeys. This potentiation persists after white matter lesions. We replicate these results in humans during intra-operative testing. We then design a stimulation protocol that immediately improves strength and force control in a patient with a chronic white matter lesion. Our results show that electrical stimulation targeting surviving neural pathways can improve motor control after white matter lesions.

Date: 2024
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DOI: 10.1038/s41467-024-52477-1

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