Expert tool users show increased differentiation between visual representations of hands and tools

The idea that when we use a tool we incorporate it into the neural representation of our body (embodiment) has been a major inspiration for philosophy, science and engineering. While theoretically appealing, there is little direct evidence for tool embodiment at the neural level. Using functional magnetic resonance imaging (fMRI) in male and female human subjects, we investigated whether expert tool users (London litter pickers: n=7) represent their expert tool more like a hand (neural embodiment) or less like a hand (neural differentiation), as compared to a group of tool novices (n=12). During fMRI scans, participants viewed first-person videos depicting grasps performed by either a hand, litter picker or a non-expert grasping tool. Using representational similarity analysis, differences in the representational structure of hands and tools were measured within occipitotemporal (OTC). Contrary to the neural embodiment theory, we find that the experts group represent their own tool less like a hand (not more) relative to novices. Using a case-study approach, we further replicated this effect, independently, in 5 of the 7 individual expert litter pickers, as compared to the novices. An exploratory analysis in left parietal cortex, a region implicated in visuomotor representations of hands and tools, also indicated that experts do not visually represent their tool more similar to hands, compared to novices. Together, our findings suggest that extensive tool use leads to an increased neural differentiation between visual representations of hands and tools. This evidence provides an important alternative framework to the prominent tool embodiment theory

Robotic hand augmentation drives changes in neural body representation

Humans have long been fascinated by the opportunities afforded through augmentation. This vision not only depends on technological innovations but also critically relies on our brain's ability to learn, adapt, and interface with augmentation devices. Here, we investigated whether successful motor augmentation with an extra robotic thumb can be achieved and what its implications are on the neural representation and function of the biological hand. Able-bodied participants were trained to use an extra robotic thumb (called the Third Thumb) over 5 days, including both lab-based and unstructured daily use. We challenged participants to complete normally bimanual tasks using only the augmented hand and examined their ability to develop hand-robot interactions. Participants were tested on a variety of behavioral and brain imaging tests, designed to interrogate the augmented hand's representation before and after the training. Training improved Third Thumb motor control, dexterity, and hand-robot coordination, even when cognitive load was increased or when vision was occluded. It also resulted in increased sense of embodiment over the Third Thumb. Consequently, augmentation influenced key aspects of hand representation and motor control. Third Thumb usage weakened natural kinematic synergies of the biological hand. Furthermore, brain decoding revealed a mild collapse of the augmented hand's motor representation after training, even while the Third Thumb was not worn. Together, our findings demonstrate that motor augmentation can be readily achieved, with potential for flexible use, reduced cognitive reliance, and increased sense of embodiment. Yet, augmentation may incur changes to the biological hand representation. Such neurocognitive consequences are crucial for successful implementation of future augmentation technologies

Motor control drives visual bodily judgements

The ‘embodied cognition’ framework proposes that our motor repertoire shapes visual perception and cognition. But recent studies showing normal visual body representation in individuals born without hands challenges the contribution of motor control on visual body representation. Here, we studied hand laterality judgements in three groups with fundamentally different visual and motor hand experiences: two-handed controls, one-handers born without a hand (congenital one-handers) and one-handers with an acquired amputation (amputees). Congenital one-handers, lacking both motor and first-person visual information of their missing hand, diverged in their performance from the other groups, exhibiting more errors for their intact hand and slower reaction-times for challenging hand postures. Amputees, who have lingering non-visual motor control of their missing (phantom) hand, performed the task similarly to controls. Amputees’ reaction-times for visual laterality judgements correlated positively with their phantom hand’s motor control, such that deteriorated motor control associated with slower visual laterality judgements. Finally, we have implemented a computational simulation to describe how a mechanism that utilises a single hand representation in congenital one-handers as opposed to two in controls, could replicate our empirical results. Together, our findings demonstrate that motor control is a driver in making visual bodily judgments

Early life experience sets hard limits on motor learning as evidenced from artificial arm use

The study of artificial arms provides a unique opportunity to address long-standing questions on sensorimotor plasticity and development. Learning to use an artificial arm arguably depends on fundamental building blocks of body representation and would therefore be impacted by early-life experience. We tested artificial arm motor-control in two adult populations with upper-limb deficiencies: a congenital group - individuals who were born with a partial arm, and an acquired group - who lost their arm following amputation in adulthood. Brain plasticity research teaches us that the earlier we train to acquire new skills (or use a new technology) the better we benefit from this practice as adults. Instead, we found that although the congenital group started using an artificial arm as toddlers, they produced increased error noise and directional errors when reaching to visual targets, relative to the acquired group who performed similarly to controls. However, the earlier an individual with a congenital limb difference was fitted with an artificial arm, the better their motor control was. Since we found no group differences when reaching without visual feedback, we suggest that the ability to perform efficient visual-based corrective movements is highly dependent on either biological or artificial arm experience at a very young age. Subsequently, opportunities for sensorimotor plasticity become more limited

Cognitive and neural embodiment of artificial-arms in individuals with hand-absence

In the typically developed brain, numerous networks and regions are involved in sensing, actuating and understanding hand functions. In this thesis I take a neurocognitive approach to provide a better understating of how prosthesis users harness hand-specific resources to support their prosthetic limb (embodiment). In a series of cognitive, motor and neural studies, I test two distinct populations: congenital one-handers who are born without a hand and acquired amputees who lost their hand in adulthood, to investigate the processes underlying upper-limb prosthesis use. First, available hand-related resources were assessed in each of the tested populations using a visual hand laterality task. Congenital one-handers were less efficient than amputees in processing visual hand information, possibly due to atypical available motor hand resources. This finding reaffirms the notion of 'embodied cognition' – that our motor repertoire shapes visual perception and cognition. This was further supported by a significant relationship between amputees’ ability to move their phantom hand and their visual hand processing efficiency. Within the embodiment framework presented in this thesis, having different hand resources could potentially lead to different capabilities in prosthetic-limb use. Next, using fMRI brain decoding analysis, I probed the neural representation of prostheses in relation to hands and tools, within the visual cortex. Increased levels of prosthesis use were associated with a formation of a novel neural visual ‘prosthesis’ category. This experience-dependent plasticity was observed in both congenital one-handers and amputees, pointing towards high levels of flexibility in occipitotemporal cortex. These findings challenge the naïve notion of neural embodiment, since prosthesis representation did not become more similar to hand representation. Finally, the control dynamics of prosthetic-arms were assessed using several reaching and localisation tasks. Motor reaching accuracy with a prosthesis was found to depend on early life experience with a hand (either prosthetic or biological). Specifically, the ability to efficiently perform visually guided reaches with a prosthesis is impaired in the absence of early experience. These findings point towards a possible reliance of prosthesis use on neural hand-specific processes and provide evidence for a sensitive developmental period for sensorimotor control. Taken together, this thesis provides a comprehensive overview of the multifaceted phenomenon of embodiment, shedding light on the underlying processes supporting human-machine interactions, and expanding our understanding of the development and plasticity of body representation.</p

Talking with Your (Artificial) Hands: Communicative Hand Gestures as an Implicit Measure of Embodiment

When people talk, they move their hands to enhance meaning. Using accelerometry, we measured whether people spontaneously use their artificial limbs (prostheses) to gesture, and whether this behavior relates to everyday prosthesis use and perceived embodiment. Perhaps surprisingly, one- and two-handed participants did not differ in the number of gestures they produced in gesture-facilitating tasks. However, they did differ in their gesture profile. One-handers performed more, and bigger, gesture movements with their intact hand relative to their prosthesis. Importantly, one-handers who gestured more similarly to their two-handed counterparts also used their prosthesis more in everyday life. Although collectively one-handers only marginally agreed that their prosthesis feels like a body part, one-handers who reported they embody their prosthesis also showed greater prosthesis use for communication and daily function. Our findings provide the first empirical link between everyday prosthesis use habits and perceived embodiment and a novel means for implicitly indexing embodiment