Slowing of Movements in Healthy Aging as a Rational Economic Response to an Elevated Effort Landscape.

Why do we move slower as we grow older? The reward circuits of the brain, which tend to invigorate movements, decline with aging, raising the possibility that reduced vigor is due to the diminishing value that our brain assigns to movements. However, as we grow older, it also becomes more effortful to make movements. Is age-related slowing principally a consequence of increased effort costs from the muscles, or reduced valuation of reward by the brain? Here, we first quantified the cost of reaching via metabolic energy expenditure in human participants (male and female), and found that older adults consumed more energy than the young at a given speed. Thus, movements are objectively more costly for older adults. Next, we observed that when reward increased, older adults, like the young, responded by initiating their movements earlier. Yet, unlike the young, they were unwilling to increase their movement speed. Was their reluctance to reach quicker for rewards due to the increased effort costs, or because they ascribed less value to the movement? Motivated by a mathematical model, we next made the young experience a component of aging by making their movements more effortful. Now the young responded to reward by reacting faster but chose not to increase their movement speed. This suggests that slower movements in older adults are partly driven by an adaptive response to an elevated effort landscape. Moving slower may be a rational economic response the brain is making to mitigate the elevated effort costs that accompany aging.

Disentangling the effects of metabolic cost and accuracy on movement speed.

On any given day, we make countless reaching movements to objects around us. While such ubiquity may suggest uniformity, each movement's speed is unique-why is this? Reach speed is known to be influenced by accuracy; we slow down to sustain high accuracy. However, in other forms of movement like walking or running, metabolic cost is often the primary determinant of movement speed. Here we bridge this gap and ask: how do metabolic cost and accuracy interact to determine speed of reaching movements? First, we systematically measure the effect of increasing mass on the metabolic cost of reaching across a range of movement speeds. Next, in a sequence of three experiments, we examine how added mass affects preferred reaching speed across changing accuracy requirements. We find that, while added mass consistently increases metabolic cost thereby leading to slower metabolically optimal movement speeds, self-selected reach speeds are slower than those predicted by an optimization of metabolic cost alone. We then demonstrate how a single model that considers both accuracy and metabolic costs can explain preferred movement speeds. Together, our findings provide a unifying framework to illuminate the combined effects of metabolic cost and accuracy on movement speed and highlight the integral role metabolic cost plays in determining reach speed.

Metabolic costs of walking and arm reaching in persons with mild multiple sclerosis.

Movement slowness is a common and disruptive symptom of multiple sclerosis (MS). A potential cause is that individuals with MS slow down to conserve energy as a behavioral adjustment to heightened metabolic costs of movement. To investigate this prospect, we measured the metabolic costs of both walking and seated arm reaching at five speeds in persons with mild MS (pwMS; n = 13; 46.0 ± 7.7 yr) and sex- and age-matched controls (HCs; n = 13; 45.8 ± 7.8 yr). Notably, the cohort of pwMS was highly mobile and no individuals required a cane or aid when walking. We found that the net metabolic power of walking was approximately 20% higher for pwMS across all speeds (P = 0.0185). In contrast, we found no differences in the gross power of reaching between pwMS and HCs (P = 0.492). Collectively, our results suggest that abnormal slowness of movement in MS-particularly reaching-is not the consequence of heightened effort costs and that other sensorimotor mechanisms are playing a considerable role in slowing.NEW & NOTEWORTHY Individuals with multiple sclerosis (MS) often move more slowly than those without the disease. A possible cause is that movements in MS are more energetically expensive and slowing is an adaptation to conserve metabolic resources. Here, we find that while walking is more costly for persons with MS, arm-reaching movements are not. These results bring into question the driving force of movement slowness in MS and implicate other motor-related networks contributing to slowing.

Effort cost of reaching prompts vigor reduction in older adults.

As people age, they move slower. Is age-related reduction in vigor a reflection of a reduced valuation of reward by the brain, or a consequence of increased effort costs by the muscles? Here, we quantified cost of movements objectively via the metabolic energy that young and old participants consumed during reaching and found that in order reach at a given speed, older adults expended more energy than the young. We next quantified how reward modulated movements in the same populations and found that like the young, older adults responded to increased reward by initiating their movements earlier. Yet, their movements were less sensitive to increased reward, resulting in little or no modulation of reach speed. Lastly, we quantified the effect of increased effort on how reward modulated movements in young adults. Like the effects of aging, when faced with increased effort the young adults responded to reward primarily by reacting faster, with little change in movement speed. Therefore, reaching required greater energetic expenditure in the elderly, suggesting that the slower movements and reactions exhibited in aging are partly driven by an adaptive response to an elevation in the energetic landscape of effort. That is, moving slower appears to be a rational economic consequence of aging. Significance statement: Healthy aging coincides with a reduction in speed, or vigor, of walking, reaching, and eye movements. Here we focused on disentangling two opposing sources of aging-related movement slowing: reduced reward sensitivity due to loss of dopaminergic tone, or increased energy expenditure movements related to mitochondrial or muscular inefficiencies. Through a series of three experiments and construction of a computational model, here we demonstrate that transient changes in reaction time and movement speed together offer a quantifiable metric to differentiate between reward- and effort-based alterations in movement vigor. Further, we suggest that objective increases in the metabolic cost of moving, not reductions in reward valuation, are driving much of the movement slowing occurring alongside healthy aging.