Evaluating initial usability of a hand augmentation device across a large and diverse sample.

The advancement of motor augmentation and the broader domain of human-machine interaction rely on a seamless integration with users' physical and cognitive capabilities. These considerations may markedly fluctuate among individuals on the basis of their age, form, and abilities. There is a need to develop a standard for considering these diversity needs and preferences to guide technological development, and large-scale testing can provide us with evidence for such considerations. Public engagement events provide an important opportunity to build a bidirectional discourse with potential users for the codevelopment of inclusive and accessible technologies. We exhibited the Third Thumb, a hand augmentation device, at a public engagement event and tested participants from the general public, who are often not involved in such early technological development of wearable robotic technology. We focused on wearability (fit and control), ability to successfully operate the device, and ability levels across diversity factors relevant for physical technologies (gender, handedness, and age). Our inclusive design was successful in 99.3% of our diverse sample of 596 individuals tested (age range from 3 to 96 years). Ninety-eight percent of participants were further able to successfully manipulate objects using the extra thumb during the first minute of use, with no significant influences of gender, handedness, or affinity for hobbies involving the hands. Performance was generally poorer among younger children (aged ≤11 years). Although older and younger adults performed the task comparably, we identified age costs with the older adults. Our findings offer tangible demonstration of the initial usability of the Third Thumb for a broad demographic.

Biomimetic versus arbitrary motor control strategies for bionic hand skill learning.

A long-standing engineering ambition has been to design anthropomorphic bionic limbs: devices that look like and are controlled in the same way as the biological body (biomimetic). The untested assumption is that biomimetic motor control enhances device embodiment, learning, generalization and automaticity. To test this, we compared biomimetic and non-biomimetic control strategies for non-disabled participants when learning to control a wearable myoelectric bionic hand operated by an eight-channel electromyography pattern-recognition system. We compared motor learning across days and behavioural tasks for two training groups: biomimetic (mimicking the desired bionic hand gesture with biological hand) and arbitrary control (mapping an unrelated biological hand gesture with the desired bionic gesture). For both trained groups, training improved bionic limb control, reduced cognitive reliance and increased embodiment over the bionic hand. Biomimetic users had more intuitive and faster control early in training. Arbitrary users matched biomimetic performance later in training. Furthermore, arbitrary users showed increased generalization to a new control strategy. Collectively, our findings suggest that biomimetic and arbitrary control strategies provide different benefits. The optimal strategy is probably not strictly biomimetic, but rather a flexible strategy within the biomimetic-to-arbitrary spectrum, depending on the user, available training opportunities and user requirements.

Correction: Gender imbalances in the editorial activities of a selective journal run by academic editors.

[This corrects the article DOI: 10.1371/journal.pone.0294805.].

Does Ipsilateral Remapping Following Hand Loss Impact Motor Control of the Intact Hand?

What happens once a cortical territory becomes functionally redundant? We studied changes in brain function and behavior for the remaining hand in humans (male and female) with either a missing hand from birth (one-handers) or due to amputation. Previous studies reported that amputees, but not one-handers, show increased ipsilateral activity in the somatosensory territory of the missing hand (i.e., remapping). We used a complex finger task to explore whether this observed remapping in amputees involves recruiting more neural resources to support the intact hand to meet greater motor control demands. Using basic fMRI analysis, we found that only amputees had more ipsilateral activity when motor demand increased; however, this did not match any noticeable improvement in their behavioral task performance. More advanced multivariate fMRI analyses showed that amputees had stronger and more typical representation-relative to controls' contralateral hand representation-compared with one-handers. This suggests that in amputees, both hand areas work together more collaboratively, potentially reflecting the intact hand's efference copy. One-handers struggled to learn difficult finger configurations, but this did not translate to differences in univariate or multivariate activity relative to controls. Additional white matter analysis provided conclusive evidence that the structural connectivity between the two hand areas did not vary across groups. Together, our results suggest that enhanced activity in the missing hand territory may not reflect intact hand function. Instead, we suggest that plasticity is more restricted than generally assumed and may depend on the availability of homologous pathways acquired early in life.

Gender imbalances in the editorial activities of a selective journal run by academic editors.

The fairness of decisions made at various stages of the publication process is an important topic in meta-research. Here, based on an analysis of data on the gender of authors, editors and reviewers for 23,876 initial submissions and 7,192 full submissions to the journal eLife, we report on five stages of the publication process. We find that the board of reviewing editors (BRE) is men-dominant (69%) and that authors disproportionately suggest male editors when making an initial submission. We do not find evidence for gender bias when Senior Editors consult Reviewing Editors about initial submissions, but women Reviewing Editors are less engaged in discussions about these submissions than expected by their proportion. We find evidence of gender homophily when Senior Editors assign full submissions to Reviewing Editors (i.e., men are more likely to assign full submissions to other men (77% compared to the base assignment rate to men RE of 70%), and likewise for women (41% compared to women RE base assignment rate of 30%))). This tendency was stronger in more gender-balanced scientific disciplines. However, we do not find evidence for gender bias when authors appeal decisions made by editors to reject submissions. Together, our findings confirm that gender disparities exist along the editorial process and suggest that merely increasing the proportion of women might not be sufficient to eliminate this bias. Measures accounting for women's circumstances and needs (e.g., delaying discussions until all RE are engaged) and raising editorial awareness to women's needs may be essential to increasing gender equity and enhancing academic publication.

Lifelong learning of cognitive styles for physical problem-solving: The effect of embodied experience.

'Embodied cognition' suggests that our bodily experiences broadly shape our cognitive capabilities. We study how embodied experience affects the abstract physical problem-solving styles people use in a virtual task where embodiment does not affect action capabilities. We compare how groups with different embodied experience - 25 children and 35 adults with congenital limb differences versus 45 children and 40 adults born with two hands - perform this task, and find that while there is no difference in overall competence, the groups use different cognitive styles to find solutions. People born with limb differences think more before acting but take fewer attempts to reach solutions. Conversely, development affects the particular actions children use, as well as their persistence with their current strategy. Our findings suggest that while development alters action choices and persistence, differences in embodied experience drive changes in the acquisition of cognitive styles for balancing acting with thinking.

Against cortical reorganisation.

Neurological insults, such as congenital blindness, deafness, amputation, and stroke, often result in surprising and impressive behavioural changes. Cortical reorganisation, which refers to preserved brain tissue taking on a new functional role, is often invoked to account for these behavioural changes. Here, we revisit many of the classical animal and patient cortical remapping studies that spawned this notion of reorganisation. We highlight empirical, methodological, and conceptual problems that call this notion into doubt. We argue that appeal to the idea of reorganisation is attributable in part to the way that cortical maps are empirically derived. Specifically, cortical maps are often defined based on oversimplified assumptions of 'winner-takes-all', which in turn leads to an erroneous interpretation of what it means when these maps appear to change. Conceptually, remapping is interpreted as a circuit receiving novel input and processing it in a way unrelated to its original function. This implies that neurons are either pluripotent enough to change what they are tuned to or that a circuit can change what it computes. Instead of reorganisation, we argue that remapping is more likely to occur due to potentiation of pre-existing architecture that already has the requisite representational and computational capacity pre-injury. This architecture can be facilitated via Hebbian and homeostatic plasticity mechanisms. Crucially, our revised framework proposes that opportunities for functional change are constrained throughout the lifespan by the underlying structural 'blueprint'. At no period, including early in development, does the cortex offer structural opportunities for functional pluripotency. We conclude that reorganisation as a distinct form of cortical plasticity, ubiquitously evoked with words such as 'take-over'' and 'rewiring', does not exist.

Reassessing referral of touch following peripheral deafferentation: The role of contextual bias.

Some amputees have been famously reported to perceive facial touch as arising from their phantom hand. These referred sensations have since been replicated across multiple neurological disorders and were classically interpreted as a perceptual correlate of cortical plasticity. Common to all these and related studies is that participants might have been influenced in their self-reports by the experimental design or related contextual biases. Here, we investigated whether referred sensations reports might be confounded by demand characteristics (e.g., compliance, expectation, suggestion). Unilateral upper-limb amputees (N = 18), congenital one-handers (N = 19), and two-handers (N = 22) were repeatedly stimulated with computer-controlled vibrations on 10 body-parts and asked to report the occurrence of any concurrent sensations on their hand(s). To further manipulate expectations, we gave participants the suggestion that some of these vibrations had a higher probability to evoke referred sensations. We also assessed similarity between (phantom) hand and face representation in primary somatosensory cortex (S1), using functional Magnetic Resonance Imaging (fMRI) multivariate representational similarity analysis. We replicated robust reports of referred sensations in amputees towards their phantom hand; however, the frequency and distribution of reported referred sensations were similar across groups. Moreover, referred sensations were evoked by stimulation of multiple body-parts and similarly reported on both the intact and phantom hand in amputees. Face-to-phantom-hand representational similarity was not different in amputees' missing hand region, compared with controls. These findings weaken the interpretation of referred sensations as a perceptual correlate of S1 plasticity and reveal the need to account for contextual biases when evaluating anomalous perceptual phenomena.

Similar somatotopy for active and passive digit representation in primary somatosensory cortex.

Scientists traditionally use passive stimulation to examine the organisation of primary somatosensory cortex (SI). However, given the close, bidirectional relationship between the somatosensory and motor systems, active paradigms involving free movement may uncover alternative SI representational motifs. Here, we used 7 Tesla functional magnetic resonance imaging to compare hallmark features of SI digit representation between active and passive tasks which were unmatched on task or stimulus properties. The spatial location of digit maps, somatotopic organisation, and inter-digit representational structure were largely consistent between tasks, indicating representational consistency. We also observed some task differences. The active task produced higher univariate activity and multivariate representational information content (inter-digit distances). The passive task showed a trend towards greater selectivity for digits versus their neighbours. Our findings highlight that, while the gross features of SI functional organisation are task invariant, it is important to also consider motor contributions to digit representation.

Should bionic limb control mimic the human body? Impact of control strategy on bionic hand skill learning.

A longstanding engineering ambition has been to design anthropomorphic bionic limbs: devices that look like and are controlled in the same way as the biological body (biomimetic). The untested assumption is that biomimetic motor control enhances device embodiment, learning, generalization, and automaticity. To test this, we compared biomimetic and non-biomimetic control strategies for able-bodied participants when learning to operate a wearable myoelectric bionic hand. We compared motor learning across days and behavioural tasks for two training groups: Biomimetic (mimicking the desired bionic hand gesture with biological hand) and Arbitrary control (mapping an unrelated biological hand gesture with the desired bionic gesture). For both trained groups, training improved bionic limb control, reduced cognitive reliance, and increased embodiment over the bionic hand. Biomimetic users had more intuitive and faster control early in training. Arbitrary users matched biomimetic performance later in training. Further, arbitrary users showed increased generalization to a novel control strategy. Collectively, our findings suggest that biomimetic and arbitrary control strategies provide different benefits. The optimal strategy is likely not strictly biomimetic, but rather a flexible strategy within the biomimetic to arbitrary spectrum, depending on the user, available training opportunities and user requirements.

Stable Cortical Body Maps Before and After Arm Amputation.

Neuroscientists have long debated the adult brain's capacity to reorganize itself in response to injury. A driving model for studying plasticity has been limb amputation. For decades, it was believed that amputation triggers large-scale reorganization of cortical body resources. However, these studies have relied on cross-sectional observations post-amputation, without directly tracking neural changes. Here, we longitudinally followed adult patients with planned arm amputations and measured hand and face representations, before and after amputation. By interrogating the representational structure elicited from movements of the hand (pre-amputation) and phantom hand (post-amputation), we demonstrate that hand representation is unaltered. Further, we observed no evidence for lower face (lip) reorganization into the deprived hand region. Collectively, our findings provide direct and decisive evidence that amputation does not trigger large-scale cortical reorganization.

Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss.

Cortical remapping after hand loss in the primary somatosensory cortex (S1) is thought to be predominantly dictated by cortical proximity, with adjacent body parts remapping into the deprived area. Traditionally, this remapping has been characterised by changes in the lip representation, which is assumed to be the immediate neighbour of the hand based on electrophysiological research in non-human primates. However, the orientation of facial somatotopy in humans is debated, with contrasting work reporting both an inverted and upright topography. We aimed to fill this gap in the S1 homunculus by investigating the topographic organisation of the face. Using both univariate and multivariate approaches we examined the extent of face-to-hand remapping in individuals with a congenital and acquired missing hand (hereafter one-handers and amputees, respectively), relative to two-handed controls. Participants were asked to move different facial parts (forehead, nose, lips, tongue) during functional MRI (fMRI) scanning. We first confirmed an upright face organisation in all three groups, with the upper-face and not the lips bordering the hand area. We further found little evidence for remapping of both forehead and lips in amputees, with no significant relationship to the chronicity of their phantom limb pain (PLP). In contrast, we found converging evidence for a complex pattern of face remapping in congenital one-handers across multiple facial parts, where relative to controls, the location of the cortical neighbour - the forehead - is shown to shift away from the deprived hand area, which is subsequently more activated by the lips and the tongue. Together, our findings demonstrate that the face representation in humans is highly plastic, but that this plasticity is restricted by the developmental stage of input deprivation, rather than cortical proximity.

Making sense of phantom limb pain.

Phantom limb pain (PLP) impacts the majority of individuals who undergo limb amputation. The PLP experience is highly heterogenous in its quality, intensity, frequency and severity. This heterogeneity, combined with the low prevalence of amputation in the general population, has made it difficult to accumulate reliable data on PLP. Consequently, we lack consensus on PLP mechanisms, as well as effective treatment options. However, the wealth of new PLP research, over the past decade, provides a unique opportunity to re-evaluate some of the core assumptions underlying what we know about PLP and the rationale behind PLP treatments. The goal of this review is to help generate consensus in the field on how best to research PLP, from phenomenology to treatment. We highlight conceptual and methodological challenges in studying PLP, which have hindered progress on the topic and spawned disagreement in the field, and offer potential solutions to overcome these challenges. Our hope is that a constructive evaluation of the foundational knowledge underlying PLP research practices will enable more informed decisions when testing the efficacy of existing interventions and will guide the development of the next generation of PLP treatments.

Malleability of the cortical hand map following a finger nerve block.

Electrophysiological studies in monkeys show that finger amputation triggers local remapping within the deprived primary somatosensory cortex (S1). Human neuroimaging research, however, shows persistent S1 representation of the missing hand's fingers, even decades after amputation. Here, we explore whether this apparent contradiction stems from underestimating the distributed peripheral and central representation of fingers in the hand map. Using pharmacological single-finger nerve block and 7-tesla neuroimaging, we first replicated previous accounts (electrophysiological and other) of local S1 remapping. Local blocking also triggered activity changes to nonblocked fingers across the entire hand area. Using methods exploiting interfinger representational overlap, however, we also show that the blocked finger representation remained persistent despite input loss. Computational modeling suggests that both local stability and global reorganization are driven by distributed processing underlying the topographic map, combined with homeostatic mechanisms. Our findings reveal complex interfinger representational features that play a key role in brain (re)organization, beyond (re)mapping.

Beyond body maps: Information content of specific body parts is distributed across the somatosensory homunculus.

The homunculus in primary somatosensory cortex (S1) is famous for its body part selectivity, but this dominant feature may eclipse other representational features, e.g., information content, also relevant for S1 organization. Using multivariate fMRI analysis, we ask whether body part information content can be identified in S1 beyond its primary region. Throughout S1, we identify significant representational dissimilarities between body parts but also subparts in distant non-primary regions (e.g., between the hand and the lips in the foot region and between different face parts in the foot region). Two movements performed by one body part (e.g., the hand) could also be dissociated well beyond its primary region (e.g., in the foot and face regions), even within Brodmann area 3b. Our results demonstrate that information content is more distributed across S1 than selectivity maps suggest. This finding reveals underlying information contents in S1 that could be harnessed for rehabilitation and brain-machine interfaces.

Going beyond primary motor cortex to improve brain-computer interfaces.

Brain-computer interfaces (BCIs) for movement restoration typically decode the user's intent from neural activity in their primary motor cortex (M1) and use this information to enable 'mental control' of an external device. Here, we argue that activity in M1 has both too little and too much information for optimal decoding: too little, in that many regions beyond it contribute unique motor outputs and have movement-related information that is absent or otherwise difficult to resolve from M1 activity; and too much, in that motor commands are tangled up with nonmotor processes such as attention and feedback processing, potentially hindering decoding. Both challenges might be circumvented, we argue, by integrating additional information from multiple brain regions to develop BCIs that will better interpret the user's intent.

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.

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.