3.3 Associations between the lesion location and kinematic gait parameters
A lesion in the proximal corona radiata was significantly associated with increased hip extension in the stance phase (corrected P < .05; Table 2, Fig. 2D). A lesion in the posterior limb of the internal capsule was significantly associated with increased knee extension in the stance phase (corrected P < .05; Table 2, Fig. 2E). A lesion in the paracentral lobule, including the cortical area, was significantly associated with decreased ankle dorsiflexion in the stance phase and knee flexion in the swing phase (corrected P < .05; Table 2, Fig. 2F, G). No lesion was significantly associated with the affected hip maximal flexion angle in the swing phase or affected ankle maximal dorsiflexion angle in the swing phase (corrected P < .05).
3.4 Associations between the lesion location and kinetic gait parameters
A lesion in the frontal lobe was associated with increased hip and ankle moment (corrected P < .05; Table 2, Fig. 2H, J). Lesions in the thalamus and lentiform nucleus were associated with increased knee moment (corrected P < .05; Table 2, Fig. 2I).
3.5 Results of post-hoc analysis between the lesioned and nonlesioned groups in walking speed-related brain regions
Results of post-hoc analysis did not reveal any significance between lesioned and nonlesioned groups in walking speed-related brain regions (P >.05). The stride length and step length tended to be longer in the lesioned group than the nonlesioned group. Most of the kinematic and gait parameters tended to be worse in the lesioned group than in the nonlesioned group, except affected knee maximal flexion in the swing phase and affected knee maximal knee extensor moment (Table 3).
3.6 Reliability results for region of interest
According to the intraclass correlation analysis, the lesion ROIs that were used for group-level inference were highly reliable (ICC>0.95, P <.001).
Knowledge of the association between stroke lesion and walking outcome is important to target rehabilitation goals after stroke. Unlike previous studies using the clinical categorization of gait with the clinical evaluation of lower extremity function,[1,9,14] we used 3DMA to assess walking characteristics in detail. The corona radiata was a common region for spatiotemporal and kinematic parameters. Furthermore, brain regions of motor regulation were associated with kinetic parameters.
Most functional recovery occurs within 6 months poststroke onset and the gait pattern after stroke changes completely during recovery.[10,15] The average period after onset in our patients was 62.2 months (Table 1), so their functional recovery and adaptive processes reached a plateau at the point of inclusion in this study. The results of this study should be carefully interpreted because we analyzed the association between the injured brain lesion for chronic stroke and final walking characteristics. Furthermore, all patients could walk at least 10 m independently; therefore, the results do not refer to the ability to walk alone, but rather take into consideration the compensatory walking pattern after stroke. The lesion associated with worse gait parameters was regarded as a critical area in which other intact brain regions could not compensate for the functional loss. Furthermore, we also analyzed the lesions associated with increased walking speed to identify the gait patterns able to compensate for the patients’ disability.
The interesting finding of this study is the association between increased walking speed and the lesions in the corona radiata and posterior limb of the internal capsule through which pass the lower leg fibers.[16,17] The post-hoc analyses demonstrated that the lesioned group had better cadence, stride length, and maximal knee flexion in the swing phase even if most of the kinetic parameters were worse than in the nonlesioned group (Table 3). The possible explanation for this may be that the recovery process of lower leg fibers archived their self-selected walking speed fast. The recovery mechanisms following corticospinal tract injury are still unclear but thought to involve subcortical reorganization. Although the subcortical lesion areas have less recovery potential than cortical lesion areas, subcortical lesions may occur after stroke.[9,18] The bilateral hemispheric connection in the lower legs may also influence the recovery mechanisms. Most previous studies have reported that corticospinal pathway injury correlates with poorer upper extremity motor function in post-stroke patients,[7,19] but not with gait function.[6,8,14] The bilateral connection in the lower legs may reinnervate in 2 ways, either by connecting with ipsilesional fibers or by connecting with contralesional fibers, and this process may result in compensatory gait pattern after injury of the corona radiata and posterior limb of the internal capsule. The better knee flexion in the swing phase was one of the compensatory motions in the lesioned group, which connects with longer stride length and increased cadence (Table 3). The flexion angle in the affected side is mainly influenced by muscle weakness with extension synergies after stroke.[9,20] The lesioned group may compensate the injury of lower leg fibers with various recovery processes and less extension synergy linked with better walking speed. However, these contradictory results could not be fully explained by the results of this study, and therefore additional studies specifically addressing this point are warranted.
The lesion in the hippocampus was associated with decreased cadence. Our results are consistent with those of previous studies showing that the hippocampus is a key human brain region involved in memorization and locomotion.[21,22] Functional MRI studies have implicated the hippocampus in walking,[23,24] and the hippocampus is known to store the motor patterns that are recalled during walking. One study demonstrated that the value of cadence was maintained during aging even if the other gait parameters had a decreasing trend. This phenomenon could be explained by the fact that the cadence is affected by the individuals’ experience and learning. The hippocampus is involved in learning and may have crucial roles in terms of cadence that could not be replaced by any other intact brain regions. However, a lesion of the frontal lobe was associated with increased cadence. The frontal lobe plays important roles in the execution of gait initiation and motor programs of voluntary movements.[26,27] The main regions reported supplementary motor area and premotor area in frontal lobe,[3,27] but the exact role of a specific small lesion in frontal lobe to gait recovery is still unknown. Further study is needed for the interpretation with our results.
Stride length and hip extension were mainly associated with the proximal corona radiata, which passes lower leg fibers.[16,17] Our results are in line with those of previous studies reporting a positive correlation between maximal hip extension and stride length.[20,28] Stride length, especially, depends on muscle strength and the weight-supporting capacity of the affected limb. Since the single support time of the affected side is significantly shorter than the unaffected side after stroke, a shorter single support time reduces the maximal hip extension in the stance phase. Furthermore, reduction of the maximum hip extension in the stance phase decreases the stride length.[9,20] Numerous complex structures, including the corticospinal tract, may be involved in asymmetric walking after stroke. Alexander et al reported that damage to the external capsule, putamen, and insula was related to gait asymmetry, whereas lesions in the corona radiata and basal ganglia were also demonstrated to be associated with lower extremity motor impairments. Our results indicated that the increase of maximum hip extension with stride length consistently correlated with the proximal corona radiata. As we previously discussed, with increased walking speed, the proximal corona radiata may have similar recovery mechanisms, and this area may have residual potential for recovery probably because it is near the cortex.
The paracentral lobule, including the cortical area, was mainly associated with decreased ankle dorsiflexion in the stance phase and reduced knee flexion in the swing phase. The 2 main factors affecting gait performance are diminished muscle strength and abnormal muscle tone. Decreased knee flexion in the swing phase and decreased ankle dorsiflexion in the stance phase are typical subtypes of poststroke gait patterns.[20,29] These phenomena are usually caused by increased muscle tone, especially of the ankle plantarflexor muscle in the stance phase and knee extensor muscle in the swing phase. The onset of spasticity after stroke is highly variable, but tends to occur shortly after or approximately 1 year after stroke. The mechanism of spasticity is still unclear, but elimination of the inhibitory signal of upper motor neurons causes over-activation of spinal motor neurons in the chronic stage of upper motor lesions. The result of this study is consistent with that of past studies reporting that an association of spasticity with the gray matter includes the corticospinal tract pathway.
Moments of the hip, knee, and ankle joints were associated with multiple brain areas. Interestingly, certain areas are consistently related to motor regulation, and these include the frontal lobe and basal ganglia. Hip and ankle moments were significantly related to the frontal area, whereas knee moment was associated with the thalamus and lentiform nucleus. The slow walking speed group of poststroke patients had increased extensor moment, thus the deficit of motor planning and regulation may have affected gait velocity in our results. As kinetic variables are the cause of the kinematic and temporal-spatial parameters of gait, further studies are needed to confirm these results.
There were limitations of this study that should be considered when interpreting the results. First, our study had a relatively small sample size, with heterogeneity in initial stroke severity, onset duration, intensity of rehabilitation training, and etiology. We also flipped all images to visualize the lesion within left hemisphere; thus, the contribution of laterality to gait function is still unclear. Future studies are required to investigate these aspects. Second, our study included only male patients because of our institutional characteristics. Because the gait characteristics between men and women are different in many clinical study populations, the generalizability of our results to all populations remains uncertain. Third, we used the MNI template for the process of VLSM analysis, but it was developed based on subjects in Western countries. Because of the morphological difference between east Asian and western populations,[33,34] future study will be needed to use Asian specific brain template. Fourth, our study had a retrospective cross-sectional design. To understand the role of rehabilitation training on the prognosis of locomotion in further detail, a prospective, longitudinal study is required. However, this is the first study on brain mapping of walking function using the quantitative parameters of 3DMA.
Mainly the cortical and corticospinal tract lesions for lower extremities are associated with spatiotemporal and kinematic variables of gait after stroke. The roles of these areas for gait could be replaced after recovery; however, the hippocampus may not be replaced by any other recovery mechanisms. Furthermore, motor regulation-related areas may affect joint moments during gait after stroke.
Data curation: Dae Hyun Kim, Suk Jung.
Formal analysis: Dae Hyun Kim, Sunghyon Kyeong.
Methodology: Kyung Hee Do.
Supervision: Seong Kyu Lim, Hye Won Kim.
Visualization: Dae Hyun Kim.
Writing – original draft: Dae Hyun Kim.
Writing – review & editing: Hyong Keun Cho, Hye Won Kim.
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Keywords:Copyright © 2018 The Authors. Published by Wolters Kluwer Health, Inc. All rights reserved.
brain mapping; gait; rehabilitation; stroke rehabilitation; stroke