Cortical Control of Virtual Self-Motion Using Task-Specific Subspaces.

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 possibility, we developed a self-motion BMI based on cortical activity as monkeys cycled 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. This was due to no neurons having consistent correlations between their responses and kinematic variables. Yet we could decode a single variable-self-motion-by nonlinearly leveraging structure that spanned multiple 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 multidimensional high-variance subspace. Fully embracing this approach requires highly nonlinear approaches tailored to the task at hand, but can produce near-native levels of performance.SIGNIFICANCE STATEMENT Many brain-machine interface 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 brain-machine interface control.

Flexible neural control of motor units.

Voluntary movement requires communication from cortex to the spinal cord, where a dedicated pool of motor units (MUs) activates each muscle. The canonical description of MU function rests upon two foundational tenets. First, cortex cannot control MUs independently but supplies each pool with a common drive. Second, MUs are recruited in a rigid fashion that largely accords with Henneman's size principle. Although this paradigm has considerable empirical support, a direct test requires simultaneous observations of many MUs across diverse force profiles. In this study, we developed an isometric task that allowed stable MU recordings, in a rhesus macaque, even during rapidly changing forces. Patterns of MU activity were surprisingly behavior-dependent and could be accurately described only by assuming multiple drives. Consistent with flexible descending control, microstimulation of neighboring cortical sites recruited different MUs. Furthermore, the cortical population response displayed sufficient degrees of freedom to potentially exert fine-grained control. Thus, MU activity is flexibly controlled to meet task demands, and cortex may contribute to this ability.

Interplay between components of pupil-linked phasic arousal and its role in driving behavioral choice in Go/No-Go perceptual decision-making.

In decision-making tasks, neural circuits involved in different aspects of information processing may activate the central arousal system, likely through their interconnection with brainstem arousal nuclei, collectively contributing to the observed pupil-linked phasic arousal. However, the individual components of the phasic arousal associated with different elements of information processing and their effects on behavior remain little known. In this study, we used machine learning techniques to decompose pupil-linked phasic arousal evoked by different components of information processing in rats performing a Go/No-Go perceptual decision-making task. We found that phasic arousal evoked by stimulus encoding was larger for the Go stimulus than the No-Go stimulus. For each session, the separation between distributions of phasic arousal evoked by the Go and by the No-Go stimulus was predictive of perceptual performance. The separation between distributions of decision-formation-evoked arousal on correct and incorrect trials was correlated with decision criterion but not perceptual performance. When a Go stimulus was presented, the action of go was primarily determined by the phasic arousal evoked by stimulus encoding. On the contrary, when a No-Go stimulus was presented, the action of go was determined by phasic arousal elicited by both stimulus encoding and decision formation. Drift diffusion modeling revealed that the four model parameters were better accounted for when phasic arousal elicited by both stimulus encoding and decision formation was considered. These results suggest that the interplay between phasic arousal evoked by both stimulus encoding and decision formation has important functional consequences on forming behavioral choice in perceptual decision-making.

Neural Trajectories in the Supplementary Motor Area and Motor Cortex Exhibit Distinct Geometries, Compatible with Different Classes of Computation.

The supplementary motor area (SMA) is believed to contribute to higher order aspects of motor control. We considered a key higher order role: tracking progress throughout an action. We propose that doing so requires population activity to display low "trajectory divergence": situations with different future motor outputs should be distinct, even when present motor output is identical. We examined neural activity in SMA and primary motor cortex (M1) as monkeys cycled various distances through a virtual environment. SMA exhibited multiple response features that were absent in M1. At the single-neuron level, these included ramping firing rates and cycle-specific responses. At the population level, they included a helical population-trajectory geometry with shifts in the occupied subspace as movement unfolded. These diverse features all served to reduce trajectory divergence, which was much lower in SMA versus M1. Analogous population-trajectory geometry, also with low divergence, naturally arose in networks trained to internally guide multi-cycle movement.

Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response.

Primate motor cortex projects to spinal interneurons and motoneurons, suggesting that motor cortex activity may be dominated by muscle-like commands. Observations during reaching lend support to this view, but evidence remains ambiguous and much debated. To provide a different perspective, we employed a novel behavioral paradigm that facilitates comparison between time-evolving neural and muscle activity. We found that single motor cortex neurons displayed many muscle-like properties, but the structure of population activity was not muscle-like. Unlike muscle activity, neural activity was structured to avoid "tangling": moments where similar activity patterns led to dissimilar future patterns. Avoidance of tangling was present across tasks and species. Network models revealed a potential reason for this consistent feature: low tangling confers noise robustness. Finally, we were able to predict motor cortex activity from muscle activity by leveraging the hypothesis that muscle-like commands are embedded in additional structure that yields low tangling.