Dynamics of sensorimotor plasticity during spatial finger augmentation

  1. Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands

Peer review process

Not revised: This Reviewed Preprint includes the authors’ original preprint (without revision), an eLife assessment, and public reviews.

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Editors

  • Reviewing Editor
    Tamar Makin
    University of Cambridge, Cambridge, United Kingdom
  • Senior Editor
    Tamar Makin
    University of Cambridge, Cambridge, United Kingdom

Reviewer #1 (Public review):

This study by Radziun and colleagues investigates the effects of using a hand-augmentation device on mental body representations. The authors use a proprioceptive localisation task to measure metric representations of finger length before and after participants wear the device, and then before and after they learn to use the device, which extends the lengths of the fingers by 10 cm. The authors find changes between different time points, which they interpret as evidence for three distinct forms of plasticity: one related to simply wearing the device, one related to learning to use it, and an aftereffect after taking the device off. A control experiment with a similar device, which does not lengthen the fingers, showed the first and third of these forms of plasticity, but not the second.

This study takes an interesting approach to a timely and theoretically significant issue. The study appears to be appropriately designed and conducted. There are, however, some points which require clarification.

(1) The nature of the localization task is unclear. On its face, the task appears to involve localization of each landmark within the 2-dimensional surface of the touchscreen. However, the regression analysis presupposes that localization is made in a 1-dimensional space. Figure S2 shows that three lines are presented on the screen above the index, middle, and ring fingers, which I imagine the participant is meant to use as a guide. But it is at least conceivable that the perceived location or orientation of the finger might not correspond exactly to these lines. While the method can deal gracefully with proximal-distal translations of the fingers (i.e., with the intercept parameter of the regression), it isn't clear how the participant is supposed to respond if their proprioceptive perception of finger location is translated left-right or rotated relative to the lines on the screen. I also worry that presenting a long, thin line to represent each finger on the screen may not be a neutral method and may prime participants to represent the finger as long and thin.

(2) The task used here fits within a wider family of tasks in the literature using localization judgments of multiple landmarks to map body representations. I feel that some discussion of this broader set of tasks and their use to measure body representation and plasticity is notably absent from the paper. It is also striking to me that some of the present authors have themselves recently criticized the use of landmark localization methods as a measure of represented body size and shape (Peviani et al, 2024, Current Biology). It is therefore surprising to see them use this task here as a measure of represented finger length without commenting on this issue.

(3) 18 participants strikes me as a relatively small sample size for this type of study. It weakens the manuscript that the authors do not provide any justification, or even comment on, the sample size. This is especially true as participants are excluded from the entire sample, and from specific analyses, on rather post-hoc grounds.

(4) I have some concerns about the interpretation of contraction in stage 2. The authors claim that wearing the finger extended produces "a contraction",i.e., an "under-representation" (page 12). But in both experiments, regression slopes in stage 2 were not significantly different from 1 (i.e., 0.98 [SE: 0.07] in Exp 1a and 1.04 [SE: 0.09] in Experiment 1b). So how can that be interpreted as "under-representation"?

(5) I also have concerns about the interpretation of the stretch that is claimed to occur following training. In Exp 1a, regression slopes in stage 3 are on average 1.15. That is LESS than in the pretest at stage 1 (mean: 1.16). The idea of stretch only comes about because of the lower slopes in stage 2, which the authors have interpreted as reflecting contraction. So what the authors call stretch and a 2nd form of plasticity could just be the contraction from stage 2 wearing off or dissipating, since perceived finger length in stage 3 just appears to return to the baseline level seen in stage 1. While the authors describe their results in terms of three distinct forms of plasticity, these are not in fact statistically independent. The dip in regression slopes in stage 2 is interpreted as evidence for two distinct plasticity effects, which I do not find convincing.

(6) The distinction between plasticity at stage 3 (which appears specific to augmentation) and plasticity at stage 4 (which does not appear specific, as it also occurs in Experiment 1b) feels strained. This feels like a very subtle distinction, and the theoretical significance of it is not convincingly developed.

(7) The reporting of statistics is not always consistent. For example, 95%CIs are presented for regression slopes in stages 1, 3, and 4, but not for stage 2. Statistics are performed on regression slopes, except for one t-test on page 7 comparing lengths in cm. Estimates of effect size would be nice additions to statistical tests.

(8) Minor point: On page 4, the authors write, "These included sorting colored blocks, stacking a Jenga tower, and sorting pegs into holes; the latter task required fine-grained manipulation and was used as our outcome measure of motor learning." This suggests that peg sorting was the outcome measure, but in Figure 1D, Jenga is presented as the outcome measure.

Reviewer #2 (Public review):

Summary:

This study aimed to explore dynamic changes in the somatosensory representation of both the body and artificial body parts. The study investigated how proprioceptive localisation along the finger changes when participants wear, actively use, and then remove a hand augmentation device - a rigid finger-extension. By mapping perceived target locations along the biological finger and the extension across multiple stages, the authors aim to characterise how the somatosensory system updates our spatial body representation during and after interaction with body augmentation technology.

Strengths:

The manuscript addresses an interesting question of how augmentation devices alter proprioceptive localisation abilities. Conceptually, the work moves beyond classic tool-use paradigms by focusing on a device that is used with the hand to extend the fingers' abilities (versus a tool that is simply used by the hand), and by attempting to map perceived spatial structure across both biological and artificial segments within the same framework.

A major strength is the multi-stage design, which samples localisation abilities at baseline, the beginning of device wear, post-training, and immediately post-removal. This provides a richer characterisation of short-term adaptation compared to a simple pre/post comparison. The dense sampling across stages and target locations generates a rich behavioural dataset that will be valuable to readers interested in somatosensory body representation. The within-subject, counterbalanced control session further strengthens interpretability, providing a useful comparison for interpreting stage-dependent effects, and to probe how functional training shapes changes in the perceptual representations. Finally, the augmentation device itself appears carefully engineered, with thoughtful design decisions regarding wearability, including comfort and customised fit. The manuscript is also communicated clearly, with transparent reporting of analyses and succinct figures that make the pattern changes across stages straightforward to evaluate.

Weaknesses:

There is conceptual ambiguity in how the regression outcomes are interpreted in relation to perceived length and spatial integration. The manuscript treats regression slope as a proxy for "length perception" and discards the intercept as "spatial bias," but in this localisation task translation (intercept) and scaling (slope) are coupled: changes in anchoring at the proximal baseline (intercept) or distal endpoint can generate slope differences without uniform rescaling across the mapped surface. Relatedly, the analyses do not establish whether the reported effects are global across targets or disproportionately driven by the most distal locations. This limits the strength of inferences about "partitioning" or "reallocation" of representational space across biological and artificial segments. Some interpretive statements also appear stronger than the evidence supports (e.g., describing the stage 2 bio-extension map as "geometrically accurate", despite Bayes factors that provide only anecdotal support for no difference from true length). Extensive repeated judgements to a fixed set of locations may additionally stabilise response strategies or anchoring even without feedback, complicating the separation of body-representation change from task-specific calibration.

The manuscript would also benefit from clearer conceptual framing of what the device is and what its training probes are. The device is described variably as an "artificial finger" versus a rigid "finger extension," with different implications for perception and function. In addition, the training tasks appear to emphasise manipulation and dexterity more than scenarios requiring an extended reachable workspace (indeed, participants appear to have performed at least as well, if not better, in the control training), which brings into question whether participants explored the device's intended functionality and possible proprioceptive consequences. The control experiment is thoughtfully designed to test whether functional training contributes to the stage 3 changes, but because localisation is not performed while wearing the short device, the design does not resolve whether the stage 2 change and the post-removal aftereffect are specific to the augmentative extension versus more general consequences of wearing a device on the finger (and the following possible distorted distal cues).

Finally, the immediate post-removal aftereffects are intriguing, but the mechanistic interpretation remains underspecified. As presented within the internal model framework, the magnitude and consistency of the aftereffect following brief exposure are difficult to reconcile with the stability expected from a lifetime biological finger model, and because the aftereffect is assessed only immediately after removal, its time course and functional significance remain unclear.

Reviewer #3 (Public review):

Summary:

The study aims to investigate sensorimotor plasticity mechanisms by exposing a cohort of 20 subjects to manipulation activities while using wearable finger extensions. With a series of experiments involving localization and motor tasks, the authors provide evidence that the finger extensions are integrated into the body representation of the subjects.

Strengths:

The study deserves attention, and the psychophysical protocols are carefully designed, and the statistical analyses are solid.

Weaknesses:

However, the current version of the manuscript, in my opinion, makes an exaggerated use of the term plasticity, and this should be amended. This is because the authors support the plasticity claims with psychophysical experiments, without providing evidence of neural-plasticity mechanisms (e.g., neuroimaging methods are not used).

The authors are recommended to revise the wording of the manuscript and possibly perform additional experiments with brain imaging methods (e.g., EEG or fMRI).

  1. Howard Hughes Medical Institute
  2. Wellcome Trust
  3. Max-Planck-Gesellschaft
  4. Knut and Alice Wallenberg Foundation