Crossmodal representation of a functional robotic hand arises after extensive training in healthy participants

Abstract

The way in which humans represent their own bodies is critical in guiding their interactions with the environment. To achieve successful body-space interactions, the body representation is strictly connected with that of the space immediately surrounding it through efficient visuo-tactile crossmodal integration. Such a body-space integrated representation is not fixed, but can be dynamically modulated by the use of external tools. Our study aims to explore the effect of using a complex tool, namely a functional prosthesis, on crossmodal visuo-tactile spatial interactions in healthy participants. By using the crossmodal visuo-tactile congruency paradigm, we found that prolonged training with a mechanical hand capable of distal hand movements and providing sensory feedback induces a pattern of interference, which is not observed after a brief training, between visual stimuli close to the prosthesis and touches on the body. These results suggest that after extensive, but not short, training the functional prosthesis acquires a visuo-tactile crossmodal representation akin to real limbs. This finding adds to previous evidence for the embodiment of functional prostheses in amputees, and shows that their use may also improve the crossmodal combination of somatosensory feedback delivered by the prosthesis with visual stimuli in the space around it, thus effectively augmenting the patients' visuomotor abilities.

Dynamic expansion of alert responses to incoming painful stimuli following tool use

“…This finding would be crucial for research on brain augmentation devices (Di Pino et al, 2014) or prosthetics for amputees (Romano et al, 2015). Indeed, ideal functional augmentation devices maybe charged of a sense of protection and emotional monitoring, besides their critical sensorimotor function (see Di Pino et al, 2014;Marini et al, 2014), body-space integration, as a complete and deep process of embodiment.…”

Augmentation-related brain plasticity

“…Moreover, as it happens for the real hands, the embodiment of the prosthesis should produce a cross-modal integration of tactile afferences with visual stimuli coming from the surroundings of the prosthesis, in order to ameliorate manipulation and sensory anticipation of stimuli in its surrounding environment. In healthy participants, long-term use of an electromyographic signal-driven detached robotic hand, able to provide substitutionary sensory feedback from its fingers via vibrotactile stimulation, produces a pattern of visuo-tactile interference from visual stimuli close to the prosthesis fingers, over tactile stimuli referred to the same fingers, in the cross-modal congruency effect, as typically shown when testing the real hand (Figure 1C; Marini et al, 2014). …”

“…As discussed previously, a key role of functional prostheses is to allow the rebuilt of a full sense of ownership and agency of the prosthesis through a process of training-induced, embodiment (Ehrsson et al, 2008; Marasco et al, 2011; D’Alonzo and Cipriani, 2012; Mulvey et al, 2012). In this respect, the plasticity induced by functional prostheses (Di Pino et al, 2009; Rossini et al, 2010; Maruishi et al, 2004), targets similar sensorimotor brain areas as those modulated by paradigms inducing illusory sense of ownership for alien body parts and could constitute the basis of a full inclusion of external devices into the self as well as the extension of visuo-tactile integration properties to an external augmentation device (Marini et al, 2014). …”

“…Prolonged use of an electromyography-driven, detached robot hand (drawn in gray on the right side of the table) providing sensory feedback referred to the participant’s arm (white circles), increased the interference from visual distracter leds located near the robot hand fingers (reddish shadowed circles) tested with the crossmodal congruency paradigm (right panel, light blue columns), as compared to the pre-training assessment (right panel, green columns). This pattern of results suggests a training-dependent expansion of crossmodal integration properties, typical of the peripersonal space near the body, to the space surrounding the robot hand (Marini et al, 2014). …”

Reward prospect interacts with trial-by-trial preparation for potential distraction

“…Inverse efficiency is defined as the ratio between the mean RT and the proportion of correct responses, thereby allowing adjusting for speed-accuracy trade-offs. In tasks where both speed and accuracy index performance, inverse efficiency has been widely used in the domain of distraction filtering (Marini et al, 2013) as well as in studies of visual attention (e.g., Austen & Enns, 2003) and crossmodal perception (e.g., Heed, Habetz, Sebanz, & Knoblich, 2010; Marini, Tagliabue, Sposito, Hernandez-Arieta et al, 2014). IE values are actually identical to RTs when accuracy is at 100% and increase proportionally with increases in the error rate (e.g., a mean RT of 600 ms combined with an accuracy of 90% would give an IE = 600/.90 = 667 ms a , where here we use the subscript “a” to show that the unit form of IE is an adjusted ms value).…”