Muscle anatomy of the macaque forearm and the tendon transfer procedure.

A schematic of the primary forearm muscles involved in the study, showing both the dorsal and volar views. The diagram illustrates the surgical crossed tendon transfer of the extensor digitorum communis (EDC) and flexor digitorum superficialis (FDS) tendons. All labeled muscles were implanted with EMG electrodes. Muscle Abbreviations: BRD: brachioradialis, ECR: extensor carpi radialis, ECU: extensor carpi ulnaris, ED2,3: extensor digitorum-2,3, ED4,5: extensor digitorum-4,5, EPL: extensor pollicis longus (not implanted), FCR: flexor carpi radialis, FCU: flexor carpi ulnaris, FDP: flexor digitorum profundus, PL: palmaris longus, PT: pronator teres (not implanted), (The deltoid (DEL) muscle was also implanted in Monkey B but is not shown as it is a shoulder muscle). See also Supplementary Table 1 for a complete list of all muscle abbreviations, their full names, and their assigned synergies.

Long term confirmation of tendon surgery effectiveness to alter mechanical properties.

(A) Set-up for the ultrasound measurement and video recordings of the stimulation induced movements of the EDC and FDS tendons. (B) Sonogram of the FDS muscle and its intramuscular tendons. Left side (B-mode, i.e., brightness mode) shows the still image of the monkeys forearm at a given point in time. Right side (M-mode, i.e., motion mode) shows the stagged images of the FDS tendon displacement induced by muscle stimulation (50mA). White arrows demarcate the FDS tendon which was used for the measurement. Grayscale gradations correspond to tissue densities: hyperechoic regions (white) denote denser structures like surface of bones and tendons, while hypoechoic areas (black) signify less dense tissues such as adipose tissue and musculature. Inset demonstrates the area measurement. The area of the displacement waves was measured in the M-mode, representing the strength of muscle contraction. We measured the duration (a, sec) and amplitude (b, cm) of three waves and calculated the average. Area = a*b/2(cm/sec) for days 0, 7 and 105 after tendon transfer. (C) Areas under the wave measured in the M-mode for 3 experimental days (0, 7 and 105 days post-TT) and regression lines in red and blue for FDS and EDC, respectively. R2>0.5 for FDS. The data suggested that muscle contractions induced by direct electrical stimulation were nearly constant. (D) Markers placed on the index, middle and ring finger nails (A) were used to measure finger displacement in xyz-dimensions. We calculated the sum of the Euclidean distances of each marker from the origin of the 3D coordinate system as a scalar quantity. Observing the movement along the Z-axis, it became reversed post-surgery indicating a reversal from finger flexion to extension due to tendon transfer (D, blue = pre-TT at surgery day; dark brown = post-TT at surgery day; light brown = 1wk post-TT; red = 3wks post-TT). The scalar quantity of the fingers during muscle stimulation did not change much at day 0, 7 and 105 days (E), suggesting that there was no tendon rupture or slackening of the tendons postoperatively (EDC stimulation, left; FDS stimulation, right). Data were collected in monkey A.

Experimental set-up, task sequence and typical EMG (monkey A).

(A) Schematic of the task object using a rod requiring monkey A to perform a controlled grasp. (B) Schematic of the behavioral sequence (hook → grasp → release). (C) Typical EMG traces of a control session (high-pass filtered) for all recorded muscles. Gray boxes represent the task sequence. Obj 1 ON: start of the hold period of object 1. Obj 1 OFF: end of the hold period of object 1, i.e., object release. Obj 2 ON: start of the hold period of object 2. Obj 2 OFF: end of the hold period of object 2, i.e., object release. Tendons of the muscles marked with * were cross-transferred. (D) Rectified and smoothed EMG for all recorded muscles (average for one recording session; amplitude [μV] over task sequence [%]). Horizontal bars illustrate the corresponding behavioral periods; red vertical lines indicate peak amplitude for each muscle). (E) The time the monkey spent on the left side of the yellow dotted line while moving from object 1 to object 2 was measured and used to quantify the maladaptive behavior.

Experimental set-up, task sequence and typical EMG (monkey B).

(A) Schematic of the task requiring monkey B to pick up food from a groove allowing for a more natural grasp. (B) Schematic of the task sequence (picking up food). (C) Typical EMG traces of a control session (high-pass filtered) for all recorded muscles. Gray boxes represent the task. Obj 1 ON: start of the hold period of object 1. Obj 1 OFF: end of object 1’s hold period, i.e. object release. LED ON: approximate start of the food touch. LED OFF: approximate time of food retrieval. Tendons of the muscles marked with * were cross-transferred. (D) rectified and smoothed EMG for all recorded muscles (average for one recording session; amplitude [μV] over task sequence [%]). Horizontal bars illustrate the corresponding behavioral periods, red vertical lines indicate peak amplitude for each muscle). (E) Example for maladaptive behavior in monkey B. The time the monkey spent in contact with or behind the object plate was measured and used to quantify the maladaptive behavior.

Behavioral and kinematic metrics of motor recovery.

(A, D) Grip formation times (mean ± SD; n = 20 trials) for Monkey A (A) and Monkey B (D). (B, E) Duration of off-target reaching movements (mean ± SD; n = 10 trials) for Monkey A (B) and Monkey B (E). (C) Pull time duration for Monkey A. (F) Grasp aperture size for Monkey B. Filled squares indicate significant difference from pre-TT baseline (p < 0.05, two-sample t-test). All data are plotted over days relative to tendon transfer (TT).

Temporal EMG profiles and cross-correlation analysis.

Temporal EMG profiles for Monkey A (left, A-J) and Monkey B (right, K-Q). (A-F, K-O) Average EMG activity profiles aligned to task events (0%; object release for A, food touch for B). Shaded envelopes represent standard deviations. Triangles indicate peak activity during extension (▾) or flexion (▽). Colored traces denote post-surgery landmark days. (A-D, K-M) Comparison of transferred muscles. Note the temporal shift in the post-surgery profile (B, L) relative to the pre-TT baseline (dashed lines). (E-F, N-O) Profiles of non-transferred muscles. (G-J, P-Q) Zero-lag cross-correlation coefficients between post-surgery EMG profiles and the pre-TT baseline profiles plotted over time. (H, I, P) Correlation coefficients calculated against the muscle’s own pre-TT baseline. (G, J, Q) Correlation coefficients calculated against the antagonist’s pre-TT baseline (e.g., Post-EDC vs. Pre-FDS). Black dashed lines on the right y-axis indicate behavioral error metrics (Off-target reaching time for Monkey A; Contact duration for Monkey B; gray shading represents SD). The // represents the recovery period.

Spatial structure and temporal activation of Primary Synergies.

Analysis of the two primary synergies: Synergy A (Flexor) and Synergy B (Extensor). (A, B, E, F) Spatial synergy weights (W) showing the contribution of each muscle to the synergy. Bar plots represent the average weights across all recording days. (C, D, G, H) Temporal activation profiles (C) aligned to task events (0%). Dashed lines with shaded tubes indicate the average pre-TT EMG profiles of the key contributing muscles (FDS, EDC, FDP) for visual comparison with the synergy profile. Symbols and alignment are as described in Figure 6. (I, J) Quantification of spatial stability. Cosine similarity of spatial synergy weights (W) calculated between individual recording days and the pre-TT average. Blue markers indicate pre-TT control days; Red markers indicate post-TT days. The horizontal gray shaded region (0.95-1.0) denotes the range of high baseline stability.

Analysis of Secondary Muscle Synergies.

(A-H) Analysis of Secondary Synergies C (Wrist Flexor) and D (Wrist Extensor). (A, B, E, F) Spatial synergy weights (W) showing the contribution of each muscle. (C, D, G, H) Temporal activation profiles (C) aligned to task events (0%). Colored traces denote post-surgery landmark days. Layout and symbols are as described in Figure 6. (I, J) Quantification of spatial stability for Synergies C and D. Cosine similarity of spatial weights calculated between individual recording days and the pre-TT average. Blue markers indicate pre-TT control days; Red markers indicate post-TT days. The horizontal gray shaded region (0.95-1.0) denotes the range of high baseline stability.

Cross-correlation analysis of Primary Synergy activation.

Zero-lag cross-correlation coefficients plotted over post-surgery days for Monkey A (A-D) and Monkey B (E-H). Activation patterns of the Primary Flexor (Synergy A) and Primary Extensor (Synergy B) were cross-correlated with pre-TT baseline profiles. (Top Row: A, B, E, F) Correlations calculated against the pre-TT Extensor Synergy (Synergy B, blue traces). (Bottom Row: C, D, G, H) Correlations calculated against the pre-TT Flexor Synergy (Synergy A, red traces). (C, G) Correlation of Synergy A with its own pre-TT baseline. (B, F) Correlation of Synergy B with its own pre-TT baseline. (A, E, D, H) Cross-correlations between antagonistic synergies (e.g., A is Synergy A vs. Pre-Synergy B). Black dashed lines on the right y-axis indicate behavioral error metrics (gray shading represents SD). The // represents the recovery period. Triangles indicate landmark days.

Cross-correlation analysis of Secondary Synergy activation.

Zero-lag cross-correlation coefficients for the secondary synergies (C and D) plotted over post-surgery days for Monkey A (A-D) and Monkey B (E-H). Activation patterns were cross-correlated with the pre-TT profiles of the Primary Synergies to assess changing affiliations. (Top Row: A, B, E, F) Correlations calculated against the pre-TT Extensor Synergy (Synergy B, blue traces). (Bottom Row: C, D, G, H) Correlations calculated against the pre-TT Flexor Synergy (Synergy A, red traces). (Left Columns: A, C, E, G) Synergy C correlations. (Right Columns: B, D, F, H) Synergy D correlations. Black dashed lines on the right y-axis indicate behavioral error metrics.

Aggregated and averaged EMG (aaEMG).

Aggregated and averaged electromyography (EMG) activities for the main contributing muscles of each synergy for Monkey A (A-H) and Monkey B (I-P). (A-D, I-L) Time course of aaEMG activity (summed within ±15% task range) plotted over post-surgery days. Black dashed lines on the right y-axis indicate behavioral error metrics. (E-H, M-P) Bar plots showing the mean (± SEM) aaEMG for the pre-TT period (“pre”) and the five selected landmark days. Vertical colored bars on the time-series plots indicate the corresponding landmark days. Asterisks indicate significant difference from the pre-TT control period (*p < 0.01, **p < 0.001, ***p < 0.0001; two-sample t-test with Bonferroni correction).

Kinematic analysis of joint angles (Monkey B).

Changes in joint angles (mean of 20 trials ± SD) for each landmark day. (A) Metacarpophalangeal (MCP) joint angle. (B) Wrist joint angle. Asterisks indicate significant difference from pre-TT baseline (**p < 0.001, ***p < 0.0001; ANOVA). (C) Schematic indicating the timing of the kinematic snapshot relative to the task timeline (dotted line; 83 ms before food touch), capturing the hand configuration during the pre-shaping phase.

Kinematic analysis reveals gradual refinement of the compensatory tenodesis strategy over time in Monkey

B. (A) Each subplot shows the trial-by-trial relationship between wrist angle (X-axis) and MCP angle (Y-axis) for a single recording day (n=20 trials per day). Points are color-coded based on the day relative to surgery (colorbar). Pre-TT (Day -4), no correlation exists (R²=0.00). Post-surgery, a negative correlation emerges and strengthens over time, peaking around Day 56 (R²=0.58), indicating the learned exploitation of the tenodesis effect where wrist flexion predicts finger extension. The tightening of the scatter plots and increase in R² over weeks provide direct evidence for a gradual motor skill learning process. (B) All data points combined.

A Proposed Model of Multi-Timescale Adaptation Following Tendon Transfer.

This schematic illustrates the hypothesized interaction between fast and slow adaptive processes driving recovery. The initial Tendon Transfer triggers a rapid but maladaptive ‘swap’ of motor commands (Fast Adaptation 1), leading to a maladaptive state. During this phase, two slower processes are hypothesized to occur in parallel: a costly ‘arms race’ within the conflicted synergy (Slow Process A, red curve) and the gradual development of a functional compensatory strategy (Slow Process B, green curve). When the ‘arms race’ reaches a threshold of unsustainable cost (dashed blue line), a second Fast Adaptation (’Switch-Back’, 2) is triggered. This allows for the abandonment of the flawed strategy and the adoption of a stable, ‘good enough’ solution, which is now supported by the newly learned compensatory strategy. The gray line represents the observed neural data (e.g., cross-correlation coefficients of electromyography and temporal activation profiles of muscle synergies), which reflects this two-phase process.