Uncovering a context-specific connectional fingerprint of human dorsal premotor cortex

Marius Moisa; Hartwig R Siebner; Rolf Pohmann; Axel Thielscher

doi:10.1523/JNEUROSCI.2757-11.2012

Uncovering a context-specific connectional fingerprint of human dorsal premotor cortex

Marius Moisa, Hartwig R Siebner, Rolf Pohmann, Axel Thielscher

32 Citations (Scopus)

Abstract

Primate electrophysiological and lesion studies indicate a prominent role of the left dorsal premotor cortex (PMd) in action selection based on learned sensorimotor associations. Here we applied transcranial magnetic stimulation (TMS) to human left PMd at low or high intensity while right-handed individuals performed externally paced sequential key presses with their left hand. Movements were cued by abstract visual stimuli, and subjects either freely selected a key press or responded according to a prelearned visuomotor mapping rule. Continuous arterial spin labeling was interleaved with TMS to directly assess how stimulation of left PMd modulates task-related brain activity depending on the mode of movement selection. Relative to passive viewing, both tasks activated a frontoparietal motor network. Compared with low-intensity TMS, high-intensity TMS of left PMd was associated with an increase in activity in medial and right premotor areas without affecting task performance. Critically, this increase in task-related activity was only present when movement selection relied on arbitrary visuomotor associations but not during freely selected movements. Psychophysiological interaction analysis revealed a context-specific increase in functional coupling between the stimulated left PMd and remote right-hemispheric and mesial motor regions that was only present during arbitrary visuomotor mapping. Our TMS perturbation approach yielded causal evidence that the left PMd is implicated in mapping external cues onto the appropriate movement in humans. Furthermore, the data suggest that the left PMd may transiently form a functional network together with right-hemispheric and mesial motor regions to sustain visuomotor mapping performed with the left nondominant hand.

Original language	English
Journal	Journal of Neuroscience
Volume	32
Issue number	21
Pages (from-to)	7244-52
Number of pages	9
ISSN	0270-6474
DOIs	https://doi.org/10.1523/JNEUROSCI.2757-11.2012
Publication status	Published - 23 May 2012

Keywords

Adult
Brain Mapping
Cues
Female
Frontal Lobe
Functional Laterality
Humans
Magnetic Resonance Imaging
Male
Motor Cortex
Neural Pathways
Parietal Lobe
Psychomotor Performance
Spin Labels
Transcranial Magnetic Stimulation

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10.1523/JNEUROSCI.2757-11.2012

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title = "Uncovering a context-specific connectional fingerprint of human dorsal premotor cortex",

abstract = "Primate electrophysiological and lesion studies indicate a prominent role of the left dorsal premotor cortex (PMd) in action selection based on learned sensorimotor associations. Here we applied transcranial magnetic stimulation (TMS) to human left PMd at low or high intensity while right-handed individuals performed externally paced sequential key presses with their left hand. Movements were cued by abstract visual stimuli, and subjects either freely selected a key press or responded according to a prelearned visuomotor mapping rule. Continuous arterial spin labeling was interleaved with TMS to directly assess how stimulation of left PMd modulates task-related brain activity depending on the mode of movement selection. Relative to passive viewing, both tasks activated a frontoparietal motor network. Compared with low-intensity TMS, high-intensity TMS of left PMd was associated with an increase in activity in medial and right premotor areas without affecting task performance. Critically, this increase in task-related activity was only present when movement selection relied on arbitrary visuomotor associations but not during freely selected movements. Psychophysiological interaction analysis revealed a context-specific increase in functional coupling between the stimulated left PMd and remote right-hemispheric and mesial motor regions that was only present during arbitrary visuomotor mapping. Our TMS perturbation approach yielded causal evidence that the left PMd is implicated in mapping external cues onto the appropriate movement in humans. Furthermore, the data suggest that the left PMd may transiently form a functional network together with right-hemispheric and mesial motor regions to sustain visuomotor mapping performed with the left nondominant hand.",

keywords = "Adult, Brain Mapping, Cues, Female, Frontal Lobe, Functional Laterality, Humans, Magnetic Resonance Imaging, Male, Motor Cortex, Neural Pathways, Parietal Lobe, Psychomotor Performance, Spin Labels, Transcranial Magnetic Stimulation",

author = "Marius Moisa and Siebner, {Hartwig R} and Rolf Pohmann and Axel Thielscher",

year = "2012",

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doi = "10.1523/JNEUROSCI.2757-11.2012",

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AU - Moisa, Marius

AU - Siebner, Hartwig R

AU - Pohmann, Rolf

AU - Thielscher, Axel

PY - 2012/5/23

Y1 - 2012/5/23

N2 - Primate electrophysiological and lesion studies indicate a prominent role of the left dorsal premotor cortex (PMd) in action selection based on learned sensorimotor associations. Here we applied transcranial magnetic stimulation (TMS) to human left PMd at low or high intensity while right-handed individuals performed externally paced sequential key presses with their left hand. Movements were cued by abstract visual stimuli, and subjects either freely selected a key press or responded according to a prelearned visuomotor mapping rule. Continuous arterial spin labeling was interleaved with TMS to directly assess how stimulation of left PMd modulates task-related brain activity depending on the mode of movement selection. Relative to passive viewing, both tasks activated a frontoparietal motor network. Compared with low-intensity TMS, high-intensity TMS of left PMd was associated with an increase in activity in medial and right premotor areas without affecting task performance. Critically, this increase in task-related activity was only present when movement selection relied on arbitrary visuomotor associations but not during freely selected movements. Psychophysiological interaction analysis revealed a context-specific increase in functional coupling between the stimulated left PMd and remote right-hemispheric and mesial motor regions that was only present during arbitrary visuomotor mapping. Our TMS perturbation approach yielded causal evidence that the left PMd is implicated in mapping external cues onto the appropriate movement in humans. Furthermore, the data suggest that the left PMd may transiently form a functional network together with right-hemispheric and mesial motor regions to sustain visuomotor mapping performed with the left nondominant hand.

AB - Primate electrophysiological and lesion studies indicate a prominent role of the left dorsal premotor cortex (PMd) in action selection based on learned sensorimotor associations. Here we applied transcranial magnetic stimulation (TMS) to human left PMd at low or high intensity while right-handed individuals performed externally paced sequential key presses with their left hand. Movements were cued by abstract visual stimuli, and subjects either freely selected a key press or responded according to a prelearned visuomotor mapping rule. Continuous arterial spin labeling was interleaved with TMS to directly assess how stimulation of left PMd modulates task-related brain activity depending on the mode of movement selection. Relative to passive viewing, both tasks activated a frontoparietal motor network. Compared with low-intensity TMS, high-intensity TMS of left PMd was associated with an increase in activity in medial and right premotor areas without affecting task performance. Critically, this increase in task-related activity was only present when movement selection relied on arbitrary visuomotor associations but not during freely selected movements. Psychophysiological interaction analysis revealed a context-specific increase in functional coupling between the stimulated left PMd and remote right-hemispheric and mesial motor regions that was only present during arbitrary visuomotor mapping. Our TMS perturbation approach yielded causal evidence that the left PMd is implicated in mapping external cues onto the appropriate movement in humans. Furthermore, the data suggest that the left PMd may transiently form a functional network together with right-hemispheric and mesial motor regions to sustain visuomotor mapping performed with the left nondominant hand.

KW - Adult

KW - Brain Mapping

KW - Cues

KW - Female

KW - Frontal Lobe

KW - Functional Laterality

KW - Humans

KW - Magnetic Resonance Imaging

KW - Male

KW - Motor Cortex

KW - Neural Pathways

KW - Parietal Lobe

KW - Psychomotor Performance

KW - Spin Labels

KW - Transcranial Magnetic Stimulation

U2 - 10.1523/JNEUROSCI.2757-11.2012

DO - 10.1523/JNEUROSCI.2757-11.2012

M3 - Journal article

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SN - 0270-6474

VL - 32

SP - 7244

EP - 7252

JO - The Journal of neuroscience : the official journal of the Society for Neuroscience

JF - The Journal of neuroscience : the official journal of the Society for Neuroscience

IS - 21

ER -

Uncovering a context-specific connectional fingerprint of human dorsal premotor cortex

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Keywords

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