L’interazione e la coordinazione tra esseri umani richiede un continuo e reciproco scambio di informazioni. La mia tesi riporta una serie di esperimenti sui meccanismi rilevanti nella coordinazione dell’azione (Joint Action – JA). Abbiamo posto l’attenzione sul contributo inibitorio del controllo motorio, in quanto l’esecuzione d’azione (AE) richiede un bilanciamento dei contributi eccitatori e inibitori. Sebbene quest’ultimo abbia ricevuto minor attenzione, una JA efficace può essere vista come l’abilità di regolare ed adattare il proprio piano motorio a quello di un altro. Abbiamo osservato come l’osservazione d’azione (AO) influenzi l’attività corticomotoria dell’osservatore nell’AE. I partecipanti avevano il compito di eseguire ed osservare, nello stesso momento, azioni simili o opposte. Questo compito prevedeva la sovrapposizione temporale tra AO e AE, caratteristica della JA. Ancora non chiarita però è la modalità con cui viene risolta l’interferenza tra AO e AE nel soggetto. Abbiamo quindi misurato, utilizzando la Stimolazione Magnetica Transcranica (TMS), sia lo stato di eccitabilità corticospinale (CSE) che di inibizione (Periodo Silente – cSP, inibizione lenta mediata da GABAb). La mancata corrispondenza tra AO e AE ha prodotto una modulazione solamente del cSP. Si suppone che l'inibizione corticospinale potrebbe essere il meccanismo neurofisiologico con cui la propria esecuzione motoria è isolata dall'elaborazione simultanea dai segnali visivi delle azioni altrui. Successivamente, abbiamo valutato le modulazioni inibitorie in un compito JA, progettando un compito di cooperazione temporale e coordinazione tattile. I partecipanti dovevano raggiungere e aprire, con una sola mano, una bottiglia tenuta o da un supporto (no-JA) o da un'altra persona (JA). Nella condizione JA il partner stabilizza l’oggetto modulando in modo anticipatorio la forza con cui lo sorregge. Abbiamo misurato il cSP e l'inibizione intracorticale ad intervallo breve (sICI, inibizione veloce mediata da GABAa). Abbiamo trovato una chiara dissociazione tra inibizione veloce e lenta durante JA, in particolare un aumento di cSP e una riduzione di sICI. Inoltre, abbiamo trovato una correlazione tra la durata del cSP e il comportamento del partner (forza di compressione massima e totale), suggerendo che l'inibizione corticospinale potrebbe essere la firma neurale del mutuo adattamento che si sviluppa durante l'interazione. L’azione, tuttavia, è il risultato dell’attività di una serie di aree corticali. Le aree premotorie, coinvolte nella trasformazione sensorimotoria, sono probabilmente coinvolte nell'inibizione durante la JA. Nel terzo esperimento, mediante la stimolazione Theta Burst continua (cTBS), abbiamo modulato l'attività della corteccia premotoria dorsale (PMd), della corteccia premotoria ventrale (PMv) o di un sito di controllo (vertice), registrando sICI e cSP mentre i partecipanti eseguivano il nostro compito. Sembra che il cSP è venga influenzato esclusivamente dalla stimolazione di PMd nella condizione JA. L’interazione a volte potrebbe richiedere anche l’arresto completo dell'azione in corso. Per valutare questo, nell'ultima serie di esperimenti abbiamo unito il nostro compito JA con uno Stop Signal task (SST), che fornisce una misura dell'inibizione comportamentale (Stop Signal Reaction Time - SSRT). A livello comportamentale abbiamo osservato un SSRT più lungo in JA. Inoltre, la cTBS applicata a PMd nella condizione JA ha modulato l'SSRT, suggerendone un ruolo anche nella modulazione dell'inibizione comportamentale. In conclusione, questi studi permettono di osservare l'importanza dei meccanismi inibitori durante la generazione di un output motorio di successo nel contesto di JA. I meccanismi inibitori svolgono un ruolo chiave nella pianificazione, preparazione e controllo dell'azione, risolvendo la competizione tra molteplici azioni potenziali e bilanciando eccitazione e inibizione.

Human interaction and coordination require a continuous and reciprocal exchange of information between people. My thesis reports a series of experiments on the neurophysiological and behavioral mechanisms relevant in the coordination of actions (Joint Action - JA). My work has focused on the inhibitory side of action control, basing on the assumption that Action Execution (AE) requires a continuous balancing of excitatory and inhibitory contributions. Although the latter has received less attention, successful JA can be seen as the ability to finely adjust an online motor plan to others’ actions. Firstly, we investigated the influence of Action Observation (AO) on the observer’s corticomotor drive during AE. Participants concurrently observed and executed matched or mismatched actions. In this task there was no interaction but temporal overlap between AO and AE, that characterize the JA. How interference between motor activations for AO and AE is resolved, is poorly understood. We measured, by means of Transcranial Magnetic Stimulation (TMS), both corticospinal excitability (CSE) and inhibition (cortical Silent Period – cSP - slow GABAb-mediated inhibition). The mismatch between AO and AE produced only a selective reduction of cSP length. Thus, we demonstrate that corticospinal inhibition could probably be the neurophysiological mechanism by which one’s own motor execution is isolated from the concurrent processing of visual cues provided by other’s actions. In a subsequent series of experiments, we investigated the inhibitory modulations during an ecological and interactive task. To this aim, we designed a motor task requiring temporal cooperation and haptic coordination. Participants have to reach and open a bottle with one hand held by a mechanical holder (no-JA) or by another person (JA). In the JA condition the stability of the object is provided by the anticipatory squeezing forces applied by the partner. We measured cSP and short-interval intracortical inhibition (sICI – fast GABAa-mediated inhibition). We found a clear dissociation between fast and slow inhibition during JA, specifically an increase of cSP and a reduction of sICI. Moreover, we found a correlation between cSP length and the partner’s behaviour (maximal and total squeezing force) in the previous trial, suggesting that corticospinal inhibition might be the neural signature of the mutual behavioural co-adaptation developing during the interaction. The motor output is however the result of a complex motor network activity. Premotor areas, involved in sensorimotor transformations, are the most likely candidate to influence inhibition in JA coordination. In the third experiment, by means of continuous Theta Burst Stimulation (cTBS), we interfered with the activity of dorsal premotor cortex (PMd), ventral premotor cortex (PMv) or a control site (vertex), recording sICI and cSP while participants performed our JA task. We showed that the cSP was affected exclusively by PMd stimulation during the JA condition. Contextual information or partner’s behaviour may call for fine motor adjustments or a complete stop of the ongoing action might be required. This is exactly what we investigated in the last series of experiments by merging our JA task with a classical Stop Signal task (SST), that provide a measure of behavioral inhibition (Stop Signal Reaction Time - SSRT). In a first behavioral study we observed longer SSRT in JA. In the second study, cTBS applied to the PMd modulated the SSRT only in JA, suggesting that PMd does play a role also in modulating JA behavioral inhibition. In conclusion, I report few studies showing the importance of inhibitory mechanisms during the generation of a successful motor output in the context of JA. Inhibitory mechanisms play a key role in action planning, preparation and control, resolving competition between multiple potential actions and balancing excitation and inhibition.

Behavioral and neurophysiological inhibition in Joint Action

DOLFINI, ELISA
2022-07-01T00:00:00+02:00

Abstract

Human interaction and coordination require a continuous and reciprocal exchange of information between people. My thesis reports a series of experiments on the neurophysiological and behavioral mechanisms relevant in the coordination of actions (Joint Action - JA). My work has focused on the inhibitory side of action control, basing on the assumption that Action Execution (AE) requires a continuous balancing of excitatory and inhibitory contributions. Although the latter has received less attention, successful JA can be seen as the ability to finely adjust an online motor plan to others’ actions. Firstly, we investigated the influence of Action Observation (AO) on the observer’s corticomotor drive during AE. Participants concurrently observed and executed matched or mismatched actions. In this task there was no interaction but temporal overlap between AO and AE, that characterize the JA. How interference between motor activations for AO and AE is resolved, is poorly understood. We measured, by means of Transcranial Magnetic Stimulation (TMS), both corticospinal excitability (CSE) and inhibition (cortical Silent Period – cSP - slow GABAb-mediated inhibition). The mismatch between AO and AE produced only a selective reduction of cSP length. Thus, we demonstrate that corticospinal inhibition could probably be the neurophysiological mechanism by which one’s own motor execution is isolated from the concurrent processing of visual cues provided by other’s actions. In a subsequent series of experiments, we investigated the inhibitory modulations during an ecological and interactive task. To this aim, we designed a motor task requiring temporal cooperation and haptic coordination. Participants have to reach and open a bottle with one hand held by a mechanical holder (no-JA) or by another person (JA). In the JA condition the stability of the object is provided by the anticipatory squeezing forces applied by the partner. We measured cSP and short-interval intracortical inhibition (sICI – fast GABAa-mediated inhibition). We found a clear dissociation between fast and slow inhibition during JA, specifically an increase of cSP and a reduction of sICI. Moreover, we found a correlation between cSP length and the partner’s behaviour (maximal and total squeezing force) in the previous trial, suggesting that corticospinal inhibition might be the neural signature of the mutual behavioural co-adaptation developing during the interaction. The motor output is however the result of a complex motor network activity. Premotor areas, involved in sensorimotor transformations, are the most likely candidate to influence inhibition in JA coordination. In the third experiment, by means of continuous Theta Burst Stimulation (cTBS), we interfered with the activity of dorsal premotor cortex (PMd), ventral premotor cortex (PMv) or a control site (vertex), recording sICI and cSP while participants performed our JA task. We showed that the cSP was affected exclusively by PMd stimulation during the JA condition. Contextual information or partner’s behaviour may call for fine motor adjustments or a complete stop of the ongoing action might be required. This is exactly what we investigated in the last series of experiments by merging our JA task with a classical Stop Signal task (SST), that provide a measure of behavioral inhibition (Stop Signal Reaction Time - SSRT). In a first behavioral study we observed longer SSRT in JA. In the second study, cTBS applied to the PMd modulated the SSRT only in JA, suggesting that PMd does play a role also in modulating JA behavioral inhibition. In conclusion, I report few studies showing the importance of inhibitory mechanisms during the generation of a successful motor output in the context of JA. Inhibitory mechanisms play a key role in action planning, preparation and control, resolving competition between multiple potential actions and balancing excitation and inhibition.
D'AUSILIO, Alessandro
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Utilizza questo identificativo per citare o creare un link a questo documento: http://hdl.handle.net/11392/2492513
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