Dopamine Function and the Efficiency of Human Movement

Abstract

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.

The Striatum: Where Skills and Habits Meet

“…This result has led to the conclusion that extremely fine-grain, trial-by-trial monitoring of least cost can be a driver of habit learning, as well as a driver of skill learning. These results are in line with the notion that the brain has a natural tendency to reduce cost across many cognitive domains and that this tendency, in addition to sensitivity to reward, can drive the character of habits (Desrochers et al 2010;Kool et al 2010;Gepshtein et al 2014). Recent electrophysiological recordings suggest that striatal projection neurons encode these outcome and cost signals in their end activity (T Desrochers, K Amemori, and AM Graybiel, unpubl.…”

Modeling falls in Parkinson's disease: Slow gait, freezing episodes and falls in rats with extensive striatal dopamine loss

“…27). As DA losses extend through the striatum, low motivation or vigor for movement manifests as a general symptom of PD [11,28,29]. In large DA rats assessed on the MCMCT, the failure to initiate corrective movements after spontaneous or slip-triggered stoppages may model this deficit, with movement stoppage being considered an extreme expression such low vigor for movement.…”

Where attention falls: Increased risk of falls from the converging impact of cortical cholinergic and midbrain dopamine loss on striatal function

“…However, striatal dopamine loss was previously documented to generally slow responding and decrease response accuracy in tasks involving habitual or automatic responding or tasks requiring shifts between behavioral contingencies (Baunez and Robbins, 1999; Cools et al, 2001; Crofts et al, 2001; Darvas and Palmiter, 2009; Devan et al, 1999; Domenger and Schwarting, 2008; Gauntlett-Gilbert et al, 1999; Hauber and Schmidt, 1994; Lex and Hauber, 2010; Rogers et al, 2001). Furthermore, low striatal dopamine levels in PD patients are associated with movement impairments if the biomechanical costs are high (Gepshtein et al, 2014). The behavioral risk factors for falls seen in DL rats (see point 3 above), particularly the slowing of traversal and the presence of micropauses, may reflect impairments in the planning and sequencing of movements and, more generally, low “motor motivation”.…”