Doctor of Philosophy, Carnegie Mellon University (2015)
Bachelor of Science, Stanford University, EE-BS (2009)
Master of Science, Stanford University, EE-MS (2009)
New neural activity patterns emerge with long-term learning.
Proceedings of the National Academy of Sciences of the United States of America
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.
View details for DOI 10.1073/pnas.1820296116
View details for PubMedID 31182595
Constraints on neural redundancy
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.
View details for PubMedID 30109848
Computation through Cortical Dynamics.
2018; 98 (5): 873–75
Population dynamics is emerging as a language for understanding high-dimensional neural recordings. Remington etal. (2018) explore how inputs to frontal cortex modulate neural dynamics in order to implement a computation of interest.
View details for PubMedID 29879388
Learning by neural reassociation
2018; 21 (4): 607-+
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.
View details for PubMedID 29531364
View details for PubMedCentralID PMC5876156
Brain-computer interfaces for dissecting cognitive processes underlying sensorimotor control
CURRENT OPINION IN NEUROBIOLOGY
2016; 37: 53–58
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.
View details for DOI 10.1016/j.conb.2015.12.005
View details for Web of Science ID 000376546300009
View details for PubMedID 26796293
View details for PubMedCentralID PMC4860084
Internal models for interpreting neural population activity during sensorimotor control
To successfully guide limb movements, the brain takes in sensory information about the limb, internally tracks the state of the limb, and produces appropriate motor commands. It is widely believed that this process uses an internal model, which describes our prior beliefs about how the limb responds to motor commands. Here, we leveraged a brain-machine interface (BMI) paradigm in rhesus monkeys and novel statistical analyses of neural population activity to gain insight into moment-by-moment internal model computations. We discovered that a mismatch between subjects' internal models and the actual BMI explains roughly 65% of movement errors, as well as long-standing deficiencies in BMI speed control. We then used the internal models to characterize how the neural population activity changes during BMI learning. More broadly, this work provides an approach for interpreting neural population activity in the context of how prior beliefs guide the transformation of sensory input to motor output.
View details for DOI 10.7554/elife.10015
View details for Web of Science ID 000373815700001
View details for PubMedID 26646183
View details for PubMedCentralID PMC4874779
Neural constraints on learning
2014; 512 (7515): 423-U428
Learning, whether motor, sensory or cognitive, requires networks of neurons to generate new activity patterns. As some behaviours are easier to learn than others, we asked if some neural activity patterns are easier to generate than others. Here we investigate whether an existing network constrains the patterns that a subset of its neurons is capable of exhibiting, and if so, what principles define this constraint. We employed a closed-loop intracortical brain-computer interface learning paradigm in which Rhesus macaques (Macaca mulatta) controlled a computer cursor by modulating neural activity patterns in the primary motor cortex. Using the brain-computer interface 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. The activity of a neural population can be represented in a high-dimensional space (termed the neural space), wherein each dimension corresponds to the activity of one neuron. These characteristic activity patterns comprise a low-dimensional subspace (termed the intrinsic manifold) within the neural space. The intrinsic manifold presumably reflects constraints imposed by the underlying neural circuitry. Here we show that the animals could readily learn to proficiently control the cursor using neural activity patterns that were within the intrinsic manifold. However, animals were less able to learn to proficiently control the cursor using activity patterns that were outside of the intrinsic manifold. These results suggest that the existing structure of a network can shape learning. On a timescale of hours, it seems 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 possess.
View details for DOI 10.1038/nature13665
View details for Web of Science ID 000340840600032
View details for PubMedID 25164754
Motor cortical control of movement speed with implications for brain-machine interface control
JOURNAL OF NEUROPHYSIOLOGY
2014; 112 (2): 411–29
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.
View details for DOI 10.1152/jn.00391.2013
View details for Web of Science ID 000339172500018
View details for PubMedID 24717350
View details for PubMedCentralID PMC4064402
Learning an Internal Dynamics Model from Control Demonstration.
JMLR workshop and conference proceedings
Much work in optimal control and inverse control has assumed that the controller has perfect knowledge of plant dynamics. However, if the controller is a human or animal subject, the subject's internal dynamics model may differ from the true plant dynamics. Here, we consider the problem of learning the subject's internal model from demonstrations of control and knowledge of task goals. Due to sensory feedback delay, the subject uses an internal model to generate an internal prediction of the current plant state, which may differ from the actual plant state. We develop a probabilistic framework and exact EM algorithm to jointly estimate the internal model, internal state trajectories, and feedback delay. We applied this framework to demonstrations by a nonhuman primate of brain-machine interface (BMI) control. We discovered that the subject's internal model deviated from the true BMI plant dynamics and provided significantly better explanation of the recorded neural control signals than did the true plant dynamics.
View details for PubMedID 24562322
View details for PubMedCentralID PMC3929129
Internal Models Engaged by Brain-computer Interface Control
IEEE. 2012: 1327–30
Internal models have been proposed to explain the brain's ability to compensate for sensory feedback delays by predicting the sensory consequences of movement commands. Single-neuron studies in the oculomotor and vestibulo-ocular systems have provided evidence of internal models, as have behavioral studies in the skeletomotor system. Here, we present evidence of internal models from simultaneously recorded population activity underlying closed-loop brain-computer interface (BCI) control. We studied cursor-based BCI control by a nonhuman primate implanted with a multi-electrode array in motor cortex. Using a novel BCI task, we measured the visual feedback processing delay to be about 130 milliseconds. By examining the task-based appropriateness of the population activity at different time lags, we found evidence that the subject compensates for the feedback delay by predicting upcoming cursor positions, suggesting the use of an internal forward model. Lastly, we examined the time course of internal model adaptation after altering the mapping between population activity and cursor movements. This study suggests that closed-loop BCI experiments combined with novel statistical analyses can provide insight into the neural substrates of feedback motor control and motor learning.
View details for Web of Science ID 000313296501146
View details for PubMedID 23366143
View details for PubMedCentralID PMC3772636