Motor cortex retains and reorients neural dynamics during motor imagery.

The most prominent characteristic of motor cortex is its activation during movement execution, but it is also active when we simply imagine movements in the absence of actual motor output. Despite decades of behavioural and imaging studies, it is unknown how the specific activity patterns and temporal dynamics in motor cortex during covert motor imagery relate to those during motor execution. Here we recorded intracortical activity from the motor cortex of two people who retain some residual wrist function following incomplete spinal cord injury as they performed both actual and imagined isometric wrist extensions. We found that we could decompose the population activity into three orthogonal subspaces, where one was similarly active during both action and imagery, and the others were active only during a single task type-action or imagery. Although they inhabited orthogonal neural dimensions, the action-unique and imagery-unique subspaces contained a strikingly similar set of dynamic features. Our results suggest that during motor imagery, motor cortex maintains the same overall population dynamics as during execution by reorienting the components related to motor output and/or feedback into a unique, output-null imagery subspace.

Propagating motor cortical patterns of excitability are ubiquitous across human and non-human primate movement initiation.

A spatiotemporal pattern of excitability propagates across the primary motor cortex prior to the onset of a reaching movement in non-human primates. If this pattern is a necessary component of voluntary movement initiation, it should be present across a variety of motor tasks, end-effectors, and even species. Here, we show that propagating patterns of excitability occur during the initiation of precision grip force and tongue protrusion in non-human primates, and even isometric wrist extension in a human participant. In all tasks, the directions of propagation across the cortical sheet were bimodally distributed across trials with modes oriented roughly opposite to one another. Propagation speed was unimodally distributed with similar mean speeds across tasks and species. Additionally, propagation direction and speed did not vary systematically with any behavioral measures except response times indicating that this propagating pattern is invariant to kinematic or kinetic details and may be a generic movement initiation signal.

Motor cortex retains and reorients neural dynamics during motor imagery.

The most prominent role of motor cortex is generating patterns of neural activity that lead to movement, but it is also active when we simply imagine movements in the absence of actual motor output. Despite decades of behavioral and imaging studies, it is unknown how the specific activity patterns and temporal dynamics within motor cortex during covert motor imagery relate to those during motor execution. Here we recorded intracortical activity from the motor cortex of two people with residual wrist function following incomplete spinal cord injury as they performed both actual and imagined isometric wrist extensions. We found that we could decompose the population-level activity into orthogonal subspaces such that one set of components was similarly active during both action and imagery, and others were only active during a single task typeâ€"action or imagery. Although they inhabited orthogonal neural dimensions, the action-unique and imagery-unique subspaces contained a strikingly similar set of dynamical features. Our results suggest that during motor imagery, motor cortex maintains the same overall population dynamics as during execution by recreating the missing components related to motor output and/or feedback within a unique imagery-only subspace.

From monkeys to humans: observation-basedEMGbrain-computer interface decoders for humans with paralysis.

Objective. Intracortical brain-computer interfaces (iBCIs) aim to enable individuals with paralysis to control the movement of virtual limbs and robotic arms. Because patients' paralysis prevents training a direct neural activity to limb movement decoder, most iBCIs rely on 'observation-based' decoding in which the patient watches a moving cursor while mentally envisioning making the movement. However, this reliance on observed target motion for decoder development precludes its application to the prediction of unobservable motor output like muscle activity. Here, we ask whether recordings of muscle activity from a surrogate individual performing the same movement as the iBCI patient can be used as target for an iBCI decoder.Approach. We test two possible approaches, each using data from a human iBCI user and a monkey, both performing similar motor actions. In one approach, we trained a decoder to predict the electromyographic (EMG) activity of a monkey from neural signals recorded from a human. We then contrast this to a second approach, based on the hypothesis that the low-dimensional 'latent' neural representations of motor behavior, known to be preserved across time for a given behavior, might also be preserved across individuals. We 'transferred' an EMG decoder trained solely on monkey data to the human iBCI user after using Canonical Correlation Analysis to align the human latent signals to those of the monkey.Main results. We found that both direct and transfer decoding approaches allowed accurate EMG predictions between two monkeys and from a monkey to a human.Significance. Our findings suggest that these latent representations of behavior are consistent across animals and even primate species. These methods are an important initial step in the development of iBCI decoders that generate EMG predictions that could serve as signals for a biomimetic decoder controlling motion and impedance of a prosthetic arm, or even muscle force directly through functional electrical stimulation.

Generalizable cursor click decoding using grasp-related neural transients.

Objective.Intracortical brain-computer interfaces (iBCI) have the potential to restore independence for individuals with significant motor or communication impairments. One of the most realistic avenues for clinical translation of iBCI technology is enabling control of a computer cursor-i.e. movement-related neural activity is interpreted (decoded) and used to drive cursor function. Here we aim to improve cursor click decoding to allow for both point-and-click and click-and-drag control.Approach.Using chronic microelectrode arrays implanted in the motor cortex of two participants with tetraplegia, we identified prominent neural responses related to attempted hand grasp. We then developed a new approach for decoding cursor click (hand grasp) based on the most salient responses.Main results.We found that the population-wide response contained three dominant components related to hand grasp: an onset transient response, a sustained response, and an offset transient response. The transient responses were larger in magnitude-and thus more reliably detected-than the sustained response, and a click decoder based on these transients outperformed the standard approach of binary state classification.Significance.A transient-based approach for identifying hand grasp can provide a high degree of cursor click control for both point-and-click and click-and-drag applications. This generalized click functionality is an important step toward high-performance cursor control and eventual clinical translation of iBCI technology.

Single reach plans in dorsal premotor cortex during a two-target task.

In many situations, we are faced with multiple potential actions, but must wait for more information before knowing which to perform. Movement scientists have long asked whether in these delayed-response situations the brain plans both potential movements simultaneously, or if it simply chooses one and then switches later if necessary. To answer this question, we used simultaneously recorded activity from populations of neurons in macaque dorsal premotor cortex to track moment-by-moment deliberation between two potential reach targets. We found that the neural activity only ever indicated a single-reach plan (with some targets favored more than others), and that initial plans often predicted the monkeys' behavior on both Free-Choice trials and incorrect Cued trials. Our results suggest that premotor cortex plans only one option at a time, and that decisions are strongly influenced by the initial response to the available set of movement options.

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

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.