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Batista, A. P.

Publications and source records attributed to Batista, A. P..

12 recordsLinked to original sources

Eyes on the prize: a neural basis of perceptual choking under pressure

Even professional athletes sometimes fail to perform when it matters most. This phenomenon, known as choking under pressure, has been observed in a variety of motor and cognitive tasks. Can inordinately large rewards influence even sensory processing, and if so, what might be its neural basis? To probe this, we studied rhesus monkeys performing a challenging color change detection task and recorded from populations of neurons in visual area V4. We found that monkeys underperformed when offered rare "jackpot" rewards and uncovered associated detrimental alterations in V4 population activity. These findings were consistent with misallocated spatial attention, providing a potential neural basis for perceptual choking under pressure.

neuroscience↗

Distinct neural modes carry information about grasp force and phase in the sensorimotor cortex

Humans perform a variety of complex hand movements to manipulate objects, requiring precise control of changing forces. Understanding the role of sensorimotor cortex and the cortical dynamics underlying these actions is crucial for developing interventions that restore dexterous hand function after injury or disease. In this study, two individuals with tetraplegia resulting from cervical spinal cord injury attempted a series of isometric grasps. Neural activity was recorded from the motor and somatosensory cortices using intracortical microelectrode arrays while participants attempted to exert a static force or to ramp force up and down. Despite their inability to execute movement, and with limited afferent input, the spiking activity in motor and somatosensory cortex was modulated with the task. Within the neural response we identified independent neural modes - distinct patterns of population-level neural activity - that were informative about both the timing and magnitude of the force. Moreover, distinct neural modes were observed during static and dynamic grasping conditions, suggesting independent control schemes for maintaining and changing forces. These modes were related to phases of the task, including the onset, offset, holding periods, as well as phases of increasing and decreasing force. These results will inform the design of intracortical brain-computer interface (iBCI) systems that can leverage these naturally occurring patterns of grasp and force control to restore dexterous hand function. Significance StatementRestoring dexterous hand function after injury remains a major challenge, partly due to an incomplete understanding of the cortical dynamics underlying grasping and force control. In this study, we investigated neural activity within the motor and somatosensory cortices of individuals with tetraplegia attempting to perform grasps to different target forces with varying temporal profiles. We identified distinct neural modes modulated during specific phases of grasp that encode force information throughout the task. These findings suggest that brain-computer interfaces could leverage these native neural modes to restore grasping and force modulation.

neuroscience↗

Reward influences movement vigor through multiple motor cortical mechanisms

The prospect of greater rewards often invigorates movements. What neural mechanisms support this increase of movement vigor for greater rewards? We had three rhesus monkeys perform reaching movements to targets worth different magnitudes of reward. We recorded neural population activity from primary motor and dorsal premotor cortex, brain areas at the output of cortical processing for voluntary movements, and asked how neural activity mediated the translation of reward into increased vigor. We identified features of neural activity during movement preparation, initiation, and execution that were both correlated with vigor and modulated by reward. We also found that the neural metrics that correlate with different aspects of movement vigor exhibit only limited correlation with one another, suggesting that there are multiple mechanisms through which reward modulates vigor. Finally, we note that the majority of rewards modulation of motor cortical activity cannot be accounted for by reward-mediated vigor differences in behavior, indicating that reward modulations within motor cortex may serve roles in addition to affecting vigor. Overall, our results provide insight into the neural mechanisms that link reward-driven motivation to the modulation of the details of movement.

neuroscience↗

A Generalist Intracortical Motor Decoder

Mapping the relationship between neural activity and motor behavior is a central aim of sensori-motor neuroscience and neurotechnology. While most progress to this end has relied on restricting complexity, the advent of foundation models instead proposes integrating a breadth of data as an alternate avenue for broadly advancing downstream modeling. We quantify this premise for motor decoding from intracortical microelectrode data, pretraining an autoregressive Transformer on 2000 hours of neural population spiking activity paired with diverse motor covariates from over 30 monkeys and humans. The resulting model is broadly useful, benefiting decoding on 8 downstream decoding tasks and generalizing to a variety of neural distribution shifts. However, we also highlight that scaling autoregressive Transformers seems unlikely to resolve limitations stemming from sensor variability and output stereotypy in neural datasets. Code: https://github.com/joel99/ndt3

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A posture subspace in primary motor cortex

To generate movements, the brain must combine information about movement goal and body posture. Motor cortex (M1) is a key node for the convergence of these information streams. How are posture and goal information organized within M1s activity to permit the flexible generation of movement commands? To answer this question, we recorded M1 activity while monkeys performed a variety of tasks with the forearm in a range of postures. We found that posture- and goal-related components of neural population activity were separable and resided in nearly orthogonal subspaces. The posture subspace was stable across tasks. Within each task, neural trajectories for each goal had similar shapes across postures. Our results reveal a simpler organization of posture information in M1 than previously recognized. The compartmentalization of posture and goal information might allow the two to be flexibly combined in the service of our broad repertoire of actions.

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A theory of brain-computer interface learning via low-dimensional control

A remarkable demonstration of the flexibility of mammalian motor systems is primates ability to learn to control brain-computer interfaces (BCIs). This constitutes a completely novel motor behavior, yet primates are capable of learning to control BCIs under a wide range of conditions. BCIs with carefully calibrated decoders, for example, can be learned with only minutes to hours of practice. With a few weeks of practice, even BCIs with randomly constructed decoders can be learned. What are the biological substrates of this learning process? Here, we develop a theory based on a re-aiming strategy, whereby learning operates within a low-dimensional subspace of task-relevant inputs driving the local population of recorded neurons. Through comprehensive numerical and formal analysis, we demonstrate that this theory can provide a unifying explanation for disparate phenomena previously reported in three different BCI learning tasks, and we derive a novel experimental prediction that we verify with previously published data. By explicitly modeling the underlying neural circuitry, the theory reveals an interpretation of these phenomena in terms of biological constraints on neural activity.

neuroscience↗

Dynamical constraints on neural population activity

The manner in which neural activity unfolds over time is thought to be central to sensory, motor, and cognitive functions in the brain. Network models have long posited that the brains computations involve time courses of activity that are shaped by the underlying network. A prediction from this view is that the activity time courses should be difficult to violate. We leveraged a brain-computer interface (BCI) to challenge monkeys to violate the naturally-occurring time courses of neural population activity that we observed in motor cortex. This included challenging animals to traverse the natural time course of neural activity in a time-reversed manner. Animals were unable to violate the natural time courses of neural activity when directly challenged to do so. These results provide empirical support for the view that activity time courses observed in the brain indeed reflect the underlying network-level computational mechanisms that they are believed to implement.

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Inferring control objectives in a virtual balancing task in humans and monkeys

Natural behaviors have redundancy, which implies that humans and animals can achieve their goals with different control objectives. Given only observations of behavior, is it possible to infer the control strategy that the subject is employing? This challenge is particularly acute in animal behavior because we cannot ask or instruct the subject to use a particular control strategy. This study presents a three-pronged approach to infer an animals control strategy from behavior. First, both humans and monkeys performed a virtual balancing task for which different control objectives could be utilized. Under matched experimental conditions, corresponding behaviors were observed in humans and monkeys. Second, a generative model was developed that represented two main control strategies to achieve the task goal. Model simulations were used to identify aspects of behavior that could distinguish which control objective was being used. Third, these behavioral signatures allowed us to infer the control objective used by human subjects who had been instructed to use one control objective or the other. Based on this validation, we could then infer strategies from animal subjects. Being able to positively identify a subjects control objective from behavior can provide a powerful tool to neurophysiologists as they seek the neural mechanisms of sensorimotor coordination. Impact statementA computational approach identifies control objectives in humans and monkeys to serve as basis for analysis of neural correlates of skillful manipulation.

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A neural basis of choking under pressure

Incentives tend to drive improvements in performance. But when incentives get too high, we can "choke under pressure" and underperform when it matters most. What neural processes might lead to choking under pressure? We studied Rhesus monkeys performing a challenging reaching task in which they underperform when an unusually large "jackpot" reward is at stake. We observed a collapse in neural information about upcoming movements for jackpot rewards: in the motor cortex, neural planning signals became less distinguishable for different reach directions when a jackpot reward was made available. We conclude that neural signals of reward and motor planning interact in the motor cortex in a manner that can explain why we choke under pressure. One-Sentence SummaryIn response to exceptionally large reward cues, animals can "choke under pressure", and this corresponds to a collapse in the neural information about upcoming movements.

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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 type--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.

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Learning alters neural activity to simultaneously support memory and action

How are we able to learn new behaviors without disrupting previously learned ones? To understand how the brain achieves this, we used a brain-computer interface (BCI) learning paradigm, which enables us to detect the presence of a memory of one behavior while performing another. We found that learning to use a new BCI map altered the neural activity that monkeys produced when they returned to using a familiar BCI map, in a way that was specific to the learning experience. That is, learning left a "memory trace." This memory trace co-existed with proficient performance under the familiar map, primarily by altering dimensions of neural activity that did not impact behavior. Such a memory trace could provide the neural underpinning for the joint learning of multiple motor behaviors without interference.

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Learning is shaped by abrupt changes in neural engagement

Internal states such as arousal, attention, and motivation are known to modulate brain-wide neural activity, but how these processes interact with learning is not well understood. During learning, the brain must modify the neural activity it produces to improve behavioral performance. How do internal states affect the evolution of this learning process? Using a brain-computer interface (BCI) learning paradigm in non-human primates, we identified large fluctuations in neural population activity in motor cortex (M1) indicative of arousal-like internal state changes. These fluctuations drove population activity along dimensions we term neural engagement axes. Neural engagement increased abruptly at the start of learning, and then gradually retreated. In a BCI, the causal relationship between neural activity and behavior is known. This allowed us to understand how these changes impacted behavioral performance for different task goals. We found that neural engagement interacted with learning, helping to explain why animals learned some task goals more quickly than others.

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