EARLY SLEEP AFTER ACTION OBSERVATION TRAINING BOOSTS IMPROVEMENTS IN MANUAL DEXTERITY

F. Temporiti^1,2, A. Calcagno³, S. Coelli³, G. Marino¹, A.M. Bianchi³, M. Galli³, R. Gatti^1,2

¹IRCCS Humanitas Clinical and Research Center, Physiotherapy Unit, Milano, Italy, ²Humanitas University, Department of Biomedical Sciences, Milano, Italy, ³Politecnico di Milano, Department of Electronic, Information and Bioengineering, Milano, Italy

Background: The observation of actions activates neural structures involved in the execution of observed tasks through a mirror mechanism. This process allows central nervous system to encode visual inputs into a motor representation of observed actions, enabling action understanding and facilitating motor learning through the building of a motor memory. The involvement of the mirror mechanism in motor learning allowed for the development of action observation training (AOT) to improve motor skills in healthy subjects or patients with motor impairments. Furthermore, when considering strategies to enhance motor learning, studies demonstrated that early sleep after practice enhances motor learning through an offline stabilization process. However, the effects of early sleep on motor learning induced by AOT have been poorly investigated.

Purpose: To investigate behavioral effects and neurophysiological correlates of AOT followed by early sleep on manual dexterity in healthy subjects.

Methods: Forty-five right-handed participants were randomized into three groups receiving a 3-week intervention (20 min. per day, 4 days a week) consisting of AOT immediately before sleeping (AOT-sleep group) or AOT at least 12 hours before sleeping (AOT-control) or a control stimulation (Control group). AOT implied the observation and motor imagery of transitive manual dexterity tasks performed in third and first-person perspectives with the dominant upper limb, whereas the control stimulation included landscape video-clips observation. Manual dexterity was assessed through functional (Purdue Pegboard Test - PPT), kinematic (kinematic indexes during Nine Hole Peg Test - NHPT) and neurophysiological outcomes (electroencephalographic signals recording during NHPT) before (T0) and after the training (T1) and at 1-month follow-up (T2).

Results: AOT-sleep and AOT-control groups improved manual dexterity during PPT and kinematic indexes during NHPT. Moreover, AOT-sleep group revealed significantly larger improvements than AOT-control group in terms of R-task of the PPT at T1 (MD: 1.72, CI₉₅ 0.12, 3.31, p=0.032), B-task of the PPT at T2 (MD: 1.6, CI₉₅ 0.28, 2.92, p=0.013), R+L+B (MD: 4.2, CI₉₅ 0.18, 8.31, p=0.038) and Assembly-task at T2 (MD: 4.8, CI₉₅ 0.07, 9.58, p=0.046). When considering electroencephalographic recording during NHPT execution, higher mu-band power variation (T1-T0) was found for AOT-sleep compared to AOT-control (p=0.016) and Control (p=0.012) groups in the frontal region of interest. In addition, higher mu-band power variation (T1-T0) was found for AOT-sleep group compared to Control (p=0.023) group in the parietal region of interest. Finally, moderate positive correlation was found between changes from T0 to T1 in the L-task of the PPT and mu-band power variations (T1-T0) in frontal (r=0.458, p=0.001) and parietal (r=0.360, p=0.016) regions of interest during NHPT with the non-dominant hand.

Conclusions: Participants undergoing AOT improved manual dexterity, but subjects performing AOT followed by early sleep had significantly larger improvements than those undergoing the same training at least 12 hours before sleeping.

Implications: Early sleep induces additional benefits on motor performance, also when the training is administered through a systematic observation and mental practice of motor tasks. The stimulation of the motor system through a mirror mechanism before sleeping may represent a strategy to enhance motor learning in several neurological and musculoskeletal conditions.

Funding acknowledgements: The authors did not receive any funding.

Keywords:
Action observation
Manual dexterity
Sleep-dependent motor learning

Topics:
Neurology
Disability & rehabilitation

Did this work require ethics approval? Yes

Institution: IRCCS Humanitas Clinical and Research Center

Committee: Internal Committee of Humanitas Clinical and Research Center

Ethics number: CLF20/08