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cognitive neuroscience of skill acquisition

cognitive neuroscience of skill acquisition



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Cognitive Neuroscience of Skill
J. Bo, J. Langan, and R. D. Seidler
University of Michigan
1. Introduction

In this chapter, we provide an overview of contemporary research on the cognitive neuroscience of human motor skill learning. Other chapters found in this volume focus on animal models (Part IV) and current beha- vioral issues (Part III) of skill learning. As such, these topics are not addressed extensively here. Rather, they are touched upon to draw links across research paradigms, demonstrate parallels in theoretical questions addressed with differing techniques, and point out gaps in integration of the existing literature.

Current cognitive neuroscience techniques amenable to the study of skill learning include functional magnetic resonance imaging (fMRI), posi- tron emission tomography (PET), electroencepholography/magnetoence- pholography (EEG/MEG), and transcranial magnetic stimulation (TMS). These techniques provide differing relative advantages in terms of spatial and temporal resolution, and whether they allow for correlative vs. causa- tive inferences. These issues have been covered extensively elsewhere (Walsh & Cowey, 2000) and will not be addressed here.

Although the study of behavioral aspects of skill learning has a rich and long history dating back over 100 years (seeJames, 1890), determining the under- lying neural bases of these processes has necessarily lagged behind. Despite several hundred cognitive neuroscience investigations of skill learning that have been performed, many of the issues addressed in the behavioral chapters on skill acquisition in this volume have yet to be investigated with this approach. This is due in part to the relative infancy of the field (cf.Grafton

et al. 1992; Seitz & Roland 1992), the physical restrictions associated with most
cognitive neuroscience techniques, and the controls required to separate
neural activation associated with performance from that associated with
Human Learning
Aaron S. Benjamin, J. Steven de Belle, Bruce Etnyre, Thad A. Polk
\u00d32008 Elsevier Ltd. All rights reserved

learning. Parametric manipulation of variables such as movement rate, force, or motor error has revealed corresponding activation changes in the sensory and motor cortical and subcortical regions (Ashe, 1997; Dai, Liu, Sahgal,

Brown, & Yue, 2001; Deiber, Honda, Ibanez, Sadato, & Hallett, 1999; Dettmers et al., 1995, 1996; Jancke et al., 1998; Kitazawa, Kimura, & Yin, 1998; Mattay & Weinberger, 1999; Muley et al., 2001; Sadato et al., 1997; Schlaug et al., 1996; Turner, Grafton, Votaw, Delong, &, Hoffman, 1998). Since these same variables

change with skill acquisition, it is difficult to disentangle whether changes in brain activation are due to differing performance levels that occur with prac- tice, or rather reflect true contributions to learning.

Skill acquisition (used interchangeably with the term \u2018\u2018motor learning\u2019\u2019 in this chapter) has been defined as \u2018\u2018...a set of processes associated with practice or experience leading to relatively permanent changes in the capability for responding\u2019\u2019 (Schmidt, 1988). Researchers studying skill acquisition have classified learning into at least two broad categories, including sensorimotor adaptation and sequence learning (Doyon & Benali,

2005; Willingham 1998). In sensorimotor adaptation paradigms, partici-

pants modify movements to adjust to changes in either sensory input or motor output characteristics. For sequence learning, individuals learn to combine isolated movements into one smooth, coherent action. The last decade and a half has seen an explosion of publications using cognitive neuroscience techniques to study skill acquisition. We have learned much about the neural underpinnings of the two types of skill acquisition, and how their contributions are altered for different stages of learning. As outlined in this chapter, however, there are still some remaining contro- versies, and much left to be learned regardinghow the underlying circuitry maps onto the many processes of skill learning. For the sake of space limitations, we have elected to review some of the major current theories on the cognitive neuroscience of skill learning, and to draw attention to the overlap and differences among these theories. Although this review is not meant to be exhaustive, we hope to give the reader a view of the current status of the field, and the underlying questions that remain to be addressed.

2. Cognitive neuroscience models of sensorimotor adaptation

Sensorimotor adaptation tasks are used to gain insight into how humans represent their environment, the mechanics of the body, and interactions between the two during movement planning and production. These tasks can be described as either (1) dynamic (or kinetic) paradigms, which alter anticipated proprioception by having participants move the limb through an opposing force field (Shadmehr and Holcomb, 1997, 1999; Shadmehr and

J. Bo, J. Langan, and R. D. Seidler
Mussa-Ivaldi, 1994), or (2) kinematic paradigms, which disrupt visual feed-
back of movements through the use of displacing wedge prisms (Bossom &
Held, 1959; Redding, Rossetti, & Wallace, 2005; von Helmholtz, 1909/1962;)
or altered visual feedback on a computer screen (Bernotat, 1970; Bock,
1992; Cunningham, 1989; Pine, Krakauer, Gordon, & Ghez, 1996). It was

originally thought that dynamic and kinematic adaptation relied on differ- ent neural substrates, due to a lack of interference between the two types of adaptation during learning and consolidation (Krakauer, Ghilardi, &

Ghez, 1999). However, subsequent work demonstrated interference
between the two types of learning when the distortions were dependent
on the same kinematic variable (e.g., position-dependent displacements;
Tong, Wolpert, & Flanagan, 2002), suggesting that there is overlap. Indeed,
error processing of movements made under both dynamic and kinematic
distortions shows extensive neural overlap (Diedrichsen et al., 2005).
One influential model of the neural bases of skill learning isWillingham\u2019s
(1998)control-based learning theory (COBALT). It proposes that learning

can occur via tuning of the processes directly involved in the control of movement, or through the use of conscious, strategic processes. This model suggests that a ventral cortical system is engaged for explicit learning, where the participant is aware of the task and the goal to learn it. In this system, task goals are transferred from the prefrontal cortex to the posterior tem- poral lobe. The dorsal cortical learning system involves parietal and premo- tor areas and operates during implicit learning, where learning occurs outside of conscious awareness. COBALT proposes that the cerebellum does not play a direct role in skill learning, regardless of whether sequence learning or sensorimotor adaptation is taking place. An early PET study of prism adaptation supports this idea (Clower et al., 1996). These authors found that only the posterior parietal cortex was associated with adaptation, after accounting for correction of motor errors, a process that is known to engage the cerebellar circuitry (Kitazawa et al., 1998).

In contrast, some argue that internal models are updated during sensor- imotor adaptation, and the cerebellum plays a central role in this process (Ito, 2002; Miall, Weir, Wolpert, & Stein, 1993;Miall & Wolpert, 1996). An internal model is thought to use efference copy to predict the sensory consequences of a motor command (Miall & Wolpert, 1996). These models are updated via error feedback during sensorimotor adaptation (Shadmehr &

Mussa-Ivaldi, 1994). Work by Imamizu and colleagues (Imamizu, Kuroda, Miyauchi, Yoshioka, & Kawato, 2003; Imamizu, Kuroda, Yoshioka, & Kawato, 2004; Imamizu et al., 2000) has consistently shown activation in

the cerebellar regions surrounding the posterior superior fissure during adaptation of movements to differing visual distortions, even after correc- tion for performance differences occurring across the time course of learning.

Cognitive Neuroscience of Skill Acquisition

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