Bimanual motor coordination controlled by cooperative interactions in intrinsic and extrinsic coordinates

Abstract

Although strong motor coordination in intrinsic muscle coordinates has frequently been reported for bimanual movements, coordination in extrinsic visual coordinates is also crucial in various bimanual tasks. To explore the bimanual coordination mechanisms in terms of the frame of reference, here we characterized implicit bilateral interactions in visuomotor tasks. Visual perturbations (finger-cursor gain change) were applied while participants performed a rhythmic tracking task with both index fingers under an in-phase or anti-phase relationship in extrinsic coordinates. When they corrected the right finger's amplitude, the left finger's amplitude unintentionally also changed [motor interference (MI)], despite the instruction to keep its amplitude constant. Notably, we observed two specificities: one was large MI and low relative-phase variability (PV) under the intrinsic in-phase condition, and the other was large MI and high PV under the extrinsic in-phase condition. Additionally, using a multiple-interaction model, we successfully decomposed MI into intrinsic components caused by motor correction and extrinsic components caused by visual-cursor mismatch of the right finger's movements. This analysis revealed that the central nervous system facilitates MI by combining intrinsic and extrinsic components in the condition with in-phases in both intrinsic and extrinsic coordinates, and that under-additivity of the effects is explained by the brain's preference for the intrinsic interaction over extrinsic interaction. In contrast, the PV was significantly correlated with the intrinsic component, suggesting that the intrinsic interaction dominantly contributed to bimanual movement stabilization. The inconsistent features of MI and PV suggest that the central nervous system regulates multiple levels of bilateral interactions for various bimanual tasks.

Keywords: bilateral interaction; cyclic movement; frame of reference; human intermanual coordination; relative phase stability.

Figure 1

Experimental setup. (A) The monitor showed real‐time visual feedback of the bilateral finger movements. The participant was instructed to match the finger cursor with guide‐cursor movement and to keep the left finger amplitude constant throughout a trial. In the post‐phase of each trial, the cursor of the left finger was eliminated. (B) Four conditions of bilateral finger movements defined by the relative phases in intrinsic muscle and extrinsic visual coordinates. Orientation of the axis of cursor movement was set along the proximal–distal direction in C₁ and C₄ and along the left–right direction in C₂ and C₃. In C₂ and C₃, finger cursors of the right and left fingertips were displayed at the upper and lower sides of the fixation cross, respectively. In the illustrations depicting the task conditions, ‘s’ indicates the start position of the cursors for the right and left fingers. The origin of the visual task field on the monitor is at the start position of the right finger's cursor.

Figure 2

Typical movement profiles of a particular participant in C₁ of experiment 1. Mean movement profiles of right (solid lines) and left (dotted lines) fingertips in (A) VG_C, (B) VG− and (C) VG+ trials. The amplitude of each cycle was defined by the difference between adjacent positional peaks as indicated in A. Left‐finger movement unintentionally changed against the task instruction. (D) Amplitude transitions of the right (solid line) and left (dotted line) fingertips in VG_C trials. Although the participant did not change the amplitude of the right finger voluntarily, the amplitude of the left finger increased gradually in the post‐phase. Asterisks indicate significant amplitude increases compared with the mean amplitude in the pre‐phase (**P < 0.01, ***P < 0.001). (E) Amplitude changes for VG− and VG+ trials and indexes of amplitude changes of the finger movements. ${\text{MC}}_R^{5\text{th}}$, amount of voluntary ‘motor correction’ of the right finger's amplitude at the fifth cycle; ${\text{MI}}_L^{5\text{th}}$, amount of unintentional ‘MI’ to the left finger's amplitude at the fifth cycle. These values are represented by the sum of absolute changes in VG− and VG+ trials by reference to the mean amplitude during the pre‐phase. Error bars represent the SD across trials for this participant.

Figure 3

Bimanual motor coordination characterized by the (A) MI and (B) coordination stability in experiment 1. (A) Although voluntary motor corrections of the right finger (${\text{MC}}_R^{5\text{th}}$) were not different among the four conditions (data not shown), the unintentional MI to the left finger $({\text{MI}}_L^{5\text{th}})$ in C₄ was significantly smaller than those in the other conditions. (B) Phase variability $({\text{PV}}_{\mathit{\varphi }}^{5\text{th}})$ for each condition was calculated by averaging its values in VG− and VG+ trials. A lower ${\text{PV}}_{\mathit{\varphi }}^{5\text{th}}$ value means stable bimanual movement. Error bars indicate the SE across the participants. **P < 0.01, ***P < 0.001.

Figure 4

Amplitude changes of fingers and coefficient values estimated by the multiple‐interaction model. (A–C) Magnitude of ${\text{MC}}_R^{5\text{th}}$, ${\text{sVE}}_R^{5\text{th}}$ and ${\text{MI}}_L^{5\text{th}}$ for each VG _i in each condition (C₁–C₄). In both ${\text{MC}}_R^{5\text{th}}$ and ${\text{sVE}}_R^{5\text{th}}$, there is no significant difference among the same VG _i. (D and E) α and β in each condition (C₁–C₄). α became large in intrinsic in‐phase conditions (C₁ and C₂), and β became large in extrinsic in‐phase conditions (C₁ and C₃). (F) Relationship between intrinsic interaction component ($\mathit{\alpha }·{\text{MC}}_{\mathrm{R}}^{5\text{th}}$) and extrinsic interaction component ($\mathit{\beta }·{\text{sVE}}_{\mathrm{R}}^{5\text{th}}$) for each VG _i (labelled by numbers 1–3) and condition (C₁, open circles; C₂, asterisks; C₃, open triangles; C₄, open squares). The dotted diagonal line indicates equal magnitudes of the interaction components. In A–E, error bars denote SE across the participants. ***P < 0.001.

Figure 5

Relationships between the strength of interaction and coordination stability for all of the VG _i combinations in experiment 2. (A) Each point indicates the mean value across participants, and the VG _i combination is labelled by suffixes 1–3. ${\text{MI}}_L^{5\text{th}}$ significantly correlated with ${\text{PV}}_{\mathit{\varphi }}^{5\text{th}}$. (B and C) ${\text{PV}}_{\mathit{\varphi }}^{5\text{th}}$ has a strong correlation with the decomposed intrinsic interaction component $(\mathit{\alpha }·{\text{MC}}_{\mathrm{R}}^{5\text{th}})$ but not with the extrinsic interaction component ($\mathit{\beta }·{\text{sVE}}_{\mathrm{R}}^{5\text{th}}$). *P < 0.05, ***P < 0.001.