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, FCR: flexor carpi radialis, FCU: flexor carpi ulnaris, FDP: flexor digitorum profundus, PL: palmaris longus, PT: pronator teres, (The deltoid (DEL) muscle was also implanted in Monkey B but is not shown as it is a shoulder muscle.)

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).

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

(A) Schematic of the behavioral sequence (hook → grasp → release). (B) Schematic of the task object using a rod requiring monkey A to perform a controlled grasp. (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 mal-adaptive behavior.

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

(A) Schematic of the task sequence (picking up food). (B) Schematic of the task requiring monkey B to pick up food from a groove allowing for a more natural grasp. (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) Development of the metacarpophalangeal joint (MCP) and wrist joint angle [deg] over task range [%]. Decreasing and increasing angles indicate extension or flexion of the MCP or wrist angle, respectively. Data are aligned on LED onset (food retrieval) and indicate consistency between behavioral observation (A), EMG (C-D) and kinematics (E). (F) Illustration of joint angle measurement using a still picture of the monkey while performing the task. (G) Example for mal-adaptive behavior in monkey B. The time the monkey spent in contact with or behind the object plate was measured and used to quantify the mal-adaptive behavior.

Behavioral recovery is preceded by maladaptive motor control in both monkeys.

(A) Grip formation times. Plotted is the average time (mean ± SD, n=20 trials) from initial touch to action onset (pull or lift) for Monkey A and Monkey B. Grip formation times were significantly elevated immediately post-surgery before returning to baseline. (B) Quantification of aberrant reaching. Plotted is the average time (mean ± SD, n=10 trials) spent executing aberrant movements. For Monkey A, this was the duration spent moving behind the target (see Fig. 3E); for Monkey B, it was the duration in contact with the object’s rear plate (see Fig. 4G). These behaviors were prominent in the early post-surgical phase and diminished over time. Filled squares indicate a significant difference from pre-TT baseline (p<0.05, two-sample t-test). All data are plotted over days relative to the tendon transfer (TT) surgery (day 0).

A Two-Phase Adaptation of Muscle Activity is Observed in Both Monkeys Following Tendon Transfer.

The figure compares EMG activity profiles and cross-correlation analyses for Monkey A (left) and Monkey B (right), demonstrating a consistent pattern of motor adaptation consisting of an initial functional swap followed by a later reversion. A representative non-transferred muscle is included for each monkey. Monkey A (A-J): Profiles are aligned on object release. Monkey B (K-Q): Profiles are aligned on food touch. Filled triangles (▾) indicate peak activity occurring during finger extension, while open triangles (▽) indicate peak activity occurring during finger flexion. Small triangles on correlation plots denote landmark days.

Muscle Synergy Compositions Remain Stable While Their Activation Timings Show a Two-Phase Adaptation.

The figure presents the spatial muscle weights and temporal activation coefficients for the primary finger flexor (Synergy A) and extensor (Synergy B) for Monkey A (A-D) and Monkey B (E-H). (A, B, E, F) Spatial Synergy Weights: The muscle weight contributions for each synergy are shown for the pre-surgery control period and for five post-surgery landmark days, demonstrating that synergy structure was preserved. (C, D, G, H) Temporal Activation Coefficients: The activation profiles show the same two-phase adaptation seen in individual muscles: an initial swap followed by a later reversion. Symbols and alignment are as described in Fig. 6.

Analysis of Secondary Muscle Synergies and Variance Accounted For (VAF).

This figure provides supporting data for the synergy analysis, including the VAF plots justifying the use of four synergies, and the detailed analysis of the secondary Synergies C and D for both Monkey A and Monkey B. (A-B) Variance Accounted For (VAF). The plots show the cumulative variance in the EMG data explained by an increasing number of synergies for Monkey A (left) and Monkey B (right). In both original datasets (blue lines), four synergies were sufficient to account for more than 80% of the variance (demarcated by the black horizontal line), justifying the dimensionality of the synergy model. VAF for corresponding shuffled data is shown for comparison (red lines). (C-F) Analysis of Synergy C (Wrist Flexor Synergy). This panel group shows the spatial weights (C, D) and temporal activation coefficients (E, F) for Synergy C in Monkey A and Monkey B, respectively. Spatial Weights (C, D): Pre-surgery control profiles (left sub-panels) are compared to post-surgery landmark days (right sub-panels), demonstrating that the muscle contributions to this synergy remained largely stable. Temporal Activation (E, F): In Monkey A, the temporal profile (C) shows a notable increase in activation during the late adaptation phase, consistent with its recruitment for a compensatory strategy. The adaptive pattern for Monkey B (E) was less distinct. (G-J) Analysis of Synergy D. This panel group shows the spatial weights (G, H) and temporal activation coefficients (I, J) for Synergy D in Monkey A and Monkey B. This synergy, which contributes to wrist extension, exhibited relatively minor and inconsistent changes following the tendon transfer in both animals. For all temporal plots, profiles are aligned on object release (Monkey A) or food touch (Monkey B) at 0% task range. Post-surgery plots show data from selected landmark days as indicated by the color legend.

Cross-correlation analysis reveals the two-phase adaptation of primary synergy activation.

Cross-correlation coefficients for the primary flexor (Synergy A) and extensor (Synergy B) synergies are plotted over post-surgery days for Monkey A (A-D) and Monkey B (E-H). For each synergy, the activation pattern was cross-correlated with its own pre-surgery profile (A, B, E, F) and with that of its antagonist (C, D, G, H). The results quantitatively demonstrate the swap-and-revert pattern in both animals. The // represents the recovery period.

Cross-correlation analysis of secondary synergy activation.

Cross-correlation coefficients for the secondary synergies (C and D) are plotted over post-surgery days for Monkey A (A-D) and Monkey B (E-H). For each synergy, the activation pattern was cross-correlated with the pre-surgery profiles of Synergy A (red lines) and Synergy B (blue lines) to reveal their changing relationships to the primary flexor and extensor commands.

Aggregated and averaged EMG (aaEMG) reveals synergy-specific adaptive patterns.

Aggregated and averaged electromyography (EMG) activities for the main contributing muscles of each of the four synergies for Monkey A (A-H) and Monkey B (I-P). For each recording session, EMG activity within a ±15% task range window was summed for the contributing muscles and then averaged. The left columns for each monkey (A-D, I-L) show the aaEMG over all post-surgery days. The right columns (E-H, M-P) show the mean (± SEM) aaEMG for the pre-surgery period (“pre”) and the five selected landmark days. Monkey A (A-H) The contributing muscles for each synergy were: Synergy A: flexor digitorum superficialis (FDS) and flexor carpi ulnaris (FCU). Synergy B: extensor digitorum communis (EDC), extensor digitorum-2,3 (ED23), and extensor carpi ulnaris (ECU). Synergy C: palmaris longus (PL) and flexor carpi radialis (FCR). Synergy D: flexor digitorum profundus (FDP), brachioradialis (BRD), and extensor carpi radialis (ECR). Monkey B (I-P) The contributing muscles for each synergy were: Synergy A: flexor digitorum profundus (FDP) and palmaris longus (PL). Synergy B: extensor digitorum communis (EDC), extensor digitorum-2,3 (ED23) and extensor digitorum-4,5 (ED45). Synergy C: extensor carpi radialis (ECR), brachioradialis (BRD), and deltoid (DEL). Synergy D: extensor carpi ulnaris (ECU). Vertical colored bars on the time-series plots indicate the landmark days shown in the bar plots. The // on the time axis represents the recovery period during which no recordings were taken. Asterisks on bar plots indicate a significant difference from the pre-surgery control period (p < 0.01, *p < 0.001, **p < 0.0001; two-sample t-test with Bonferroni correction, α = 0.01).

Kinematic analysis reveals a compensatory tenodesis strategy in Monkey B.

Changes in joint angles at the wrist and metacarpophalangeal (MCP) joint for Monkey B (mean of 20 trials ±SD for each landmark day, taken 83ms before food touch). (A) The MCP joint angle increased post-surgery, indicating greater finger extension. (B) Concurrently, the wrist joint angle decreased, indicating wrist flexion. This coordinated movement pattern is characteristic of an active tenodesis effect, suggesting it was used as a compensatory strategy to achieve finger extension. Statistical analysis confirmed these changes were significant (p < 0.0001, α = 0.01, ANOVA).

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 coefficients of muscle synergies), which reflects this two-phase process.