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Animals readily execute learned behaviors in a consistent manner over long periods of time, and yet no equally stable neural correlate has been demonstrated. How does the cortex achieve this stable control? Using the sensorimotor system as a model of cortical processing, we investigated the hypothesis that the dynamics of neural latent activity, which captures the dominant co-variation patterns within the neural population, must be preserved across time. We recorded from populations of neurons in premotor, primary motor and somatosensory cortices as monkeys performed a reaching task, for up to 2 years. Intriguingly, despite a steady turnover in the recorded neurons, the low-dimensional latent dynamics remained stable. The stability allowed reliable decoding of behavioral features for the entire timespan, while fixed decoders based directly on the recorded neural activity degraded substantially. We posit that stable latent cortical dynamics within the manifold are the fundamental building blocks underlying consistent behavioral execution.Gallego, Perich et al. report that latent dynamics in the neural manifold across three cortical areas are stable throughout years of consistent behavior. The authors posit that these dynamics are fundamental building blocks of learned behavior.

Populations of cortical neurons flexibly perform different functions; for the primary motor cortex (M1) this means a rich repertoire of motor behaviors. We investigate the flexibility of M1 movement control by analyzing neural population activity during a variety of skilled wrist and reach-to-grasp tasks. We compare across tasks the neural modes that capture dominant neural covariance patterns during each task. While each task requires different patterns of muscle and single unit activity, we find unexpected similarities at the neural population level: the structure and activity of the neural modes is largely preserved across tasks. Furthermore, we find two sets of neural modes with task-independent activity that capture, respectively, generic temporal features of the set of tasks and a task-independent mapping onto muscle activity. This system of flexibly combined, well-preserved neural modes may underlie the ability of M1 to learn and generate a wide-ranging behavioral repertoire. Motor cortical neurons enable performance of a wide range of movements. Here, the authors report that dominant population activity patterns, the neural modes, are largely preserved across various tasks, with many displaying consistent temporal dynamics and reliably mapping onto muscle activity.

Animals use feedback to rapidly correct ongoing movements in the presence of a perturbation. Repeated exposure to a predictable perturbation leads to behavioural adaptation that compensates for its effects. Here, we tested the hypothesis that all the processes necessary for motor adaptation may emerge as properties of a controller that adaptively updates its policy. We trained a recurrent neural network to control its own output through an error-based feedback signal, which allowed it to rapidly counteract external perturbations. Implementing a biologically plausible plasticity rule based on this same feedback signal enabled the network to learn to compensate for persistent perturbations through a trial-by-trial process. The network activity changes during learning matched those from populations of neurons from monkey primary motor cortex — known to mediate both movement correction and motor adaptation — during the same task. Furthermore, our model natively reproduced several key aspects of behavioural studies in humans and monkeys. Thus, key features of trial-by-trial motor adaptation can arise from the internal properties of a recurrent neural circuit that adaptively controls its output based on ongoing feedback. How the brain adapts our movements to new conditions remains unclear. Here, the authors show that a recurrent neural network that controls its output using error-based feedback can learn to counteract a persistent perturbation using a biologically plausible plasticity rule, recapitulating key neural and behavioural features of motor adaptation.

Animals can quickly adapt learned movements to external perturbations, and their existing motor repertoire likely influences their ease of adaptation. Long-term learning causes lasting changes in neural connectivity, which shapes the activity patterns that can be produced during adaptation. Here, we examined how a neural population’s existing activity patterns, acquired through de novo learning, affect subsequent adaptation by modeling motor cortical neural population dynamics with recurrent neural networks. We trained networks on different motor repertoires comprising varying numbers of movements, which they acquired following various learning experiences. Networks with multiple movements had more constrained and robust dynamics, which were associated with more defined neural ‘structure’—organization in the available population activity patterns. This structure facilitated adaptation, but only when the changes imposed by the perturbation were congruent with the organization of the inputs and the structure in neural activity acquired during de novo learning. These results highlight trade-offs in skill acquisition and demonstrate how different learning experiences can shape the geometrical properties of neural population activity and subsequent adaptation. Using recurrent neural networks, here the authors show that learning the same task through different experiences can lead to important differences in how neural activity is structured. These differences can play a crucial role for subsequent adaptation, with networks that are equally good at the initial task showing opposing trends in adaptation.

Regaining arm control is a top priority for people with paralysis. Unfortunately, the complexity of the neural mechanisms underlying arm control has limited the effectiveness of neurotechnology approaches. Here, we exploited the neural function of surviving spinal circuits to restore voluntary arm and hand control in three monkeys with spinal cord injury, using spinal cord stimulation. Our neural interface leverages the functional organization of the dorsal roots to convey artificial excitation via electrical stimulation to relevant spinal segments at appropriate movement phases. Stimulation bursts targeting specific spinal segments produced sustained arm movements, enabling monkeys with arm paralysis to perform an unconstrained reach-and-grasp task. Stimulation specifically improved strength, task performances and movement quality. Electrophysiology suggested that residual descending inputs were necessary to produce coordinated movements. The efficacy and reliability of our approach hold realistic promises of clinical translation.This paper describes a neurotechnology that interacts with neural circuits in the spinal cord to restore arm and hand control after injury. With this implant, monkeys with paralysis recovered the ability to reach and grasp just a few days after injury.

Our bodies and the environment constrain our movements. For example, when our arm is fully outstretched, we cannot extend it further. More generally, the distribution of possible movements is conditioned on the state of our bodies in the environment, which is constantly changing. However, little is known about how the brain represents such distributions, and uses them in movement planning. Here, we record from dorsal premotor cortex (PMd) and primary motor cortex (M1) while monkeys reach to randomly placed targets. The hand’s position within the workspace creates probability distributions of possible upcoming targets, which affect movement trajectories and latencies. PMd, but not M1, neurons have increased activity when the monkey’s hand position makes it likely the upcoming movement will be in the neurons’ preferred directions. Across the population, PMd activity represents probability distributions of individual upcoming reaches, which depend on rapidly changing information about the body’s state in the environment. Movements are continually constrained by the current body position and its relation to the surroundings. Here the authors report that the population activity of monkey dorsal premotor cortex neurons dynamically represents the probability distribution of possible reach directions.

Animals rapidly adapt their movements to external perturbations, a process paralleled by changes in neural activity in the motor cortex. Experimental studies suggest that these changes originate from altered inputs (H input ) rather than from changes in local connectivity (H local ), as neural covariance is largely preserved during adaptation. Since measuring synaptic changes in vivo remains very challenging, we used a modular recurrent neural network to qualitatively test this interpretation. As expected, H input resulted in small activity changes and largely preserved covariance. Surprisingly given the presumed dependence of stable covariance on preserved circuit connectivity, H local led to only slightly larger changes in activity and covariance, still within the range of experimental recordings. This similarity is due to H local only requiring small, correlated connectivity changes for successful adaptation. Simulations of tasks that impose increasingly larger behavioural changes revealed a growing difference between H input and H local , which could be exploited when designing future experiments. How animals are able to rapidly adapt their behaviour to changing environmental demands remains poorly understood. Here, the authors use a modelling approach to show that synaptic plasticity in motor cortex may underlie rapid motor learning, demonstrating that small, correlated connectivity changes that preserve neural covariance are highly effective in driving behavioural adaptation.

The spiking activity of populations of cortical neurons is well described by the dynamics of a small number of population-wide covariance patterns, whose activation we refer to as ‘latent dynamics’. These latent dynamics are largely driven by the same correlated synaptic currents across the circuit that determine the generation of local field potentials (LFPs). Yet, the relationship between latent dynamics and LFPs remains largely unexplored. Here, we characterised this relationship for three different regions of primate sensorimotor cortex during reaching. The correlation between latent dynamics and LFPs was frequency-dependent and varied across regions. However, for any given region, this relationship remained stable throughout the behaviour: in each of primary motor and premotor cortices, the LFP-latent dynamics correlation profile was remarkably similar between movement planning and execution. These robust associations between LFPs and neural population latent dynamics help bridge the wealth of studies reporting neural correlates of behaviour using either type of recordings.

Prominent models of spike trains assume only one source of variability – stochastic (Poisson) spiking – when stimuli and behavior are fixed. However, spike trains may also reflect variability due to internal processes such as planning. For example, we can plan a movement at one point in time and execute it at some arbitrary later time. Neurons involved in planning may thus share an underlying time course that is not precisely locked to the actual movement. Here we combine the standard Linear-Nonlinear-Poisson (LNP) model with Dynamic Time Warping (DTW) to account for shared temporal variability. When applied to recordings from macaque premotor cortex, we find that time warping considerably improves predictions of neural activity. We suggest that such temporal variability is a widespread phenomenon in the brain which should be modeled.

The process by which the cerebral cortex generates movements to achieve different tasks remains poorly understood. Here, we leveraged the rich repertoire of well-controlled primate locomotor behaviors to study how task-specific movements are encoded across the dorsal premotor cortex (PMd), primary motor cortex (M1), and primary somatosensory cortex (S1) under naturalistic conditions. Neural population activity was confined within low-dimensional manifolds and partitioned into task-dependent and task-independent subspaces. However, the prevalence of these subspaces differed between cortical regions. PMd primarily operated within its task-dependent subspace, while S1, and to a lesser extent M1, largely evolved within their task-independent subspaces. The temporal structure of movement was encoded in the task-independent subspaces, which also dominated the PMd-to-M1 communication as the movement plans were translated into motor commands. Our results suggest that the brain utilizes different cortical regions to serialize the motor control by first performing task-specific computations in PMd to then generate task-independent commands in M1. How the cortex generates movement to achieve different tasks remains poorly understood. Here the authors show that the cortex serializes motor control by first performing task-specific computations in dorsal premotor cortex in order to then generate task-independent commands in primary motor cortex.