Motor, sensory, and cognitive learning require networks of neurons to generate new activity patterns. Because some behaviors are easier to learn than others1,2, we wondered if some neural activity patterns are easier to generate than others. We asked whether the existing network constrains the patterns that a subset of its neurons is capable of exhibiting, and if so, what principles define the constraint. We employed a closed-loop intracortical brain-computer interface (BCI) learning paradigm in which Rhesus monkeys controlled a computer cursor by modulating neural activity patterns in primary motor cortex. Using the BCI paradigm, we could specify and alter how neural activity mapped to cursor velocity. At the start of each session, we observed the characteristic activity patterns of the recorded neural population. These patterns comprise a low-dimensional space (termed the intrinsic manifold, or IM) within the high-dimensional neural firing rate space. They presumably reflect constraints imposed by the underlying neural circuitry. We found that the animals could readily learn to proficiently control the cursor using neural activity patterns that were within the IM. However, animals were less able to learn to proficiently control the cursor using activity patterns that were outside of the IM. This result suggests that the existing structure of a network can shape learning. On the timescale of hours, it appears to be difficult to learn to generate neural activity patterns that are not consistent with the existing network structure. These findings offer a network-level explanation for the observation that we are more readily able to learn new skills when they are related to the skills that we already possess3,4.

Significant experimental, computational, and theoretical work has identified rich structure within the coordinated activity of interconnected neural populations. An emerging challenge now is to uncover the nature of the associated computations, how they are implemented, and what role they play in driving behavior. We term this computation through neural population dynamics. If successful, this framework will reveal general motifs of neural population activity and quantitatively describe how neural population dynamics implement computations necessary for driving goal-directed behavior. Here, we start with a mathematical primer on dynamical systems theory and analytical tools necessary to apply this perspective to experimental data. Next, we highlight some recent discoveries resulting from successful application of dynamical systems. We focus on studies spanning motor control, timing, decision-making, and working memory. Finally, we briefly discuss promising recent lines of investigation and future directions for the computation through neural population dynamics framework.

Behavior is driven by coordinated activity across a population of neurons. Learning requires the brain to change the neural population activity produced to achieve a given behavioral goal. How does population activity reorganize during learning? We studied intracortical population activity in the primary motor cortex of rhesus macaques during short-term learning in a brain-computer interface (BCI) task. In a BCI, the mapping between neural activity and behavior is exactly known, enabling us to rigorously define hypotheses about neural reorganization during learning. We found that changes in population activity followed a suboptimal neural strategy of Reassociation: animals relied on a fixed repertoire of activity patterns and associated those patterns with different movements after learning. These results indicate that the activity patterns that a neural population can generate are even more constrained than previously thought and might explain why it is often difficult to quickly learn to a high level of proficiency.

Learning has been associated with changes in the brain at every level of organization. However, it remains difficult to establish a causal link between specific changes in the brain and new behavioral abilities. We establish that new neural activity patterns emerge with learning. We demonstrate that these new neural activity patterns cause the new behavior. Thus, the formation of new patterns of neural population activity can underlie the learning of new skills.

Motor cortex plays a substantial role in driving movement, yet the details underlying this control remain unresolved. We analyzed the extent to which movement-related information could be extracted from single-trial motor cortical activity recorded while monkeys performed center-out reaching. Using information theoretic techniques, we found that single units carry relatively little speed-related information compared with direction-related information. This result is not mitigated at the population level: simultaneously recorded population activity predicted speed with significantly lower accuracy relative to direction predictions. Furthermore, a unit-dropping analysis revealed that speed accuracy would likely remain lower than direction accuracy, even given larger populations. These results suggest that the instantaneous details of single-trial movement speed are difficult to extract using commonly assumed coding schemes. This apparent paucity of speed information takes particular importance in the context of brain-machine interfaces (BMIs), which rely on extracting kinematic information from motor cortex. Previous studies have highlighted subjects' difficulties in holding a BMI cursor stable at targets. These studies, along with our finding of relatively little speed information in motor cortex, inspired a speed-dampening Kalman filter (SDKF) that automatically slows the cursor upon detecting changes in decoded movement direction. Effectively, SDKF enhances speed control by using prevalent directional signals, rather than requiring speed to be directly decoded from neural activity. SDKF improved success rates by a factor of 1.7 relative to a standard Kalman filter in a closed-loop BMI task requiring stable stops at targets. BMI systems enabling stable stops will be more effective and user-friendly when translated into clinical applications.

Sensorimotor control engages cognitive processes such as prediction, learning, and multisensory integration. Understanding the neural mechanisms underlying these cognitive processes with arm reaching is challenging because we currently record only a fraction of the relevant neurons, the arm has nonlinear dynamics, and multiple modalities of sensory feedback contribute to control. A brain–computer interface (BCI) is a well-defined sensorimotor loop with key simplifying advantages that address each of these challenges, while engaging similar cognitive processes. As a result, BCI is becoming recognized as a powerful tool for basic scientific studies of sensorimotor control. Here, we describe the benefits of BCI for basic scientific inquiries and review recent BCI studies that have uncovered new insights into the neural mechanisms underlying sensorimotor control.

Millions of neurons drive the activity of hundreds of muscles, meaning many different neural population activity patterns could generate the same movement. Studies have suggested that these redundant (i.e. behaviorally equivalent) activity patterns may be beneficial for neural computation. However, it is unknown what constraints may limit the selection of different redundant activity patterns. We leveraged a brain-computer interface, allowing us to define precisely which neural activity patterns were redundant. Rhesus monkeys made cursor movements by modulating neural activity in primary motor cortex. We attempted to predict the observed distribution of redundant neural activity. Principles inspired by work on muscular redundancy did not accurately predict these distributions. Surprisingly, the distributions of redundant neural activity and task-relevant activity were coupled, which enabled accurate predictions of the distributions of redundant activity. This suggests limits on the extent to which redundancy may be exploited by the brain for computation.

Animals have a remarkable capacity to learn new motor skills, but it remains an open question as to how learning changes neural population dynamics underlying movement 1 . Specifically, we asked whether changes in neural population dynamics relate purely to newly learned movements or if additional patterns are generated that facilitate learning without matching motor output. We trained rhesus monkeys to learn a curl force field 2 task that elicited new arm-movement kinetics for some but not all reach directions 3,4 . We found that along certain neural dimensions, preparatory activity in motor cortex reassociated existing activity patterns with new movements. These systematic changes were observed only for learning-altered reaches. Surprisingly, we also found prominent shifts of preparatory activity along a nearly orthogonal neural dimension. These changes in preparatory activity were observed uniformly for all reaches including those unaltered by learning. This uniform shift during learning implies formation of new neural activity patterns, which was not observed in other short-term learning contexts [5][6][7][8] . During a washout period when the curl field was removed, movement kinetics gradually reverted, but the learning-induced uniform shift of preparatory activity persisted and a second, orthogonal uniform shift occurred. This persistent shift may retain a motor memory of the learned field 9-11 , consistent with faster relearning of the same curl field observed behaviorally and neurally. When multiple different curl fields were learned sequentially, we found distinct uniform shifts, each reflecting the identity of the field applied and potentially separating the associated motor memories 12,13 . The neural geometry of these shifts in preparatory activity could serve to organize skill-specific changes in movement production, facilitating the acquisition and retention of a broad motor repertoire..