Uncertainty leads to persistent effects on reach representations in dorsal premotor cortex

  • Dekleva B
  • Ramkumar P
  • Wanda P
  • et al.
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Abstract

Every movement we make represents one of many possible actions. In reaching tasks with multiple targets, dorsal premotor cortex (PMd) appears to represent all possible actions simultaneously. However, in many situations we are not presented with explicit choices. Instead, we must estimate the best action based on noisy information and execute it while still uncertain of our choice. Here we asked how both primary motor cortex (M1) and PMd represented reach direction during a task in which a monkey made reaches based on noisy, uncertain target information. We found that with increased uncertainty, neurons in PMd actually enhanced their representation of unlikely movements throughout both planning and execution. The magnitude of this effect was highly variable across sessions, and was correlated with a measure of the monkeys’ behavioral uncertainty. These effects were not present in M1. Our findings suggest that PMd represents and maintains a full distribution of potentially correct actions.Whether it is trying to find the light switch in a dimly lit room or reaching for your glasses when you wake in the morning, we often need to reach toward objects that we cannot see clearly. In these situations, we plan our movements based both on the limited sensory information that is available, as well as what we have learned from similar situations in the past.The brain areas involved in using information to decide on the best movement plan appear to be different from those involved in actually executing that plan. One area in particular, called the dorsal premotor cortex (or PMd), is thought to help a person decide where to reach when they are presented with two or more alternative targets. However, it was not known how this brain area is involved in choosing a direction to reach when the targets are fuzzy, or unable to be seen clearly.Dekleva et al. trained Rhesus macaque monkeys to reach in various directions, towards targets that were represented by fuzzy, uncertain visual cues. These targets were not simply positioned randomly; instead they were more likely to require reaches in certain directions over other directions. Because there were many such training and experimental sessions, the monkeys were able to learn where targets were more likely to be located. Dekleva et al. found that, like humans, the monkeys combined this knowledge from previous experience with the fuzzy visual information; like people, the monkeys also weighted each source of information based on how well they trusted it. For example, blurrier targets were treated as less trustworthy.Further analysis showed that neurons in the PMd signaled the chosen direction well before the monkey began to reach. However, throughout the entire time the monkey was reaching, the same neurons also seemed to hold in reserve the other, less likely reach directions. In contrast, neurons in the area of the brain that directly controls movement – the primary motor cortex – only ever signaled the direction in which the monkey actually reached.Further work is now needed to understand the decision-making process that appears to start in the PMd and resolve in the primary motor cortex. In particular, future experiments could explore why the retained information about other possible reach decisions persists throughout the movement, including if this helps the individual to rapidly correct errors or to slowly improve movements over time.

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Dekleva, B. M., Ramkumar, P., Wanda, P. A., Kording, K. P., & Miller, L. E. (2016). Uncertainty leads to persistent effects on reach representations in dorsal premotor cortex. ELife, 5. https://doi.org/10.7554/elife.14316

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