Covert motor learning can sometimes transfer to overt behavior. We investigated the neural mechanism underlying transfer by constructing a two-context paradigm. Subjects performed cursor movements either overtly using arm movements, or covertly via a brain-machine interface that moves the cursor based on motor cortical activity (in lieu of arm movement). These tasks helped evaluate whether and how cortical changes resulting from "covert rehearsal" affect overt performance. We found that covert learning indeed transfers to overt performance and is accompanied by systematic population-level changes in motor preparatory activity. Current models of motor cortical function ascribe motor preparation to achieving initial conditions favorable for subsequent movement-period neural dynamics. We found that covert and overt contexts share these initial conditions, and covert rehearsal manipulates them in a manner that persists across context changes, thus facilitating overt motor learning. This transfer learning mechanism might provide new insights into other covert processes like mental rehearsal.

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Voluntary movements are widely considered to be planned before they are executed. Recent studies have hypothesized that neural activity in motor cortex during preparation acts as an ‘initial condition’ which seeds the proceeding neural dynamics. Here, we studied these initial conditions in detail by investigating 1) the organization of neural states for different reaches and 2) the variance of these neural states from trial to trial. We examined population-level responses in macaque premotor cortex (PMd) during the preparatory stage of an instructed-delay center-out reaching task with dense target configurations. We found that after target onset the neural activity on single trials converges to neural states that have a clear low-dimensional structure which is organized by both the reach endpoint and maximum speed of the following reach. Further, we found that variability of the neural states during preparation resembles the spatial variability of reaches made in the absence of visual feedback: there is less variability in direction than distance in neural state space. We also used offline decoding to understand the implications of this neural population structure for brain-machine interfaces (BMIs). We found that decoding of angle between reaches is dependent on reach distance, while decoding of arc-length is independent. Thus, it might be more appropriate to quantify decoding performance for discrete BMIs by using arc-length between reach end-points rather than the angle between them. Lastly, we show that in contrast to the common notion that direction can better be decoded than distance, their decoding capabilities are comparable. These results provide new insights into the dynamical neural processes that underline motor control and can inform the design of BMIs.

Objective Making mistakes is inevitable, but identifying them allows us to correct or adapt our behavior to improve future performance. Current brain-machine interfaces (BMIs) make errors that need to be explicitly corrected by the user, thereby consuming time and thus hindering performance. We hypothesized that neural correlates of the user perceiving the mistake could be used by the BMI to automatically correct errors. However, it was unknown whether intracortical outcome error signals were present in the premotor and primary motor cortices, brain regions successfully used for intracortical BMIs. Approach We report here for the first time a putative outcome error signal in spiking activity within these cortices when rhesus macaques performed an intracortical BMI computer cursor task. Main results We decoded BMI trial outcomes shortly after and even before a trial ended with 96% and 84% accuracy, respectively. This led us to develop and implement in real-time a first-of-its-kind intracortical BMI error “detect-and-act” system that attempts to automatically “undo” or “prevent” mistakes. The detect-and-act system works independently and in parallel to a kinematic BMI decoder. In a challenging task that resulted in substantial errors, this approach improved the performance of a BMI employing two variants of the ubiquitous Kalman velocity filter, including a state-of-the-art decoder (ReFIT-KF). Significance Detecting errors in real-time from the same brain regions that are commonly used to control BMIs should improve the clinical viability of BMIs aimed at restoring motor function to people with paralysis.

Brain machine interfaces (BMIs) aim to assist people with paralysis by increasing their independence and ability to communicate, e.g., by using a cursor-based virtual keyboard. Current BMI clinical trials are hampered by modest performance that causes selection of wrong characters (errors) and thus reduces achieved typing rate. If it were possible to detect these errors without explicit knowledge of the task goal, this could be used to automatically "undo" wrong selections or even prevent upcoming wrong selections. We decoded imminent or recent errors during closed-loop BMI control from intracortical spiking neural activity. In our experiment, a non-human primate controlled a neurally-driven BMI cursor to acquire targets on a grid, which simulates a virtual keyboard. In offline analyses of this closed-loop BMI control data, we identified motor cortical neural signals indicative of task error occurrence. We were able to detect task outcomes (97% accuracy) and even predict upcoming task outcomes (86% accuracy) using neural activity alone. This novel strategy may help increase the performance and clinical viability of BMIs.