Internal models for interpreting neural population activity during sensorimotor control

• Published in: eLife Vol. 4
• Main Authors: Golub, Matthew D, Yu, Byron M, Chase, Steven M
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 08.12.2015; eLife Sciences Publications, Ltd
• Subjects: Animals; Brain-Computer Interfaces; brain-machine interfaces; Extremities - physiology; Feedback, Sensory; internal models; Macaca mulatta; Models, Neurological; motor control; Movement; Neuroscience; Psychomotor Performance; rhesus macaque; Sensorimotor Cortex - physiology; rhesus macaque; internal models; motor control; neuroscience; brain-machine interfaces
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.10015

To successfully guide limb movements, the brain takes in sensory information about the limb, internally tracks the state of the limb, and produces appropriate motor commands. It is widely believed that this process uses an internal model, which describes our prior beliefs about how the limb responds to motor commands. Here, we leveraged a brain-machine interface (BMI) paradigm in rhesus monkeys and novel statistical analyses of neural population activity to gain insight into moment-by-moment internal model computations. We discovered that a mismatch between subjects’ internal models and the actual BMI explains roughly 65% of movement errors, as well as long-standing deficiencies in BMI speed control. We then used the internal models to characterize how the neural population activity changes during BMI learning. More broadly, this work provides an approach for interpreting neural population activity in the context of how prior beliefs guide the transformation of sensory input to motor output. The human brain is widely hypothesized to construct “inner beliefs” about how the world works. It is thought that we need this conception to coordinate our movements and anticipate rapid events that go on around us. A driver, for example, needs to predict how the car should behave in response to every turn of the steering wheel and every tap on the brake. But on icy roads, these predictions will often not reflect how the car would behave. Applying the brakes sharply in these conditions could send the car skidding uncontrollably rather than stopping. In general, a mismatch between one’s inner beliefs and reality is thought to cause errors and accidents. Yet this compelling hypothesis has not yet been fully investigated. Golub et al. investigated this hypothesis by conducting a “brain-machine interface” experiment. In this experiment, neural signals from the brains of two rhesus macaques were recorded using arrays of electrodes and translated into movements of a cursor on a computer screen. The monkeys were then trained to mentally move the cursor to hit targets on the screen. The monkeys’ cursor movements were remarkably precise. In fact, the experiment showed that the monkeys could internally predict their cursor movements just as a driver predicts how a car will move when turning the steering wheel. These findings indicate that the monkeys have likely developed inner beliefs to predict how their neural signals drive the cursor, and that these beliefs helped coordinate their performance. In addition, when the monkeys did make mistakes, their neural signals were not entirely wrong—in fact they were typically consistent with the monkeys’ inner beliefs about how the cursor moves. A mismatch between these inner beliefs and reality explained most of the monkeys’ mistakes. The brain constructs such inner beliefs over time through experience and learning. To study this learning process, Golub et al. next conducted an experiment in which the cursor moved in a way that was substantially different from the monkey’s inner beliefs. This experiment uncovered that, during the course of learning, the monkey’s inner beliefs realigned to better match the movements of the new cursor. Taken together, this work provides a framework for understanding how the brain transforms sensory information into instructions for movement. The findings could also help improve the performance of brain-machine interfaces and suggest how we can learn new skills more rapidly and proficiently in everyday life.