Robust neural control of virtual locomotion enabled by a novel decoding strategy

Abstract

Brain-machine interfaces (BMIs) for reaching have enjoyed continued performance improvements, yet there remains significant need for BMIs that control other movement classes. Recent scientific findings suggest that the intrinsic covariance structure of neural activity depends strongly on movement class, potentially necessitating different decode algorithms across classes. To address this, we developed a self-motion BMI based on cortical activity as monkeys performed non-reaching arm movements: cycling a hand-held pedal to progress along a virtual track. Unlike during reaching, we found no high-variance dimensions that directly correlated with to-be-decoded variables. Yet we could decode a single variable - self-motion - by non-linearly leveraging structure that spanned many high-variance neural dimensions. Resulting online BMI-control success rates approached those during manual control. These findings make two broad points regarding how to build decode algorithms that harmonize with the empirical structure of neural activity in motor cortex. First, even when decoding from the same cortical region (e.g., arm-related motor cortex) different movement classes may need to employ very different strategies. Although correlations between neural activity and hand velocity are prominent during reaching tasks, they are not a fundamental property of motor cortex and cannot be counted on to be present in general. Second, although one generally desires a low-dimensional readout, it can be beneficial to leverage a multi-dimensional high-variance subspace. Fully embracing this approach requires highly non-linear approaches tailored to the task at hand, but can produce near-native levels of performance. Significance StatementMany BMI decoders have been constructed for controlling movements normally performed with the arm. Yet it is unclear how these will function beyond the reach-like scenarios where they were developed. Existing decoders implicitly assume that neural covariance structure, and correlations with to-be-decoded kinematic variables, will be largely preserved across tasks. We find that the correlation between neural activity and hand kinematics, a feature typically exploited when decoding reach-like movements, is essentially absent during another task performed with the arm: cycling through a virtual environment. Nevertheless, the use of a different strategy, one focused on leveraging the highest-variance neural signals, supported high performance real-time BMI control.