Reward processing abnormalities in Parkinson's disease

Kapogiannis, Dimitrios; Mooshagian, Eric; Campion, Paul; Grafman, Jordan; Zimmermann, Trelawny; Ladt, Kelsey; Wassermann, Eric M.

doi:10.1002/mds.23701

Cited by 41 publications

(36 citation statements)

References 37 publications

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“…Other TMS studies (Gupta & Aron, 2011; Kapogiannis et al, 2008; 2011) have shown that excitability of the corticospinal system changes in response to predicted outcomes in extrinsically rewarded tasks. However, this is the first TMS experiment attempting to dissociate the influences of probability and uncertainty.…”

Section: Discussionmentioning

confidence: 99%

“…In a few recent human studies, investigators applied TMS over M1 to measure changes in corticospinal output excitability in response to reward-related events. These studies found increased corticospinal excitability with the desirability of an outcome (Gupta & Aron, 2011) or a momentary reward (Thabit et al, 2011), and increased paired-pulse inhibition with increased expectation of receiving a reward while passively viewing a slot-machine simulation (Kapogiannis, Campion, Grafman, & Wassermann, 2008; Kapogiannis et al, 2011). The neural basis of these effects remains unknown, but they almost certainly reflect neural signaling about outcomes and values (Kapogiannis et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Modulation of corticospinal excitability by reward depends on task framing

et al. 2015

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Findings from previous transcranial magnetic stimulation (TMS) experiments suggest that the primary motor cortex (M1) is sensitive to reward conditions in the environment. However, the nature of this influence on M1 activity is poorly understood. The dopamine neuron response to conditioned stimuli encodes reward probability and outcome uncertainty, or the extent to which the outcome of a situation is known. Reward uncertainty and probability are related: uncertainty is maximal when probability is 0.5 and minimal when probability is 0 or 1 (i.e., certain outcome). Previous TMS-reward studies did not examine these factors independently. Here, we used single-pulse TMS to measure corticospinal excitability in 40 individuals while they performed a simple computer task, making guesses to find or avoid a hidden target. The task stimuli implied three levels of reward probability and two levels of uncertainty. We found that reward probability level interacted with the trial search condition. That is, motor evoked potential (MEP) amplitude, a measure of corticospinal neuron excitability, increased with increasing reward probability when participants were instructed to “find” a target, but not when they were instructed to “avoid” a target. There was no effect of uncertainty on MEPs. Response times varied with the number of choices. A subset of participants also received paired-pulse stimulation to evaluate changes in short-intracortical inhibition (SICI). No effects of SICI were observed. Taken together, the results suggest that the reward-contingent modulation of M1 activity reflects reward probability or a related aspect of utility, not outcome uncertainty, and that this effect is sensitive to the conceptual framing of the task.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Modulation of corticospinal excitability by reward depends on task framing

et al. 2015

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“…This in turn may lead to the encoding of longer-term representations of motor learning in M1. The hypothesis that reward-related midbrain dopaminergic signals modulate M1 activity is supported by findings that reward modulates M1 excitability in neurologically intact adults (Thabit et al 2011) but not in PD patients (Kapogiannis et al 2011). In PD, a rewarded motor outcome that occurs as a result of executing the adapted movement might elicit a blunted response from midbrain dopaminergic neurons and lead to attenuated modulation of M1 excitability and thus impaired encoding of longer-term representations of motor learning in M1.…”

Section: Neural Mechanisms Underlying Savingsmentioning

confidence: 98%

Impaired savings despite intact initial learning of motor adaptation in Parkinson’s disease

2012

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In motor adaptation, the occurrence of savings (faster relearning of a previously learned motor adaptation task) has been explained in terms of operant reinforcement learning (Huang et al. in Neuron 70(4):787-801, 2011), which is thought to associate an adapted motor command with outcome success during repeated execution of the adapted movement. There is some evidence for deficient savings in Parkinson's Disease (PD), which might result from deficient operant reinforcement processes. However, this evidence is compromised by limited adaptation training during initial learning and by multi-target adaptation, which reduces the number of reinforced movement repetitions for each target. Here, we examined savings in PD patients and controls following overlearning with a single target. PD patients showed less savings than controls after successive adaptation and deadaptation blocks within the same test session, as well as less savings across test sessions separated by a 24-h delay. It is argued that impaired blunted dopaminergic signals in PD impairs the modulation of dopaminergic signals to the motor cortex in response to rewarding motor outcomes, thus impairing the association of the adapted motor command with rewarding motor outcomes. Consequently, the previously adapted motor command is not preferentially selected during relearning, and savings is impaired.

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“…Given these considerations, one might speculate that motor cortex excitability may be related to state rather than trait measures of personality. This speculation is carried by two recent publications of Wassermann and colleagues which showed dependency of motor cortex excitability on reward expectation as elicited by double-pulse TMS (Kapogiannis et al, 2008(Kapogiannis et al, , 2011. Increased reward expectation was accompanied by an increase in paired-pulse inhibition (Kapogiannis et al, 2008).…”

Section: Discussionmentioning

confidence: 87%

“…Increased reward expectation was accompanied by an increase in paired-pulse inhibition (Kapogiannis et al, 2008). In addition, this effect could not be found in patients with Parkinson's disease; however, one single dose of the dopamine agonist pramipexole restored this effect (Kapogiannis et al, 2011). The authors concluded that this effect is probably mediated by the physiological state of dopaminergic reward areas of the basal ganglia which project to M1.…”

Section: Discussionmentioning

confidence: 93%