A Common Optimization Principle for Motor Execution in Healthy Subjects and Parkinsonian Patients

Baraduc, Pierre; Thobois, Stéphane; Gan, Jing; Broussolle, Emmanuel; Desmurget, Michel

doi:10.1523/jneurosci.1482-12.2013

Cited by 66 publications

(72 citation statements)

References 82 publications

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“…Our results are also consistent with the results of Baraduc, Thobois, Gan, Broussolle, and Desmurget (2013), who studied one-dimensional reaching movements by PD patients who had stimulating electrodes surgically implanted in the subthalamic nucleus. The latter study showed that a single optimal control model that minimized total neuromuscular cost (motor effort) could predict the speed of reaching movements by both healthy individuals and PD patients.…”

Section: Discussionsupporting

confidence: 91%

Dopamine Function and the Efficiency of Human Movement

Gepshtein

Snider

et al. 2014

Journal of Cognitive Neuroscience

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To sustain successful behavior in dynamic environments, active organisms must be able to learn from the consequences of their actions and predict action outcomes. One of the most important discoveries in systems neuroscience over the last 15 years has been about the key role of the neurotransmitter dopamine in mediating such active behavior. Dopamine cell firing was found to encode differences between the expected and obtained outcomes of actions. Although activity of dopamine cells does not specify movements themselves, a recent study in humans has suggested that tonic levels of dopamine in the dorsal striatum may in part enable normal movement by encoding sensitivity to the energy cost of a movement, providing an implicit “motor motivational” signal for movement. We investigated the motivational hypothesis of dopamine by studying motor performance of patients with Parkinson disease who have marked dopamine depletion in the dorsal striatum and compared their performance with that of elderly healthy adults. All participants performed rapid sequential movements to visual targets associated with different risk and different energy costs, countered or assisted by gravity. In conditions of low energy cost, patients performed surprisingly well, similar to prescriptions of an ideal planner and healthy participants. As energy costs increased, however, performance of patients with Parkinson disease dropped markedly below the prescriptions for action by an ideal planner and below performance of healthy elderly participants. The results indicate that the ability for efficient planning depends on the energy cost of action and that the effect of energy cost on action is mediated by dopamine.

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Section: Discussionsupporting

confidence: 91%

Dopamine Function and the Efficiency of Human Movement

Gepshtein

Snider

et al. 2014

Journal of Cognitive Neuroscience

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“…Although comprising a relatively small fraction of the general population of dopamine neurons, degeneration of the utility-encoding neurons described here (cells who’s encoding of reward was discounted by predicted energetic expenditures) may contribute to such a defective valuation. This inference is in agreement with clinical findings that parkinsonian bradykinesia reflects an exaggerated sensitivity to a movement’s energetic cost (Mazzoni et al, 2007; Baraduc et al, 2013). …”

Section: Discussionsupporting

confidence: 91%

“…These impairments cannot be explained by intrinsic limitations in motor execution, but rather result from a problem in scaling movement vigor due to a defective valuation of actions in terms of their energetic cost-benefit trade-off (Hallett and Khoshbin, 1980; Berardelli et al, 2001; Baraduc et al, 2013). Although comprising a relatively small fraction of the general population of dopamine neurons, degeneration of the utility-encoding neurons described here (cells who’s encoding of reward was discounted by predicted energetic expenditures) may contribute to such a defective valuation.…”

Section: Discussionmentioning

confidence: 99%

Limited Encoding of Effort by Dopamine Neurons in a Cost–Benefit Trade-off Task

Pasquereau

Turner

2013

J. Neurosci.

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Animals are thought to evaluate the desirability of action options using a unified scale that combines predicted benefits (“rewards”), costs, and the animal’s internal motivational state. Midbrain dopamine neurons have long been associated with the reward part of this equation, but it is unclear whether these neurons also estimate the costs of taking an action. We studied the spiking activity of dopamine neurons in the substantia nigra pars compacta of monkeys (Macaca mulatta) during a reaching task in which the energetic costs incurred (friction loads) and the benefits gained (drops of food) were manipulated independently. Although the majority of dopamine neurons encoded the upcoming reward alone, a subset predicted net utility of a course of action by signaling the expected reward magnitude, discounted by the invested cost in terms of physical effort. In addition, the tonic activity of some dopamine neurons was slowly reduced in conjunction with the accumulated trials, which is consistent with the hypothesized role for tonic dopamine in the invigoration or motivation of instrumental responding. The present results shed light on an oft-hypothesized role for dopamine in the regulation of the balance in natural behaviors between the energy expended and the benefits gained, which could explain why dopamine disorders, such as Parkinson’s disease, lead to a breakdown of that balance.

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“…This revealed that patients are biased toward slow movements, but also demonstrated that patients can move with the same speed and accuracy as control subjects (recently confirmed in a similar design by reference ). A subsequent study by Baraduc and colleagues allowed subjects to move a 1D joystick to a cued eccentric position without a prescribed range of movement speed . In this version of a free choice, variable‐amplitude operant task (hereafter, a VAO task), they found that untreated PD patients moved at systematically slower speeds, yet their movements were described by control laws that were indistinguishable from non‐PD subjects.…”

Section: Activity In Basal Ganglia Circuits Represents Movement Kinemmentioning

confidence: 99%

“…As a result, much interest has been focused on attempting to account for the mechanisms by which dopamine‐depletion produces the profound deficits in voluntary movement typical of parkinsonism . Bradykinesia, the slowing of movement speed, is directly attributed to the loss of dopaminergic innervation and dopamine replacement therapy using l ‐dopa can ameliorate bradykinesia in PD patients (although movement velocity does not fully recover with dopamine replacement therapy or deep brain stimulation). Further, the presence of augmented dopamine levels increased the speed and amplitude of voluntary movements …”

mentioning

confidence: 99%

A Proposed Circuit Computation in Basal Ganglia: History‐Dependent Gain

Yttri

Dudman

2018

Movement Disorders

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In this Scientific Perspectives we first review the recent advances in our understanding of the functional architecture of basal ganglia circuits. Then we argue that these data can best be explained by a model in which basal ganglia act to control the gain of movement kinematics to shape performance based on prior experience, which we refer to as a history‐dependent gain computation. Finally, we discuss how insights from the history‐dependent gain model might translate from the bench to the bedside, primarily the implications for the design of adaptive deep brain stimulation. Thus, we explicate the key empirical and conceptual support for a normative, computational model with substantial explanatory power for the broad role of basal ganglia circuits in health and disease. © 2018 The Authors. Movement Disorders published by Wiley Periodicals, Inc. on behalf of International Parkinson and Movement Disorder Society.

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A Common Optimization Principle for Motor Execution in Healthy Subjects and Parkinsonian Patients

Cited by 66 publications

References 82 publications

Dopamine Function and the Efficiency of Human Movement

Dopamine Function and the Efficiency of Human Movement

Limited Encoding of Effort by Dopamine Neurons in a Cost–Benefit Trade-off Task

A Proposed Circuit Computation in Basal Ganglia: History‐Dependent Gain

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