Does the brain know who is at the origin of what in an imitative interaction?

Abstract

Brain correlates of the sense of agency have recently received increased attention. However, the explorations remain largely restricted to the study of brains in isolation. The prototypical paradigm used so far consists of manipulating visual perception of own action while asking the subject to draw a distinction between self- versus externally caused action. However, the recent definition of agency as a multifactorial phenomenon combining bottom-up and top-down processes suggests the exploration of more complex situations. Notably there is a need of accounting for the dynamics of agency in a two-body context where we often experience the double faceted question of who is at the origin of what in an ongoing interaction. In a dyadic context of role switching indeed, each partner can feel body ownership, share a sense of agency and altogether alternate an ascription of the primacy of action to self and to other. To explore the brain correlates of these different aspects of agency, we recorded with dual EEG and video set-ups 22 subjects interacting via spontaneous versus induced imitation (II) of hand movements. The differences between the two conditions lie in the fact that the roles are either externally attributed (induced condition) or result from a negotiation between subjects (spontaneous condition). Results demonstrate dissociations between self- and other-ascription of action primacy in delta, alpha and beta frequency bands during the condition of II. By contrast a similar increase in the low gamma frequency band (38–47 Hz) was observed over the centro-parietal regions for the two roles in spontaneous imitation (SI). Taken together, the results highlight the different brain correlates of agency at play during live interactions.

Frontal alpha oscillations distinguish leaders from followers: Multivariate decoding of mutually interacting brains

“…Consistent with previous studies of neural oscillations during joint attention (Lachat et al, 2012), coordination (Tognoli et al, 2007, Dumas et al, 2012, Naeem et al, 2012a, and observation (Cochin et al, 1999, Caetano et al, 2007, 10 Hz suppression was found over left-central electrodes when interacting with another person versus a nonresponsive computer, with additional frontal components. While mu-rhythm suppression is well known to occur over the bilateral sensorimotor cortex (but stronger over the contralateral cortex) when engaging in motor activity in contrast to rest (Gastaut, 1952, Gastaut and Bert, 1954, Pfurtscheller and Lopes da Silva, 1999, it has also been found during action observation (Hari et al, 1998, Cochin et al, 1999, Caetano et al, 2007, and is hence thought to be part of a common coding mechanism of perception and action (Hari, 2006, de Lange et al, 2008.…”

“…followers) and initiators (i.e. leaders) of action in reciprocal imitation paradigms in both interactive (Dumas et al, 2012, Guionnet et al, 2012) and non-interactive scenarios (Decety et al, 2002). These studies have shown activation of the inferior parietal cortex during initiation and imitation of stimuli, in the absence of interaction (Decety et al, 2002), as well as recruitment of fronto-parietal regions during interactive imitation (Guionnet et al, 2012).…”

“…More specifically, previous dual-EEG studies have consistently identified amplitude-modulation of oscillations around 10 Hz (alpha-band) over centro-parietal electrodes during joint attention and social coordination (Tognoli et al, 2007, Dumas et al, 2012, Lachat et al, 2012, which has also been reported in non-interactive experiments, during execution and observation of motor tasks (Cochin et al, 1999, Caetano et al, 2007) -corresponding to modulation in the rolandic mu rhythm (Gastaut, 1952). Interpersonally, two-brain studies have primarily focused on quantifying functional similarities or temporal synchronization between brains (Hasson et al, 2012) during interaction, showing evidence of inter-brain coupling when people engage in behaviourally coupled interactions (Dumas et al, 2010).…”

“…The power spectra of the two conditions were compared across two frequency ranges of interest: alpha (8-12) and beta (13-30 Hz) using the cluster permutation test. These frequency bands were selected based on previous research showing modulation of sensorimotor rhythms during social interaction or observation of motor actions (Caetano et al, 2007, Tognoli et al, 2007, Kilner et al, 2009, Dumas et al, 2012, Lachat et al, 2012.…”

“…In addition to quantifying synchronized and symmetric brain-networks between brains, some dual-EEG studies have also shown asymmetric brain-coupling patterns between leader-follower participants of a dyad (Babiloni et al, 2007, Dumas et al, 2012, Sanger et al, 2012. This asymmetry has been reported either as functional connectivity (i.e.…”