Elsevier

NeuroImage

Volume 29, Issue 2, 15 January 2006, Pages 677-684
NeuroImage

Rapid Communication
Encoding a motor memory in the older adult by action observation

https://doi.org/10.1016/j.neuroimage.2005.07.039Get rights and content

Abstract

The ability of motor training to encode a motor memory is reduced in older adults. Here, we tested the hypothesis that training-dependent memory encoding, an issue of relevance in neurorehabilitation, is enhanced in elder individuals by action observation which alone can contribute to learning processes. A group of 11 healthy older adults participated in this study, which consisted of three randomized counterbalanced sessions on different days testing the effects of motor training (MT) alone, action observation (AO) alone, and a combination of both (MT + AO) on motor memory encoding. The combination of MT + AO formed a motor memory in the primary motor cortex and differentially modulated motor cortical excitability in muscles that were agonist and antagonist with respect to the training task, but MT or AO alone did not. These results suggest that action observation can enhance the effects of motor training on memory encoding protocols in the older adult, possibly through Hebbian modulation of intracortical excitatory mechanisms.

Introduction

Normal aging results in a decline in memory functions (Small, 2001, Hedden and Gabrieli, 2004), including episodic encoding (Schaie, 1993) and working memory (Park et al., 1996, Park et al., 2002). In the motor domain, training involving performance of simple repetitive thumb movements in a consistent direction encodes a memory trace in the primary motor cortex that reflects the kinematic details of the practiced movements (Classen et al., 1998, Butefisch et al., 2000, Butefisch et al., 2002, Sawaki et al., 2002b). In this protocol, transcranial magnetic stimulation (TMS) is applied to the primary motor cortex (M1) to identify changes in the organization and cortical excitability of motor representations within M1. This form of motor memory encoding is influenced by GABA, NMDA, cholinergic, alpha, and possibly beta adrenergic receptor function (Butefisch et al., 2000, Sawaki et al., 2002a, Sawaki et al., 2003a) and is enhanced by dopaminergic (Floel et al., 2005a, Floel et al., 2005b) and adrenergic agents (Butefisch et al., 2002, Sawaki et al., 2002b). The ability to form memories as a function of training, proposed to represent the first step in the acquisition of complex motor skills (Classen et al., 1998), decreases with normal aging (Sawaki et al., 2003b), a decline that may contribute to the limitations of functional recovery processes after CNS lesions such as stroke in older adults (Classen et al., 1998, Butefisch et al., 2004).

Action observation (AO) activates motor areas of the brain (Rizzolatti and Craighero, 2004) such as the ventral premotor cortex (PMv), and also the inferior parietal lobule (IPL). Neurons in these regions that discharge both in association with performance of a motor task and with observation of another individual performing the same action are described as “mirror neurons” (di Pellegrino et al., 1992, Gallese et al., 1996, Rizzolatti et al., 1996). Indirect evidence of the existence of the mirror neuron system exists in humans, where observation of an individual performing a motor task results in increased fMRI activity and cortical excitability in the observer's motor cortical regions that mediate performance of the observed movements (Iacoboni et al., 1999, Buccino et al., 2001). The mirror neuron system (Rizzolatti and Craighero, 2004) contributes to imitation (Iacoboni et al., 1999) and is probably involved in skill acquisition (Buccino et al., 2004). Recent work demonstrated in young adult human subjects that observation of another individual performing a motor task results in cortical reorganization within the motor representations in M1 that mediate the practiced motions (Stefan et al., 2003), encoding a motor memory. It is then possible that in the process of formation of motor memories, action observation could interact with motor training (MT), possibly enhancing training effects in older adults, the purpose of our investigation.

Section snippets

Participants

Eleven right-handed (Oldfield, 1971), healthy older adult volunteers (4 of them women, age range 58–78, 65 ± 6.8, mean ± SD) were included in this study. They all gave informed consent and the National Institute of Neurological Disorders and Stroke Institutional Review Board approved the experimental protocol. All participants fulfilled the following inclusion criteria: (a) ability of TMS to elicit isolated thumb movements in the absence of movements of any other digits, the wrist, or the arm;

Results

All participants completed the experimental protocol. None of the subjects could see their own hand or discern TMS-evoked movement directions and none of the subjects reported imagining themselves performing thumb movements during AO alone.

Discussion

The main findings of this study were (a) that action observation and motor training alone failed to encode a motor memory in older adults, and (b) that the combination of motor training + action observation compensated this deficit, enhancing training effects.

The process of aging is associated with memory decay (Small, 2001, Hedden and Gabrieli, 2004). For instance, motor memory encoding after training protocols decline in older adults (Sawaki et al., 2003b), possibly influencing motor learning

Acknowledgments

We wish to thank Steven Wise for his comments and Devee Schoenberg for skillful editing. PC is supported by the Rehabilitation Medicine Scientist Training Program (RMSTP), grant number: 5K12HD001097. FH is supported by a grant (Feodor-Lynen) from the A.v. Humboldt Foundation. This research was supported in part by the Intramural Research Program of the NIH, NINDS.

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