Modulatory Effects of Motor State During Paired Associative Stimulation on Motor Cortex Excitability and Motor Skill Learning

Repeated pairing of electrical stimulation of a peripheral nerve with transcranial magnetic stimulation (TMS) over the primary motor cortex (M1) representation for a target muscle can induce neuroplastic adaptations in the human brain related to motor learning. The extent to which the motor state du...

Full description

Bibliographic Details
Main Authors: Jacqueline A. Palmer, Alice Halter, Whitney Gray, Steven L. Wolf, Michael R. Borich
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-01-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2019.00008/full
_version_ 1817989944267767808
author Jacqueline A. Palmer
Alice Halter
Whitney Gray
Steven L. Wolf
Steven L. Wolf
Michael R. Borich
author_facet Jacqueline A. Palmer
Alice Halter
Whitney Gray
Steven L. Wolf
Steven L. Wolf
Michael R. Borich
author_sort Jacqueline A. Palmer
collection DOAJ
description Repeated pairing of electrical stimulation of a peripheral nerve with transcranial magnetic stimulation (TMS) over the primary motor cortex (M1) representation for a target muscle can induce neuroplastic adaptations in the human brain related to motor learning. The extent to which the motor state during this form of paired associative stimulation (PAS) influences the degree and mechanisms of neuroplasticity or motor learning is unclear. Here, we investigated the effect of volitional muscle contraction during PAS on: (1) measures of general corticomotor excitability and intracortical circuit excitability; and (2) motor performance and learning. We assessed measures of corticomotor excitability using TMS and motor skill performance during a serial reaction time task (SRTT) at baseline and at 0, 30, 60 min post-PAS. Participants completed a SRTT retention test 1 week following the first two PAS sessions. Following the PAS intervention where the hand muscle maintained an active muscle contraction (PASACTIVE), there was lower short interval intracortical inhibition compared to PAS during a resting motor state (PASREST) and a sham PAS condition (PASCONTROL). SRTT performance improved within the session regardless of PAS condition. SRTT retention was greater following both PASACTIVE and PASREST after 1 week compared to PASCONTROL. These findings suggest that PAS may enhance motor learning retention and that motor state may be used to target different neural mechanisms of intracortical excitation and inhibition during PAS. This observation may be important to consider for the use of therapeutic noninvasive brain stimulation in neurologic patient populations.
first_indexed 2024-04-14T00:53:48Z
format Article
id doaj.art-ab24004c2a614a738e2176350b8d714e
institution Directory Open Access Journal
issn 1662-5161
language English
last_indexed 2024-04-14T00:53:48Z
publishDate 2019-01-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Human Neuroscience
spelling doaj.art-ab24004c2a614a738e2176350b8d714e2022-12-22T02:21:42ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612019-01-011310.3389/fnhum.2019.00008420567Modulatory Effects of Motor State During Paired Associative Stimulation on Motor Cortex Excitability and Motor Skill LearningJacqueline A. Palmer0Alice Halter1Whitney Gray2Steven L. Wolf3Steven L. Wolf4Michael R. Borich5Department of Rehabilitation Medicine, Division of Physical Therapy, Emory University, Atlanta, GA, United StatesDepartment of Rehabilitation Medicine, Division of Physical Therapy, Emory University, Atlanta, GA, United StatesDepartment of Rehabilitation Medicine, Division of Physical Therapy, Emory University, Atlanta, GA, United StatesDepartment of Rehabilitation Medicine, Division of Physical Therapy, Emory University, Atlanta, GA, United StatesAtlanta VA Health Care System Visual and Neurocognitive Center of Excellence, Decatur, GA, United StatesDepartment of Rehabilitation Medicine, Division of Physical Therapy, Emory University, Atlanta, GA, United StatesRepeated pairing of electrical stimulation of a peripheral nerve with transcranial magnetic stimulation (TMS) over the primary motor cortex (M1) representation for a target muscle can induce neuroplastic adaptations in the human brain related to motor learning. The extent to which the motor state during this form of paired associative stimulation (PAS) influences the degree and mechanisms of neuroplasticity or motor learning is unclear. Here, we investigated the effect of volitional muscle contraction during PAS on: (1) measures of general corticomotor excitability and intracortical circuit excitability; and (2) motor performance and learning. We assessed measures of corticomotor excitability using TMS and motor skill performance during a serial reaction time task (SRTT) at baseline and at 0, 30, 60 min post-PAS. Participants completed a SRTT retention test 1 week following the first two PAS sessions. Following the PAS intervention where the hand muscle maintained an active muscle contraction (PASACTIVE), there was lower short interval intracortical inhibition compared to PAS during a resting motor state (PASREST) and a sham PAS condition (PASCONTROL). SRTT performance improved within the session regardless of PAS condition. SRTT retention was greater following both PASACTIVE and PASREST after 1 week compared to PASCONTROL. These findings suggest that PAS may enhance motor learning retention and that motor state may be used to target different neural mechanisms of intracortical excitation and inhibition during PAS. This observation may be important to consider for the use of therapeutic noninvasive brain stimulation in neurologic patient populations.https://www.frontiersin.org/article/10.3389/fnhum.2019.00008/fulltranscranial magnetic stimulationpaired associative stimulationmotor learningcortical excitabilityplasticitymotor cortex
spellingShingle Jacqueline A. Palmer
Alice Halter
Whitney Gray
Steven L. Wolf
Steven L. Wolf
Michael R. Borich
Modulatory Effects of Motor State During Paired Associative Stimulation on Motor Cortex Excitability and Motor Skill Learning
Frontiers in Human Neuroscience
transcranial magnetic stimulation
paired associative stimulation
motor learning
cortical excitability
plasticity
motor cortex
title Modulatory Effects of Motor State During Paired Associative Stimulation on Motor Cortex Excitability and Motor Skill Learning
title_full Modulatory Effects of Motor State During Paired Associative Stimulation on Motor Cortex Excitability and Motor Skill Learning
title_fullStr Modulatory Effects of Motor State During Paired Associative Stimulation on Motor Cortex Excitability and Motor Skill Learning
title_full_unstemmed Modulatory Effects of Motor State During Paired Associative Stimulation on Motor Cortex Excitability and Motor Skill Learning
title_short Modulatory Effects of Motor State During Paired Associative Stimulation on Motor Cortex Excitability and Motor Skill Learning
title_sort modulatory effects of motor state during paired associative stimulation on motor cortex excitability and motor skill learning
topic transcranial magnetic stimulation
paired associative stimulation
motor learning
cortical excitability
plasticity
motor cortex
url https://www.frontiersin.org/article/10.3389/fnhum.2019.00008/full
work_keys_str_mv AT jacquelineapalmer modulatoryeffectsofmotorstateduringpairedassociativestimulationonmotorcortexexcitabilityandmotorskilllearning
AT alicehalter modulatoryeffectsofmotorstateduringpairedassociativestimulationonmotorcortexexcitabilityandmotorskilllearning
AT whitneygray modulatoryeffectsofmotorstateduringpairedassociativestimulationonmotorcortexexcitabilityandmotorskilllearning
AT stevenlwolf modulatoryeffectsofmotorstateduringpairedassociativestimulationonmotorcortexexcitabilityandmotorskilllearning
AT stevenlwolf modulatoryeffectsofmotorstateduringpairedassociativestimulationonmotorcortexexcitabilityandmotorskilllearning
AT michaelrborich modulatoryeffectsofmotorstateduringpairedassociativestimulationonmotorcortexexcitabilityandmotorskilllearning