We tested the notion that action observation engages learning processes and mnemonic representations overlapping with those engaged in actual performance. An identical number of training instances, actual performance, or observation, was afforded on a finger opposition sequence task. Both training modes resulted in immediate gains in performance, as well as in robust delayed, "off-line," gains, indicating post-training consolidation. However, the expression of delayed gains could be blocked by the subsequent performance of a second sequence (post-training interference), but not by its observation. The mnemonic representations of "how-to" knowledge acquired from actual or observed movement may not overlap.[Supplemental material is available for this article.]The observation of action can lead to subsequent specific performance gains, presumably facilitating learning processes (Heyes and Foster 2002;Brown et al. 2003;Torriero et al. 2007;Hayes et al. 2010;Zhang et al. 2011). It is not clear, however, to what degree the beneficial effects of observation reflect a direct recruitment of the motor network involved in actual movement execution; specifically, whether the recruitment of the motor network through putative systems such as the "mirror neuron system," or an "action observation network" (AON) overlaps with the recruitment of the motor network in actual performance (Hari et al. 1998;Buccino et al. 2001;Calvo-Merino et al. 2006;Gazzola and Keysers 2009;Mukamel et al. 2010).This is a pertinent question given that there is increasing evidence that taskspecific changes in the motor cortex constitute an important part of the mnemonic representation of well-trained movement sequences (Karni et al. 1998;Yang et al. 2009Yang et al. , 2014Xu et al. 2010;Gabitov et al. 2014) and that along Hebbian lines, neurons involved in task execution are an integral part of the subsequent mnemonic representation. The AON presumably matches the perceived action with a neural representation within the motor repertoire of the observer. There is evidence, nevertheless, for performance gains even in observing new motor tasks, for which no representation is available in the observer's repertoire (Mattar and Gribble 2005;Stefan et al. 2005;Gatti et al. 2013).The aim of Experiment 1 was to compare the training-related performance gains in two training modes: actual training (Act) and training by observation (Obs) given equal practice on a five-element sequence of opposition movements ( Fig. 2A). Skill acquisition in different brain systems (modalities) is characterized by a distinct time-course (phases) (Karni and Sagi 1991, 1993;Karni 1996;Ari-Even Roth et al. 2005) presumably reflecting a similar repertoire of basic mechanism of plasticity and procedural memory consolidation processes (Karni and Bertini 1997;Dudai 2004;Robertson et al. 2004). Thus, a reasonable expectation would be that the acquisition of motor skills by observation would show phases of learning similar to those known to characterize learning when physical motor training...
Using the finger-to-thumb opposition sequence (FOS) learning task, we characterized motor skill learning in sub-acute patients hospitalized for rehabilitation following traumatic brain injury (TBI). Ten patients (Trained TBI) and 11 healthy participants (Trained Healthy) were trained using a multi-session protocol: a single session was afforded in the first week of the study, and four daily sessions were afforded during the second week. Intensity of practice was adapted to patients. Performance speed and accuracy were tested before and after each session. Retention was tested 1 month later. Ten patients (Control TBI) had no FOS training and were tested only at the beginning and the end of the 6 week period. Although baseline performance on the FOS was very slow, all three phases of skill learning found in healthy adults (acquisition, between-session consolidation gains, and long-term retention) could be identified in patients with TBI. However, their time-course of learning was atypical. The Trained TBI group improved in speed about double the spontaneous improvements observed in the Control TBI group, with no speed-accuracy tradeoff. Normalized to their initial performance on the FOS, the gains accrued by the Trained TBI group after a first training were comparable to those accrued by healthy adults. Only during the second week with daily training, the rate of improvement of the Trained TBI group lagged behind that of the Trained Healthy group, due to increasing within-sessions losses in performance speed; no such losses were found in healthy participants. The Functional Independence Measure scores at the start of the study correlated with the total gains attained at the end of the study; no correlations were found with severity of injury or explicit memory impairments. Despite within-sessions losses in performance, which we propose reflect cognitive fatigue, training resulted in robust overall learning and long-term retention in patients with moderate-severe TBI. Given that the gains in performance evolved mainly between sessions, as delayed, offline, gains, our results suggest that memory consolidation processes can be effectively engaged in patients with TBI. However, practice protocols and schedules may need to be optimized to better engage the potential for long-term plasticity in these patients.
The acquisition and retention of motor skills is necessary for everyday functioning in the elderly and may be critical in the context of motor rehabilitation. Recent studies indicate that motor training closely followed by sleep may result in better engagement of procedural (“how to”) memory consolidation processes in the elderly. Nevertheless, elderly individuals are mostly morning oriented and a common practice is to time rehabilitation programs to morning hours. Here, we tested whether the time-of-day wherein training is afforded (morning, 8–10:30 a.m., or evening, 6–9 p.m.) affects the long-term outcome of a multi-session motor practice program (10 sessions across 3–4 weeks) in healthy elderly participants. Twenty-nine (15 women) older adults (60–75 years) practiced an explicitly instructed five-element key-press sequence by repeatedly generating the sequence “as fast and accurately as possible.” The groups did not differ in terms of sleep habits and quality (1-week long actigraphy); all were morning-oriented individuals. All participants gained robustly from the intervention, shortening sequence tapping duration and retaining the gains (> 90%) at 1-month post-intervention, irrespective of the time-of-day of training. However, retesting at 7-months post-intervention showed that the attrition of the training induced gains was more pronounced in the morning trained group compared to the evening group (76 and 56.5% loss in sequence tapping time; 7/14 and 3/14 participants showed a > 5% decline in accuracy relative to end of training, respectively). Altogether, the results show that morning-oriented older adults effectively acquired skill in the performance of a sequence of finger movements, in both morning and evening practice sessions. However, evening training leads to a significant advantage, over morning training, in the long-term retention of the skill. Evening training should be considered an appropriate time window for motor skill learning in older adults, even in individuals with morning chronotype. The results are in line with the notion that motor training preceding a sleep interval may be better consolidated into long-term memory in the elderly, and thus result in lower forgetting rates.
How does the time of day of a practice session affect learning of a new motor sequence in the elderly? Participants practiced a given finger tapping sequence either during morning or evening hours. All participants robustly improved performance speed within the session concurrent with a reorganization of the tapping pattern of the sequence. However, evening-trained participants showed additional gains overnight and at 1 wk posttraining; moreover, evening training led to a further reorganization of the tapping pattern offline. A learning experience preceding nocturnal sleep can lead to a task-specific movement routine as an expression of novel “how to” knowledge in the elderly.
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