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Interpretive conundrums when practice doesn't always make perfect

The literature on motor learning in patients with Parkinson’s disease and the potential remedial effects of medication with L-dopa has yet to converge on an agreed message. Rather, many carefully controlled studies have produced a range of results beset with inconsistencies. Although, given the complexity of the neural networks implicated in generating adaptive movement, perhaps we should not be so surprised. Some of the important factors that interact to influence the variable outcomes of relevant experiments have already been identified. First, the concept of what constitutes, and the terms used to describe adaptive motor control can vary in different literatures. An important and clarifying distinction is between the acquisition of a motor skill (improvements in speed and accuracy), and motor adaptation (shifts in performance favoring speed or accuracy, or some form of sensorimotor recalibration). However, misunderstandings have arisen by researchers in different disciplines using different words for the same thing, and the same words for different things. For example, the concepts of conscious, voluntary, explicit, controlled, goal-directed, and model-based motor learning overlap, but may not be identical. Similarly, unconscious, involuntary, implicit, automatic, habitual and model-free motor learning may represent similar phenomenon at different levels of description. But at our present stage of understanding, it may be unwise to consider them as synonymous. It is possible, therefore, that some of the seemingly paradoxical findings in the motor learning literature arise through a lack of an agreed nomenclature and taxonomy. Secondly, many tasks of varying complexity have been used to investigate different aspects of motor learning in patients with Parkinson’s disease. However, for understandably practical reasons (issues associated with testing elderly patients), most studies have confined themselves to investigations of the rapid, early stages of learning. The levels of practice required for automatized, habitual control to become fully established have usually been avoided. Consequently, the current motor skill literature with patients is likely to be biased towards their refinement of goaldirected movements. Moreover, some more complex tasks could require variable mixtures of goal-directed and previously acquired habitual control. This is important because regionally segregated functional territories of the basal ganglia are differentially engaged during goal-directed and habitual control of behavior. Thirdly, Parkinson’s disease is a progressive disorder, which in itself has important implications for investigations of motor learning. Because many of the tests measure speed of responding, the difficulties patients experience in initiating movement and bradykinesia at different stages of the disease could account for some of the variable results. A further source of variability may be the progressive and sequential loss of dopamine from the regionally segregated functional territories of the basal ganglia. Typically, dopaminergic innervation is lost first from the sensorimotor territories of the caudal putamen, which over time, extends forward and ventrally to encompass the associative and limbic territories. Insofar as habits are associated with the sensorimotor basal ganglia, and goal-directed actions with the associative territories, patients tested at different stages of Parkinson’s disease will vary in their ability to acquire, perform and refine goal-directed actions and habits. Finally, when one part of the brain fails, other parts frequently adapt. Tests conducted at different stages of the disease may therefore face a variable interplay between degenerative and adaptive mechanisms. Fourthly, a critically important factor is whether patients are tested ON or OFF dopamine-restoring medication, usually L-dopa and/or direct acting dopaminergic agonists. Typically, patients receive sufficient medication to relieve their motor systems. In practice, this means a level of medication sufficient to restore dopaminergic transmission in the dopamine deprived sensorimotor basal ganglia. However, in patients where dopaminergic transmission in the associative and limbic territories is preserved, their medication is likely to produce supranormal levels of dopaminergic transmission. This effect may be -*Correspondence to: Peter Redgrave Dept. Psychology, University of Sheffield, Sheffield, S10 2TN, U.K.; P.Redgrave@sheffield.ac.uk