Left dorsal premotor cortex and supramarginal gyrus complement each other during rapid action reprogramming

Gesa Hartwigsen; Sven Bestmann; Nick S Ward; Saskia Woerbel; Claudia Mastroeni; Oliver Granert; Hartwig R Siebner

doi:10.1523/JNEUROSCI.1010-12.2012

Left dorsal premotor cortex and supramarginal gyrus complement each other during rapid action reprogramming

Gesa Hartwigsen, Sven Bestmann, Nick S Ward, Saskia Woerbel, Claudia Mastroeni, Oliver Granert, Hartwig R Siebner

41 Citations (Scopus)

Abstract

The ability to discard a prepared action plan in favor of an alternative action is critical when facing sudden environmental changes. We tested whether the functional contribution of left supramarginal gyrus (SMG) during action reprogramming depends on the functional integrity of left dorsal premotor cortex (PMd). Adopting a dual-site repetitive transcranial magnetic stimulation (rTMS) strategy, we first transiently disrupted PMd with "off-line" 1 Hz rTMS and then applied focal "on-line" rTMS to SMG while human subjects performed a spatially precued reaction time (RT) task. Effective on-line rTMS of SMG but not sham rTMS of SMG increased errors when subjects had to reprogram their action in response to an invalid precue regardless of the type of preceding off-line rTMS. This suggests that left SMG primarily contributes to the on-line updating of actions by suppressing invalidly prepared responses. On-line rTMS of SMG additionally increased RTs for correct responses in invalidly precued trials, but only after off-line rTMS of PMd. We infer that off-line rTMS caused an additional dysfunction of PMd, which increased the functional relevance of SMG for rapid activation of the correct response, and sensitized SMG to the disruptive effects of on-line rTMS. These results not only provide causal evidence that left PMd and SMG jointly contribute to action reprogramming, but also that the respective functional weight of these areas can be rapidly redistributed. This mechanism might constitute a generic feature of functional networks that allows for rapid functional compensation in response to focal dysfunctions.

Original language	English
Journal	Journal of Neuroscience
Volume	32
Issue number	46
Pages (from-to)	16162-71a
ISSN	0270-6474
DOIs	https://doi.org/10.1523/JNEUROSCI.1010-12.2012
Publication status	Published - 14 Nov 2012

Keywords

Adaptation, Psychological
Adult
Analysis of Variance
Cues
Data Interpretation, Statistical
Female
Humans
Male
Mental Processes
Motor Cortex
Nerve Net
Neuronavigation
Parietal Lobe
Psychomotor Performance
Reaction Time
Transcranial Magnetic Stimulation
Young Adult

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10.1523/JNEUROSCI.1010-12.2012

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title = "Left dorsal premotor cortex and supramarginal gyrus complement each other during rapid action reprogramming",

abstract = "The ability to discard a prepared action plan in favor of an alternative action is critical when facing sudden environmental changes. We tested whether the functional contribution of left supramarginal gyrus (SMG) during action reprogramming depends on the functional integrity of left dorsal premotor cortex (PMd). Adopting a dual-site repetitive transcranial magnetic stimulation (rTMS) strategy, we first transiently disrupted PMd with {"}off-line{"} 1 Hz rTMS and then applied focal {"}on-line{"} rTMS to SMG while human subjects performed a spatially precued reaction time (RT) task. Effective on-line rTMS of SMG but not sham rTMS of SMG increased errors when subjects had to reprogram their action in response to an invalid precue regardless of the type of preceding off-line rTMS. This suggests that left SMG primarily contributes to the on-line updating of actions by suppressing invalidly prepared responses. On-line rTMS of SMG additionally increased RTs for correct responses in invalidly precued trials, but only after off-line rTMS of PMd. We infer that off-line rTMS caused an additional dysfunction of PMd, which increased the functional relevance of SMG for rapid activation of the correct response, and sensitized SMG to the disruptive effects of on-line rTMS. These results not only provide causal evidence that left PMd and SMG jointly contribute to action reprogramming, but also that the respective functional weight of these areas can be rapidly redistributed. This mechanism might constitute a generic feature of functional networks that allows for rapid functional compensation in response to focal dysfunctions.",

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author = "Gesa Hartwigsen and Sven Bestmann and Ward, {Nick S} and Saskia Woerbel and Claudia Mastroeni and Oliver Granert and Siebner, {Hartwig R}",

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T1 - Left dorsal premotor cortex and supramarginal gyrus complement each other during rapid action reprogramming

AU - Hartwigsen, Gesa

AU - Bestmann, Sven

AU - Ward, Nick S

AU - Woerbel, Saskia

AU - Mastroeni, Claudia

AU - Granert, Oliver

AU - Siebner, Hartwig R

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N2 - The ability to discard a prepared action plan in favor of an alternative action is critical when facing sudden environmental changes. We tested whether the functional contribution of left supramarginal gyrus (SMG) during action reprogramming depends on the functional integrity of left dorsal premotor cortex (PMd). Adopting a dual-site repetitive transcranial magnetic stimulation (rTMS) strategy, we first transiently disrupted PMd with "off-line" 1 Hz rTMS and then applied focal "on-line" rTMS to SMG while human subjects performed a spatially precued reaction time (RT) task. Effective on-line rTMS of SMG but not sham rTMS of SMG increased errors when subjects had to reprogram their action in response to an invalid precue regardless of the type of preceding off-line rTMS. This suggests that left SMG primarily contributes to the on-line updating of actions by suppressing invalidly prepared responses. On-line rTMS of SMG additionally increased RTs for correct responses in invalidly precued trials, but only after off-line rTMS of PMd. We infer that off-line rTMS caused an additional dysfunction of PMd, which increased the functional relevance of SMG for rapid activation of the correct response, and sensitized SMG to the disruptive effects of on-line rTMS. These results not only provide causal evidence that left PMd and SMG jointly contribute to action reprogramming, but also that the respective functional weight of these areas can be rapidly redistributed. This mechanism might constitute a generic feature of functional networks that allows for rapid functional compensation in response to focal dysfunctions.

AB - The ability to discard a prepared action plan in favor of an alternative action is critical when facing sudden environmental changes. We tested whether the functional contribution of left supramarginal gyrus (SMG) during action reprogramming depends on the functional integrity of left dorsal premotor cortex (PMd). Adopting a dual-site repetitive transcranial magnetic stimulation (rTMS) strategy, we first transiently disrupted PMd with "off-line" 1 Hz rTMS and then applied focal "on-line" rTMS to SMG while human subjects performed a spatially precued reaction time (RT) task. Effective on-line rTMS of SMG but not sham rTMS of SMG increased errors when subjects had to reprogram their action in response to an invalid precue regardless of the type of preceding off-line rTMS. This suggests that left SMG primarily contributes to the on-line updating of actions by suppressing invalidly prepared responses. On-line rTMS of SMG additionally increased RTs for correct responses in invalidly precued trials, but only after off-line rTMS of PMd. We infer that off-line rTMS caused an additional dysfunction of PMd, which increased the functional relevance of SMG for rapid activation of the correct response, and sensitized SMG to the disruptive effects of on-line rTMS. These results not only provide causal evidence that left PMd and SMG jointly contribute to action reprogramming, but also that the respective functional weight of these areas can be rapidly redistributed. This mechanism might constitute a generic feature of functional networks that allows for rapid functional compensation in response to focal dysfunctions.

KW - Adaptation, Psychological

KW - Adult

KW - Analysis of Variance

KW - Cues

KW - Data Interpretation, Statistical

KW - Female

KW - Humans

KW - Male

KW - Mental Processes

KW - Motor Cortex

KW - Nerve Net

KW - Neuronavigation

KW - Parietal Lobe

KW - Psychomotor Performance

KW - Reaction Time

KW - Transcranial Magnetic Stimulation

KW - Young Adult

U2 - 10.1523/JNEUROSCI.1010-12.2012

DO - 10.1523/JNEUROSCI.1010-12.2012

M3 - Journal article

C2 - 23152600

SN - 0270-6474

VL - 32

SP - 16162-71a

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 - 46

ER -

Left dorsal premotor cortex and supramarginal gyrus complement each other during rapid action reprogramming

Abstract

Keywords

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