Evidence of the existence of multiple modules for the stroke-caused flexion synergy from Fugl-Meyer assessment scores

Abstract

Stroke-caused synergies may result from the preferential use of the reticulospinal tract (RST) due to damage to the corticospinal tract. The RST branches multiple motoneuron pools across the arm together resulting in gross motor control or abnormal synergies, and accordingly, the controllability of individual muscles decreases. However, it is not clear whether muscles involuntarily activated by abnormal synergy vary depending on the muscles voluntarily activated when motor commands descend through the RST. Studies showed that abnormal synergies may originate from the merging and reweighting of synergies in individuals without neurological deficits. This leads to a hypothesis that those abnormal synergies are still selectively excited depending on the context. In this study, we test this hypothesis, leveraging the Fugl-Meyer assessment that could characterize the neuroanatomical architecture in individuals with a wide range of impairments. We examine the ability to perform an out-of-synergy movement with the flexion synergy caused by either shoulder or elbow loading. The results reveal that about 14% [8/57, 95% confidence interval (5.0%, 23.1%)] of the participants with severe impairment (total Fugl-Meyer score <29) in the chronic phase (6 months after stroke) are able to keep the elbow extended during shoulder loading and keep the shoulder at neutral during elbow loading. Those participants underwent a different course of neural reorganization, which enhanced abnormal synergies in comparison with individuals with mild impairment (P < 0.05). These results provide evidence that separate routes and synergy modules to motoneuron pools across the arm might exist even if the motor command is mediated possibly via the RST.NEW & NOTEWORTHY We demonstrate that abnormal synergies are still selectively excited depending on the context.

Keywords: abnormal synergies; reticulospinal tract; stroke; synergy module.

Graphical abstract

Figure 1.

Simplified conceptual models of the neuroanatomical architecture of the upper extremity with no neurological damage (A) and hypothetical working mechanisms of stroke-caused synergy (B and C). Joints x, y, and z are assumed to be the primary joints in the upper extremity. Filled rectangular boxes represent a stroke-caused synergy module from which a motor command is sent to the muscles of joints. The size of the boxes indicates the strength of synergy. A: with no neurological damage, we assume that the cortex decends motor commands to each of joints x, y, and z through separate pathways, accordingly allowing for joint individuation. B: one synergy module exists that governs synergetic movement across all joints of the upper extremity. The synergy module is turned on once the cortex descends motor command to move any of joints x, y, and z, and then the module descends motor command all muscles of joints x, y, and z . This model hypothesizes that all muscles involved in the synergy are involuntarily activated regardless of which joint the cortex intends to move. C: multiple synergy modules exist that lead to the same sort of synergy but different degrees of strength of synergy. This model hypothesizes that the strength of synergy depends on the joint that the cortex intends to move. We assume that if the direct drive (dashed line) from the cortex to the target joint overwhelms the drive (solid line) from synergy modules to the joint, “out-of-synergy” motions can be performed.

Figure 2.

Time evolutions of the grand total score, total score of in-synergy test items and total score of out-of-synergy test items of the Mild group and Severe group. Error bars are SE. *P < 0.05, statistically significant difference in mean between 2 assessments.

Figure 3.

Distributions of the increment in the total score of the out-of-synergy test items normalized to its possible maximum score with the increment in the total score of the in-synergy test items normalized to its possible maximum score between time points of assessment. The blue solid lines are the regression lines and dotted lines are lines with a slope of 1.

Figure 4.

Proportions of the participants who scored 0, 1, or 2 over all participants with very severe, severe, moderate, and mild impairment for each FMA test item that assessed an out-of-synergy movement under either shoulder loading or elbow loading.

Figure 5.

Time evolution of Symmetry of participants from the Mild group (n = 12) and Severe group (n = 8), respectively, who scored 1 on both test items of forearm supination/pronation under shoulder loading or elbow loading. The results at 7 days do not reflect Symmetry of 6 participants from the Mild group and 5 participants from Severe group, because they do not score in any of in-synergy or out-of-synergy test items. Error bars are SE. *P < 0.05, significant difference in mean between 2 groups at an assessment.