Temporal Profile of Descending Cortical Modulation of Spinal Excitability: Group and Individual-Specific Effects

Sensorimotor control is modulated through complex interactions between descending corticomotor pathways and ascending sensory inputs. Pairing sub-threshold transcranial magnetic stimulation (TMS) with peripheral nerve stimulation (PNS) modulates the Hoffmann’s reflex (H-reflex), providing a neurophy...

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Main Authors: Jiang Xu, Alejandro J. Lopez, Maruf M. Hoque, Michael R. Borich, Trisha M. Kesar
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-01-01
Series:Frontiers in Integrative Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnint.2021.777741/full
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author Jiang Xu
Jiang Xu
Alejandro J. Lopez
Alejandro J. Lopez
Maruf M. Hoque
Michael R. Borich
Trisha M. Kesar
author_facet Jiang Xu
Jiang Xu
Alejandro J. Lopez
Alejandro J. Lopez
Maruf M. Hoque
Michael R. Borich
Trisha M. Kesar
author_sort Jiang Xu
collection DOAJ
description Sensorimotor control is modulated through complex interactions between descending corticomotor pathways and ascending sensory inputs. Pairing sub-threshold transcranial magnetic stimulation (TMS) with peripheral nerve stimulation (PNS) modulates the Hoffmann’s reflex (H-reflex), providing a neurophysiologic probe into the influence of descending cortical drive on spinal segmental circuits. However, individual variability in the timing and magnitude of H-reflex modulation is poorly understood. Here, we varied the inter-stimulus interval (ISI) between TMS and PNS to systematically manipulate the relative timing of convergence of descending TMS-induced volleys with respect to ascending PNS-induced afferent volleys in the spinal cord to: (1) characterize effective connectivity between the primary motor cortex (M1) and spinal circuits, mediated by both direct, fastest-conducting, and indirect, slower-conducting descending pathways; and (2) compare the effect of individual-specific vs. standard ISIs. Unconditioned and TMS-conditioned H-reflexes (24 different ISIs ranging from −6 to 12 ms) were recorded from the soleus muscle in 10 able-bodied individuals. The magnitude of H-reflex modulation at individualized ISIs (earliest facilitation delay or EFD and individual-specific peak facilitation) was compared with standard ISIs. Our results revealed a significant effect of ISI on H-reflex modulation. ISIs eliciting earliest-onset facilitation (EFD 0 ms) ranged from −3 to −5 ms across individuals. No difference in the magnitude of facilitation was observed at EFD 0 ms vs. a standardized short-interval ISI of −1.5 ms. Peak facilitation occurred at longer ISIs, ranging from +3 to +11 ms. The magnitude of H-reflex facilitation derived using an individual-specific peak facilitation was significantly larger than facilitation observed at a standardized longer-interval ISI of +10 ms. Our results suggest that unique insights can be provided with individual-specific measures of top-down effective connectivity mediated by direct and/or fastest-conducting pathways (indicated by the magnitude of facilitation observed at EFD 0 ms) and other descending pathways that encompass relatively slower and/or indirect connections from M1 to spinal circuits (indicated by peak facilitation and facilitation at longer ISIs). By comprehensively characterizing the temporal profile and inter-individual variability of descending modulation of spinal reflexes, our findings provide methodological guidelines and normative reference values to inform future studies on neurophysiological correlates of the complex array of descending neural connections between M1 and spinal circuits.
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spelling doaj.art-e40dd464637041e593de1fdbf09b7be02022-12-22T01:34:16ZengFrontiers Media S.A.Frontiers in Integrative Neuroscience1662-51452022-01-011510.3389/fnint.2021.777741777741Temporal Profile of Descending Cortical Modulation of Spinal Excitability: Group and Individual-Specific EffectsJiang Xu0Jiang Xu1Alejandro J. Lopez2Alejandro J. Lopez3Maruf M. Hoque4Michael R. Borich5Trisha M. Kesar6Department of Rehabilitation Medicine, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaDivision of Physical Therapy, Department of Rehabilitation Medicine, Emory University, Atlanta, GA, United StatesDivision of Physical Therapy, Department of Rehabilitation Medicine, Emory University, Atlanta, GA, United StatesNeuroscience Graduate Program, Graduate Division of Biological and Biomedical Sciences, Emory University, Atlanta, GA, United StatesDivision of Physical Therapy, Department of Rehabilitation Medicine, Emory University, Atlanta, GA, United StatesDivision of Physical Therapy, Department of Rehabilitation Medicine, Emory University, Atlanta, GA, United StatesDivision of Physical Therapy, Department of Rehabilitation Medicine, Emory University, Atlanta, GA, United StatesSensorimotor control is modulated through complex interactions between descending corticomotor pathways and ascending sensory inputs. Pairing sub-threshold transcranial magnetic stimulation (TMS) with peripheral nerve stimulation (PNS) modulates the Hoffmann’s reflex (H-reflex), providing a neurophysiologic probe into the influence of descending cortical drive on spinal segmental circuits. However, individual variability in the timing and magnitude of H-reflex modulation is poorly understood. Here, we varied the inter-stimulus interval (ISI) between TMS and PNS to systematically manipulate the relative timing of convergence of descending TMS-induced volleys with respect to ascending PNS-induced afferent volleys in the spinal cord to: (1) characterize effective connectivity between the primary motor cortex (M1) and spinal circuits, mediated by both direct, fastest-conducting, and indirect, slower-conducting descending pathways; and (2) compare the effect of individual-specific vs. standard ISIs. Unconditioned and TMS-conditioned H-reflexes (24 different ISIs ranging from −6 to 12 ms) were recorded from the soleus muscle in 10 able-bodied individuals. The magnitude of H-reflex modulation at individualized ISIs (earliest facilitation delay or EFD and individual-specific peak facilitation) was compared with standard ISIs. Our results revealed a significant effect of ISI on H-reflex modulation. ISIs eliciting earliest-onset facilitation (EFD 0 ms) ranged from −3 to −5 ms across individuals. No difference in the magnitude of facilitation was observed at EFD 0 ms vs. a standardized short-interval ISI of −1.5 ms. Peak facilitation occurred at longer ISIs, ranging from +3 to +11 ms. The magnitude of H-reflex facilitation derived using an individual-specific peak facilitation was significantly larger than facilitation observed at a standardized longer-interval ISI of +10 ms. Our results suggest that unique insights can be provided with individual-specific measures of top-down effective connectivity mediated by direct and/or fastest-conducting pathways (indicated by the magnitude of facilitation observed at EFD 0 ms) and other descending pathways that encompass relatively slower and/or indirect connections from M1 to spinal circuits (indicated by peak facilitation and facilitation at longer ISIs). By comprehensively characterizing the temporal profile and inter-individual variability of descending modulation of spinal reflexes, our findings provide methodological guidelines and normative reference values to inform future studies on neurophysiological correlates of the complex array of descending neural connections between M1 and spinal circuits.https://www.frontiersin.org/articles/10.3389/fnint.2021.777741/fulltranscranial magnetic stimulation (TMS)spinal reflex excitabilitylower extremity musclesinter-stimulus interval (ISI)corticospinal pathways
spellingShingle Jiang Xu
Jiang Xu
Alejandro J. Lopez
Alejandro J. Lopez
Maruf M. Hoque
Michael R. Borich
Trisha M. Kesar
Temporal Profile of Descending Cortical Modulation of Spinal Excitability: Group and Individual-Specific Effects
Frontiers in Integrative Neuroscience
transcranial magnetic stimulation (TMS)
spinal reflex excitability
lower extremity muscles
inter-stimulus interval (ISI)
corticospinal pathways
title Temporal Profile of Descending Cortical Modulation of Spinal Excitability: Group and Individual-Specific Effects
title_full Temporal Profile of Descending Cortical Modulation of Spinal Excitability: Group and Individual-Specific Effects
title_fullStr Temporal Profile of Descending Cortical Modulation of Spinal Excitability: Group and Individual-Specific Effects
title_full_unstemmed Temporal Profile of Descending Cortical Modulation of Spinal Excitability: Group and Individual-Specific Effects
title_short Temporal Profile of Descending Cortical Modulation of Spinal Excitability: Group and Individual-Specific Effects
title_sort temporal profile of descending cortical modulation of spinal excitability group and individual specific effects
topic transcranial magnetic stimulation (TMS)
spinal reflex excitability
lower extremity muscles
inter-stimulus interval (ISI)
corticospinal pathways
url https://www.frontiersin.org/articles/10.3389/fnint.2021.777741/full
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