Plasticity and Spontaneous Activity Pulses in Disused Human Brain Circuits

Dillan J Newbold; Timothy O Laumann; Catherine R Hoyt; Jacqueline M Hampton; David F Montez; Ryan V Raut; Mario Ortega; Anish Mitra; Ashley N Nielsen; Derek B Miller; Babatunde Adeyemo; Annie L Nguyen; Kristen M Scheidter; Aaron B Tanenbaum; Andrew N Van; Scott Marek; Bradley L Schlaggar; Alexandre R Carter; Deanna J Greene; Evan M Gordon; Marcus E Raichle; Steven E Petersen; Abraham Z Snyder; Nico U F Dosenbach

doi:10.1016/j.neuron.2020.05.007

Plasticity and Spontaneous Activity Pulses in Disused Human Brain Circuits

Neuron. 2020 Aug 5;107(3):580-589.e6. doi: 10.1016/j.neuron.2020.05.007. Epub 2020 Jun 16.

Authors

Dillan J Newbold¹, Timothy O Laumann², Catherine R Hoyt³, Jacqueline M Hampton², David F Montez⁴, Ryan V Raut⁵, Mario Ortega⁶, Anish Mitra⁷, Ashley N Nielsen⁸, Derek B Miller⁶, Babatunde Adeyemo⁶, Annie L Nguyen⁶, Kristen M Scheidter⁶, Aaron B Tanenbaum⁶, Andrew N Van⁹, Scott Marek⁶, Bradley L Schlaggar¹⁰, Alexandre R Carter¹¹, Deanna J Greene¹², Evan M Gordon¹³, Marcus E Raichle¹⁴, Steven E Petersen¹⁵, Abraham Z Snyder¹⁴, Nico U F Dosenbach¹⁶

Affiliations

¹ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA. Electronic address: newbold@wustl.edu.
² Department of Psychiatry, Washington University School of Medicine, St. Louis, MO 63110, USA.
³ Program in Occupational Therapy, Washington University School of Medicine, St. Louis, MO 63110, USA.
⁴ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Psychiatry, Washington University School of Medicine, St. Louis, MO 63110, USA.
⁵ Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA.
⁶ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA.
⁷ Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Psychiatry, Stanford University, Stanford, CA 94305, USA.
⁸ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA; Institute for Innovations in Developmental Sciences, Northwestern University, Chicago, IL 60611, USA.
⁹ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Biomedical Engineering, Washington University in St. Louis, St. Louis, MO 63110, USA.
¹⁰ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA; Kennedy Krieger Institute, Baltimore, MD 21205, USA; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA; Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA.
¹¹ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA; Program in Occupational Therapy, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹² Department of Psychiatry, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹³ VISN 17 Center of Excellence for Research on Returning War Veterans, Waco, TX 76711, USA; Center for Vital Longevity, School of Behavioral and Brain Sciences, University of Texas at Dallas, Dallas, TX 75080, USA; Department of Psychology and Neuroscience, Baylor University, Waco, TX 76706, USA.
¹⁴ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA.
¹⁵ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Biomedical Engineering, Washington University in St. Louis, St. Louis, MO 63110, USA; Department of Neuroscience, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Psychological and Brain Sciences, Washington University in St. Louis, St. Louis, MO 63130, USA.
¹⁶ Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA; Program in Occupational Therapy, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Biomedical Engineering, Washington University in St. Louis, St. Louis, MO 63110, USA; Department of Pediatrics, Washington University School of Medicine, St. Louis, MO 63110, USA. Electronic address: dosenbachn@wustl.edu.

Abstract

To induce brain plasticity in humans, we casted the dominant upper extremity for 2 weeks and tracked changes in functional connectivity using daily 30-min scans of resting-state functional MRI (rs-fMRI). Casting caused cortical and cerebellar regions controlling the disused extremity to functionally disconnect from the rest of the somatomotor system, while internal connectivity within the disused sub-circuit was maintained. Functional disconnection was evident within 48 h, progressed throughout the cast period, and reversed after cast removal. During the cast period, large, spontaneous pulses of activity propagated through the disused somatomotor sub-circuit. The adult brain seems to rely on regular use to maintain its functional architecture. Disuse-driven spontaneous activity pulses may help preserve functionally disconnected sub-circuits.

Keywords: ALFF; amplitude of low-frequency fluctuations; cerebellum; disuse; fMRI; functional connectivity; plasticity; primary motor cortex; resting state; spontaneous activity; supplementary motor area.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Video-Audio Media

MeSH terms

Activities of Daily Living
Casts, Surgical
Female
Functional Laterality
Functional Neuroimaging
Humans
Magnetic Resonance Imaging
Male
Motor Cortex / diagnostic imaging*
Motor Cortex / physiology
Motor Skills / physiology
Muscle Strength / physiology
Neural Pathways / diagnostic imaging
Neural Pathways / physiology
Neuronal Plasticity / physiology*
Restraint, Physical*
Upper Extremity

Abstract

Publication types

MeSH terms

Grants and funding