Altered perception‐action binding modulates inhibitory control in Gilles de la Tourette syndrome

Petruo, Vanessa A.; Bodmer, Benjamin; Brandt, Valerie; Baumung, Leoni; Roessner, Veit; Münchau, Alexander; Beste, Christian

doi:10.1111/jcpp.12938

Cited by 50 publications

(59 citation statements)

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“…No difference was evident in the NoGo incompatible condition and the NoGo compatible condition (all t < 1.01; p > 0.3). This is completely in line with the previous results by Petruo et al (2018) and cross-validates these results. At time point T2, the ANOVA revealed a main effect "condition" (F(2,40) = 53.40; p < 0.001; η p 2 = 0.572), showing that the FAs were, again, highest in the NoGo without condition (24.28 ± 3.1), followed by the NoGo incompatible condition (16.81 ± 1.8) and the NoGo compatible condition (6.66 ± 1.2).…”

Section: Resultssupporting

confidence: 93%

“…GtS patients and healthy controls. This is a follow-up study of Petruo et al (2018) testing patients with GTS diagnosed according to DSM-IV using an auditory-visual Go/NoGo task. For the follow-up, a subsample of N = 21 GTS out of N = 35 previously studied patients between 9 to 19 years was available (mean age 13.09 ± 2.1; mean IQ = 107.13 ± 10.5).…”

Section: Methodsmentioning

confidence: 99%

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Comprehensive Behavioral Intervention for Tics reduces perception-action binding during inhibitory control in Gilles de la Tourette syndrome

Petruo

Bodmer

Bluschke

et al. 2020

Sci Rep

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Gilles de la tourette Syndrome (GtS) is a developmental disorder. empirical studies and an emerging cognitive framework on GtS suggest that GtS is a disorder of abnormally strong 'perception-action binding'. Theoretical considerations imply that the effectiveness of long-established behavioral interventions might be related to a normalization of increased binding in GtS. this has not been tested yet. We examined the effect of a standardized Comprehensive Behavior Intervention for Tics (CBIT) in n = 21 adolescent GTS patients and N = 21 healthy controls on perception-action binding in an inhibitory control paradigm. Prior to CBIT, GTS patients showed compromised performance compared to controls, specifically when inhibitory control was triggered by uni-modal visual compared to bi-modal stimuli. After CBIT intervention, GTS patient's performance was at the same level as healthy controls. This is supported by a Bayesian data analysis. CBIT specifically affected inhibitory control in a condition where reconfigurations of perception-action bindings are necessary to perform inhibitory control. A power of 95% was evident for these effects. CBIT reduces increased 'binding' between perception and action in GTS and thereby increases the ability to perform response inhibition. The results are the first to provide insights as to why CBIT is effective by relating elements of this intervention to overarching cognitive theoretical frameworks on perception-action bindings.Gilles de la Tourette Syndrome (GTS) is a developmental disorder with multi-faceted neuropsychiatric symptoms, as onset and highest prevalence in childhood or adolescence and is characterized by multiple motor and vocal tics 1,2 . Traditionally, GTS has been considered as a movement disorder. This is not undisputed though given that most tics can, at least partially, be controlled, are associated with premonitory sensations and might reflect motor learning and habit formation 3 . On the basis of these findings, it has recently been suggested that a hallmark of GTS is an abnormally strong interrelation of perceptual processes and motor actions, particularly between premonitory sensation including preceding urges and tics, and that GTS might be conceptualized as a disorder in which purposeful actions play an important role 3 . Indeed, several studies have reported that GTS patients make better use of multi-or bi-modal sensory stimuli for response selection 4,5 . Moreover, findings from procedural learning also suggest that GTS patients establish connections between stimuli and the corresponding response faster and more strongly 6,7 . In line with this, GTS is associated with increased habit formation tendencies 8 depending on the establishment of strong stimulus-response mappings. These findings corroborate the notion that GTS might be a disorder characterized by an abnormally strong 'binding' between perception and action, for which a cognitive framework based on the Theory of Event Coding (TEC) detailing the link between perception and action is an attractive o...

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Section: Resultssupporting

confidence: 93%

Section: Methodsmentioning

confidence: 99%

Comprehensive Behavioral Intervention for Tics reduces perception-action binding during inhibitory control in Gilles de la Tourette syndrome

Petruo

Bodmer

Bluschke

et al. 2020

Sci Rep

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“…The source localization using sLORETA suggests that regions in superior frontal gyrus (BA6), the medial frontal cortex (BA24), anterior cingulate cortex (BA24) and the inferior parietal cortex (BA40) were modulated by interactive effects between “feature overlap × response” for the P3 and the C‐cluster. These regions have previously been suggested to be involved in event coding processes (Chmielewski & Beste, ; Chmielewski & Beste, ; Chmielewski & Beste, ; Elsner et al, ; Kühn et al, ; Petruo et al, ; Petruo et al, ; Zmigrod et al, ). However, the source localization findings were most consistent for the inferior parietal cortex (BA40), since this area was seen both in the sLORETA using the C‐cluster data and the nondecomposed P3 ERP data.…”

Section: Discussionmentioning

confidence: 92%

Connecting EEG signal decomposition and response selection processes using the theory of event coding framework

Takács

Zink

Wolff

et al. 2020

Human Brain Mapping

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The neurophysiological mechanisms underlying the integration of perception and action are an important topic in cognitive neuroscience. Yet, connections between neurophysiology and cognitive theoretical frameworks have rarely been established. The theory of event coding (TEC) details how perceptions and actions are associated (bound) in a common representational domain (the “event file”), but the neurophysiological mechanisms underlying these processes are hardly understood. We used complementary neurophysiological methods to examine the neurophysiology of event file processing (i.e., event‐related potentials [ERPs], temporal EEG signal decomposition, EEG source localization, time‐frequency decomposition, EEG network analysis). We show that the P3 ERP component and activity modulations in inferior parietal regions (BA40) reflect event file binding processes. The relevance of this parietal region is corroborated by source localization of temporally decomposed EEG data. We also show that temporal EEG signal decomposition reveals a pattern of results suggesting that event file processes can be dissociated from pure stimulus and response‐related processes in the EEG signal. Importantly, it is also documented that event file binding processes are reflected by modulations in the network architecture of theta frequency band activity. That is, when stimulus–response bindings in event files hamper response selection this was associated with a less efficient theta network organization. A more efficient organization was evident when stimulus–response binding in event files facilitated response selection. Small‐world network measures seem to reflect event file processing. The results show how cognitive‐theoretical assumptions of TEC can directly be mapped to the neurophysiology of response selection.

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“…In letzter Zeit rückt ein weiterer Kortexabschnitt, der rechte inferiore parietale Kortex (BA 40], in den Fokus. Dieser ist entscheidend an der Kopplung zwischen Wahrnehmungen und Aktionen (perception-action-binding) beteiligt [43], die bei GTS-Patienten gestört zu sein scheint [44].…”

Section: Kortikale Arealeunclassified

“…Wichtig ist, dass vorausgehende Bindungen darauffolgende Aktionen beeinflussen können. Wenn ein bekannter Stimulus eine neue Aktion auslösen soll, bereiten bereits etablierte Verbindungen ("event files") Probleme [43,88,89]. Genauer bedeutet dies, dass bei nur teilweiser Wiederholung der Eigenschaften eines "event files" schlechtere Ergebnisse erzielt werden als bei Wiederholung aller Eigenschaften oder wenn alle Eigenschaften unbekannt sind ("partial-repetition costs") [90].…”

Section: Perzeption Handlungunclassified

Pathophysiologie des Gilles-de-la-Tourette-Syndroms

Kleimaker¹,

Kleimaker²,

Beste³

et al. 2020

Nervenheilkunde

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ZUSAMMENFASSUNGBeim Gilles-de-la-Tourette-Syndrom (GTS) handelt es sich um eine häufige facettenreiche, typischerweise im Kindes- oder Jugendalter beginnende neuropsychiatrische Erkrankung. Die Pathophysiologie ist nicht sicher geklärt. Eine wichtige Rolle scheinen die Basalganglien und kortiko-striato-thalamo-kortikale Regelkreise einzunehmen. Eine der konstantesten Veränderungen stellt eine diskrete Volumenreduktion des Striatums bei Kindern dar. Auch konnten Veränderungen im Bereich der weißen Substanz innerhalb dieses Regelkreises nachgewiesen werden. Auf kortikaler Ebene wurden Veränderungen im Bereich des sensomotorischen und präfrontalen Kortex, der supplementär motorischen Region und des inferioren parietalen Kortex (BA 40) beschrieben. Auf biochemischer Ebene zeigt sich vor allem eine erhöhte dopaminerge Transmission. Auch Serotonin scheint durch den Wegfall Dopamin hemmender Effekte eine Rolle zu spielen. Kognitionspsychologische bzw. wahrnehmungspsychologische Ansätze gingen zunächst von einer gestörten inhibitorischen Kontrolle aus.Aufgrund uneinheitlicher Ergebnisse wird eher eine Interferenz mit Kompensationsmechanismen zur Tic-Kontrolle vermutet. Auch zeigen sich Veränderungen der interozeptiven Wahrnehmung. Allerdings ist unsicher, ob diese ursächlich sind oder eine sekundäre Veränderung des GTS darstellen. Einer der aktuellsten Ansätze stützt sich auf die „Theory of Event Coding“, welche besagt, dass sowohl Wahrnehmungen als auch Handlungen gemeinsam in „event files“ gespeichert werden und in enger Verbindung stehen. Es gibt erste experimentelle Hinweise, dass bei Patienten mit einem GTS die Kopplung zwischen Wahrnehmung und Handlung besonders stark ausgeprägt ist und Tics aufgrund dieser starken Bindung durch verschiedene Stimuli ausgelöst werden könnten.

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Altered perception‐action binding modulates inhibitory control in Gilles de la Tourette syndrome

Abstract: Stimulus-action inhibition binding is stronger in GTS patients than healthy controls and affects inhibitory control corroborating the concept suggesting that GTS might be a condition of altered perception-action integration (binding); i.e. a disorder of purposeful actions.

Cited by 50 publications

References 48 publications

Comprehensive Behavioral Intervention for Tics reduces perception-action binding during inhibitory control in Gilles de la Tourette syndrome

Comprehensive Behavioral Intervention for Tics reduces perception-action binding during inhibitory control in Gilles de la Tourette syndrome

Connecting EEG signal decomposition and response selection processes using the theory of event coding framework

Pathophysiologie des Gilles-de-la-Tourette-Syndroms

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