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Measuring and Manipulating Functionally Specific Neural Pathways in the Human Motor System with Transcranial Magnetic Stimulation

Understanding interactions between brain areas is important for the study of goal-directed behavior. Functional neuroimaging of brain connectivity has ...

University of Michigan

Unimanual grasp movements with mirrored visual feedback (MVF) can improve function and increase excitability of primary motor cortex (M1) ipsilateral to the moving hand. However, no study to date has examined the contribution of vision and movement of the opposite hand during an object-directed precision grasp. In this study, we tested 15 healthy individuals in three conditions: MVF (vision + motor), Movement (motor component), and Action Observation (vision component). We hypothesized that unimanual grasp movements with MVF increases the excitability and reduces intracortical inhibition of the M1 ipsilateral to the moving hand. We found increased excitability in the right primary motor cortex (M1) ipsilateral to the moving right hand for MVF movements compared to Rest (Baseline). In contrast, no change was found in right M1 with only movement of the right hand or observation of object-directed precision grasp with left hand. We also found a reduction in short-interval intracortical inhibition in MVF movements compared to baseline. These findings suggest that excitability in M1 during an object-directed precision grasp is mediated by the combination of viewing the movement performed and performing the movement from the opposite hand.

Increases in motor cortical excitability during mirror visual feedback of a precision grasp is influenced by vision and movement of the opposite limb.

While many of our motor skills are acquired through physical practice, we can also learn how to make movements by observing others. For example, individuals can learn how to reach in novel dynamical environments ('force fields', FF) by observing the movements of a tutor. Previous neurophysiological and neuroimaging studies in humans suggest a role for the motor system in motor learning by observing. Here, we tested the role of primary motor cortex (M1) in motor learning by observing. We used single-pulse transcranial magnetic stimulation to elicit motor-evoked potentials (MEPs) in hand muscles at rest. MEPs were elicited before and after participants observed either a video showing a tutor adapting her reaches to an FF or a control video showing a tutor performing reaches in an unlearnable FF. During MEP acquisition, participants fixated a crosshair while their hand muscles were relaxed. We predicted that observing motor learning would result in greater increases in offline M1 excitability compared to observing movements that did not involve learning. We found that observing FF learning resulted in subsequent increases in MEP amplitudes recorded from right first dorsal interosseous and right abductor pollicis brevis muscles at rest. There were no changes in MEP amplitudes after control participants observed a tutor performing similar movements but not learning. The observed MEP changes can thus be specifically linked to observing motor learning. These results are consistent with the idea that observing motor learning produces functional changes in M1, corticospinal networks or both.

Changes in corticospinal excitability associated with motor learning by observing.

Recent findings suggest that the dorsal premotor cortex (PMd), a cortical area in the dorsomedial pathway, is involved in grasp control. It is unclear, however, whether human PMd transfers grasp-related information to the primary motor cortex hand area (M1HAND) during action preparation. The present study tested whether ipsilateral cortico-cortical connections between PMd and M1HAND in the left hemisphere are modulated during grasp preparation. Ten participants performed object-directed grasps and reaches with the right hand. Functional connectivity between left PMd and ipsilateral M1HAND was probed with dual-site transcranial magnetic stimulation. We found that PMd-M1HAND functional interactions were facilitated selectively for the muscles involved in the preparation of the upcoming grasps. The PMd-M1HAND interaction was facilitated for first dorsal interosseous muscle for both precision grip and whole-hand grasps and for abductor digiti minimi muscle for whole-hand grasps. We conclude that human dorsomedial PMd-M1HAND circuit encodes handgrip formation during grasp preparation.

Functional interaction between human dorsal premotor cortex and the ipsilateral primary motor cortex for grasp plans: a dual-site TMS study.

Action observation can facilitate motor skill learning and lead to a memory trace in motor representations of action. However, it remains unclear whether the action itself or the goal of the action drive changes in motor representations after learning by observation. We performed two experiments. In Experiment 1, using serial reaction time task and transcranial magnetic stimulation, we showed that observation of right-hand actions during skill learning only increased left motor cortical excitability, leading to behavioral gains in the same hand as the observed hand. In contrast, observing a sequence of visual cue positions devoid of hand action increases motor cortical excitability in both hemispheres and facilitates motor skill learning in the right hand (Experiment 1) and left hand for a mirror-symmetric sequence (Experiment 2). We propose that the encoding of observed movements maps onto motor representations of the same action to form a limb-specific motor memory, whereas the learning of spatial goals forms memory traces in the motor representations in both hemispheres to prepare for potential action in either hand.

Learning from Goal and Action Based Observations Differentially Modulates Functional Motor Cortical Plasticity.

Dual-site transcranial magnetic stimulation (ds-TMS) is a neurophysiological technique to measure functional connectivity between cortical areas.

Somatosensory-motor cortex interactions measured using dual-site transcranial magnetic stimulation.

Dual-site transcranial magnetic stimulation to the primary motor cortex (M1) and dorsolateral prefrontal cortex (DLPFC) can be used to probe functional connectivity between these regions. The purpose of this study was to characterize the effect of DLPFC stimulation on ipsilateral M1 excitability while participants were at rest and contracting the left- and right-hand first dorsal interosseous muscle. Twelve participants were tested in two separate sessions at varying inter-stimulus intervals (ISI: 4, 5, 6, 7, 8, 9, 10, 11, 12, 15, and 20 ms) at two different conditioning stimulus intensities (80% and 120% of resting motor threshold). No significant effect on ipsilateral M1 excitability was found when applying a conditioning stimulus over DLPFC at any specific inter-stimulus interval or intensity in either the left or right hemisphere. Our findings suggest neither causal inhibitory nor faciliatory influences of DLPFC on ipsilateral M1 activity while participants were at rest or when performing an isometric contraction in the target hand muscle.

Using Dual-Site Transcranial Magnetic Stimulation to Probe Connectivity between the Dorsolateral Prefrontal Cortex and Ipsilateral Primary Motor Cortex in Humans.

Article	Year
Increases in motor cortical excitability during mirror visual feedback of a precision grasp is influenced by vision and movement of the opposite limb. Neuroscience letters\| PubMed ID: 29787788	2018
Changes in corticospinal excitability associated with motor learning by observing. Experimental brain research\| PubMed ID: 30032353	2018
Functional interaction between human dorsal premotor cortex and the ipsilateral primary motor cortex for grasp plans: a dual-site TMS study. Neuroreport\| PubMed ID: 30119106	2018
Learning from Goal and Action Based Observations Differentially Modulates Functional Motor Cortical Plasticity. Neuroscience\| PubMed ID: 30797894	2019
Somatosensory-motor cortex interactions measured using dual-site transcranial magnetic stimulation. Brain stimulation\| PubMed ID: 31043330	2019
Using Dual-Site Transcranial Magnetic Stimulation to Probe Connectivity between the Dorsolateral Prefrontal Cortex and Ipsilateral Primary Motor Cortex in Humans. Brain sciences\| PubMed ID: 31357468	2019

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