How many years longer will you allow your incompetent stroke hospital to exist? All this requires is finding videos of all the movements you currently can't do well and provide them to patients. Fuckingly simple, yet your hospital has completely failed at that task.
action observation (110 posts to January 2013)
Observation of others’ actions during limb immobilization prevents the subsequent decay of motor performance
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Contributed by Giacomo Rizzolatti, September 29, 2021 (sent for review December 23, 2020; reviewed by Ferdinand Binkofski, Günther Knoblich, and Steven Small)
Significance
In several clinical conditions, especially those related to orthopedic trauma or specific injuries of the peripheral nervous system, patients may experience a period of limb nonuse that has detrimental cascade effects on corticomotor organization and ultimately, on motor performance. During limb nonuse, treatments based on action observation may be suitable for stimulating the motor system via the mirror mechanism. Using short-term immobilization in healthy volunteers, our study showed that administering action observation during immobilization limits the movement alterations induced by limb nonuse. Given action observation’s protective role against the decline of motor performance, it represents a valid tool for early interventions during limb nonuse, thus reducing the burden of further motor rehabilitation.
Abstract
There is rich clinical evidence that observing normally executed actions promotes the recovery of the corresponding action execution in patients with motor deficits. In this study, we assessed the ability of action observation to prevent the decay of healthy individuals’ motor abilities following upper-limb immobilization. To this end, upper-limb kinematics was recorded in healthy participants while they performed three reach-to-grasp movements before immobilization and the same movements after 16 h of immobilization. The participants were subdivided into two groups; the experimental group observed, during the immobilization, the same reach-to-grasp movements they had performed before immobilization, whereas the control group observed natural scenarios. After bandage removal, motor impairment in performing reach-to-grasp movements was milder in the experimental group. These findings support the hypothesis that action observation, via the mirror mechanism, plays a protective role against the decline of motor performance induced by limb nonuse. From this perspective, action observation therapy is a promising tool for anticipating rehabilitation onset in clinical conditions involving limb nonuse, thus reducing the burden of further rehabilitation.
There is rich clinical evidence that observing normally executed actions promotes the recovery of the corresponding action execution in patients with motor deficits. This procedure, which is based on the activation of the motor system via the mirror mechanism (1, 2), is called action observation treatment (AOT) (3, 4). The effectiveness of AOT in motor recovery has been demonstrated in several clinical conditions, including stroke (5⇓–7), Parkinson's disease (8⇓–10), multiple sclerosis (11), and cerebral palsy (12⇓⇓⇓–16), as well as in patients with orthopedic trauma and postsurgical patients (17⇓–19).
In recent decades, researchers have advanced covert motor approaches based on action observation other than AOT. Such approaches include mirror therapy (20, 21), which improves the symptoms resulting from absent or altered feedback from the affected side of the body [e.g., phantom pain in arm amputees (22, 23)] and may also enhance motor function in poststroke patients (24⇓–26). More recently, noninvasive brain stimulation techniques, such as transcranial magnetic stimulation, transcranial direct current stimulation, and peripheral electrical stimulation, have been used to enhance motor recovery in neurological (27⇓–29) and orthopedic patients (30). When tested in combination with interventions based on action observation, these approaches exhibited the ability to enhance the magnitude of treatment effects (31, 32).
In some of the abovementioned clinical conditions, especially those involving orthopedic trauma or affecting the peripheral nervous system, the patient may experience a period of limb nonuse. It has been demonstrated that limb nonuse (or disuse) induces a reduction in the size and excitability of the cortical representation of the immobilized limb, gradually leading to maladaptive plasticity changes and the appearance of motor alterations (33⇓–35), which can interfere with the rehabilitative outcome. In this context, action observation is an effective treatment alternative when physical therapy is not applicable. The aim of the present study is to determine whether administering AOT during the immobilization period can limit the progressive impoverishment of motor performance—an effect researchers have yet to be establish.
To this end, a short-term immobilization (STI) was administered to healthy volunteers. This procedure is commonly used to model the neurophysiological changes leading to motor impairments in injured people (reviews are in refs. 36 and 37) because it minimizes the impact of confounding variables (e.g., immobilization duration, cause of immobilization, associated pain, potential comorbidities) and consequently, isolates the hypoactivity-induced effects on neurophysiological processes. Moreover, the use of healthy volunteers enables a within-subjects comparison between pre- and postimmobilization performance, whereas the use of clinical populations makes the same procedure virtually impossible due to the sudden nature of the injury.
The participants were subdivided into two groups: those receiving AOT and those receiving control stimulations. In both groups, the upper-limb kinematics of goal-directed movements was tested before and after the immobilization. We evaluated whether the motor performance of subjects who underwent AOT was better preserved after the immobilization compared with that of the control (CTRL) group, and we determined which aspects of movement organization were mostly affected by AOT.
The present study’s results could lead to the use of AOT during immobilization in a spectrum of clinical conditions in which the patient's movement is transiently impeded, thus favoring an early treatment onset and potentially limiting the extent of motor deficits to be later rehabilitated.
Results
In order to assess AOT’s protective role against the motor impairments that typically occur after immobilization, we recorded the upper-limb kinematics of a group of healthy volunteers before and after arm immobilization (16 h). The participants were asked to perform three reach-to-grasp movements, which were distinguished by the location of the target object, as follows: 1) located anteriorly at the height of the subject’s shoulders (A-Low), 2) located anteriorly at the height of the subject’s head (A-High), and 3) located laterally at the height of the subject’s shoulders (L-Low) (Fig. 1A). During immobilization, half of the participants (the AOT group) repeatedly observed and imagined the same movements previously executed, whereas the other half (the CTRL group) observed natural scenarios for an equivalent amount of time.
No significant differences between AOT and CTRL groups at baseline were found for reaching duration (RD), reaching velocity peak (VP), or movement fractionation (MFr; all P > 0.18) (SI Appendix, Table S1). Table 1 reports the results for RD, VP, and MFr for the three tested movements. According to the ANOVA, all the variables showed a significant main effect of TIME. The worst impairments were observed immediately after bandage removal, namely at the first postimmobilization trial (T1), and all the subjects underwent a noticeable recovery over the course of the postimmobilization trials (from T1 to T10). This finding indicates that 16 h of immobilization was sufficient to induce a subtle but quantifiable alteration of kinematic performance, the recovery of which could be evaluated during the postimmobilization procedures.
The most interesting finding indeed concerns the effect of the GROUP factor, which appeared to be limited to MFr, a parameter indexing the relative ratio between the range of motion (ROM) for the elbow- and shoulder-joint angles of interest. Comparing pre- and postimmobilization scores, MFr scores were higher for CTRL participants relative to the AOT group for all the three movements [F(1, 38) = 7.55, P = 0.009, partial η2 = 0.16, Bayes Factor (BF)10 = 5.15]. A significant main effect of MOVEMENT also emerged, likely reflecting a stronger effect of the immobilization procedure on the coordination of shoulder and elbow joints in the L-low movement. However, no interaction effects were found, evidencing a similar effect of AOT on the three movement patterns. More detailed statistical analysis results for RD, VP, and MFr are reported in SI Appendix, Table S2.
As the MFr depends on the shoulder- and elbow-joint angles, we assessed the effects of immobilization (TIME factor) and AOT (GROUP factor) on each joint separately. The comparison between each postimmobilization trial and the average preimmobilization kinematics was performed using the linear fit method [LFM (38)], which returns three indexes (amplitude modulation [AM], R2, amplitude offset between the curves [AOff]) describing different features of the movement pattern. Considering that MFr scores vary according to elbow and shoulder ROM, we focused on the AM parameter, which indicates whether postimmobilization movements are more/less scaled in amplitude (AM > 1 and AM < 1, respectively) relative to baseline (T0). On the contrary, we did not expect variation in the R2 and AOff indexes, which test differences in the time course and offset of the joint angle curves, respectively.
Fig. 2 depicts the average time course of the elbow flexion–extension angle in the preimmobilization phase and the first trial of the postimmobilization phase for the AOT and CTRL groups. The results showed that immobilization reduces the elbow ROM, in particular for the CTRL group. In support of this point, the ANOVA for AM (Fig. 2, Right) showed a significant main effect of GROUP [F(1, 38) = 10.98, P = 0.002, partial η2 = 0.22, BF10 =15.94], with CTRL participants systematically showing lower AM scores: that is, a higher level of joint stiffness for all movements relative to the AOT group.
A main effect of TIME was found [F(2, 76) = 10.06, P < 0.01, partial η2 = 0.21, BF10 > 100]. Post hoc comparisons revealed that T1 had systematically lower values than T4 and T9 (all P < 0.05) (SI Appendix, Table S2), underlining that the initial shrinkage of elbow movement was reversed over the course of the postimmobilization training. The absence of a significant GROUP × TIME interaction suggested that the recovery dynamics, present for all movements as indicated by the significant TIME effect, were not impacted by AOT. Rather, AOT seemed to preserve participants’ original motor abilities, reflected in a lower degree of impairment at T1 compared with CTRL, which persisted for the entire postimmobilization period.
No significant effect of the factor GROUP was observed for the shoulder movements, but a significant effect of TIME emerged [F(2, 76) = 9.05, P < 0.001, partial η2 = 0.19, BF10 > 100]. However, it should be noted that AM values for the shoulder were generally higher than those for the elbow, suggesting that shoulder-joint angles were weakly impacted by the immobilization (SI Appendix, Fig. S1 and Table S2). This difference may have been due to the different degrees of constraint the bandage exerted on the two joints. Whereas the elbow was constrained in a fixed position, with no residual opportunity for flexion or extension, the shoulder maintained some residual mobility, which could have obscured the overall impact of immobilization on shoulder kinematics. The factorial analysis for R2 and AOff indicated that immobilization did not affect the temporal pattern of either shoulder or elbow kinematics or the absence of offset between the curves (SI Appendix, Table S3). The lack of significant effects on R2 and AOff excluded any biases in determining differences in AM values.
Given that the distance between the participant and the object remained constant throughout the experimental procedure, it is reasonable to ask whether the reduced elbow flexion–extension could be ascribed to a different dynamic postural adjustment of the trunk before and after immobilization. However, we ruled out this possibility by computing the displacement of the trunk during the movement and verifying the absence of any significant effect of GROUP (SI Appendix, Table S3).
Discussion
In the present study, STI induced an alteration of motor performance, with participants showing longer movement duration, higher MFr, and reduced ranges of motion after immobilization. These findings are in line with previous evidence that STI impairs the motor performance of the restricted body part, even after periods of immobilization ranging from 10 to 12 h (33, 39, 40). The alterations observed in both groups appeared to be largely reversible, with an almost complete recovery of motor performance within the 10 trials administered after the immobilization (ref. 40 has similar results).
STI in healthy participants provides a neurobehavioral model for exploring the efficacy of covert motor interventions (e.g., action observation or motor imagery), which can adaptively stimulate corticomotor representations within a context of maladaptive neural plasticity, without the influence of disease-related confounding factors (36, 41⇓–43). One could argue that the young age of our study’s participants (mean age 22.5 y) limits the generalizability of our findings to older populations. However, previous studies have shown that the activity of frontoparietal networks shared by action observation, motor imagery, and action execution (44) does not exhibit any age-dependent changes when comparing old and young populations (45), thus supporting the generalizability of our findings across age groups.
Most interestingly, our data show that participants receiving AOT during the immobilization period had better-preserved motor performance at the end of the immobilization period (Fig. 3). Notably, this effect pertains to the spatial organization of the movement, reflected in more increased MFr scores for the CTRL group. Conversely, the temporal features of the movement were weakly affected by the AOT intervention. This discrepancy may be due to the neural substrates of action observation, which rely heavily on frontoparietal networks encoding movement organization (1) and only to a minor extent, on the neural substrates responsible for the temporal organization of the movement (46⇓–48).
Which neural mechanism enables AOT to prevent the decay of motor performance in healthy volunteers undergoing STI? STI is known to induce a corticomotor depression of the neural representation of the immobilized limb (41, 49, 50). Over the long term, this lowered excitability could facilitate the emergence of maladaptive behaviors or the consolidation of compensatory attitudes that, although initially beneficial for the patient, are often detrimental to the long-term outcome (51). For these reasons, the development of early-onset interventions that counteract the corticomotor depression might play a fundamental role in limiting the progressive impoverishment of motor performance.
In this regard, AOT has proven effective in limiting the STI-induced reorganization of cortical maps. Bassolino et al. (41) demonstrated that after a 10-h immobilization of the upper limb, healthy volunteers who received action observation stimuli had an almost completely preserved corticomotor map, whereas CTRL participants not receiving AOT suffered from a large reduction of the corticospinal excitability. These findings indicate that AOT has the capacity to counteract the corticomotor depression following limb nonuse, and they likely explain the neural mechanism underlying the preserved motor performance of the AOT group in our study. Given our experimental design, whether the reduced effects of immobilization were mainly driven by observing specific movements or rather, by observing any movement remains an open point. However, the notion that action observation elicits a motor activity following a somatotopic and actotopic organization (52) points at congruent actions as the ideal stimuli for an AOT. This is also in line with previous behavioral data, showing that during a physical practice task, action observation induces a strengthening of the motor memory encoding but only if the observed action is congruent with the practiced one (53).
Although our study involved healthy subjects, its results are informative for different clinical scenarios. Orthopedic and peripheral nervous system diseases (e.g., brachial plexopathy, nerve or radicular injuries, inflammatory disorders like Guillain–Barré syndrome) represent the clinical conditions closest to those of our experimental model because the brain structures hosting the mirror mechanism are intact. In all these circumstances, corticomotor depression might lead to the instantiation of dysfunctional motor behavior. AOT can promote the maintenance of a central-to-periphery interplay resembling the premorbid one, thus favoring a faster restoration of motor function.
In central nervous system disorders (e.g., stroke), the patient's inability to move is due not to peripheral constraints but rather, to the damage of brain structures responsible for the generation and control of the movement. Following the abrupt disruption of motor programs, the motor system undergoes compensatory neural processes like perilesional remapping (54, 55) and interhemispheric functional rebalancing (56, 57); thus, the view of an exclusive, progressive corticomotor depression is unsuitable here. Maladaptive neural plasticity processes might occur in this case, and AOT can still limit their instantiation. This benefit is in line with the well-known effectiveness of AOT in promoting motor recovery in poststroke patients (4, 5). However, this capacity depends largely on the lesion’s extent and topography: that is, on the postinjury functioning of the corticomotor system. A promising aspect of our findings in relation to poststroke patients is the capacity of AOT to intervene mainly in MFr, which has been described as a key feature of stroke-related motor dysfunctions (58, 59).
Conclusions
The present study showed that administering AOT during immobilization limits the movement alterations induced by limb nonuse. Given AOT’s protective role against the decline of motor performance, action observation represents a valid, effective tool for early intervention in the motor system during limb nonuse, thus reducing the burden of further rehabilitation.
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