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Visual detection is a fundamental natural task. Detection becomes more challenging as the similarity between the target and the background in which it is embedded increases, a phenomenon termed 'similarity masking'. To test the hypothesis that V1 contributes to similarity masking, we used voltage sensitive dye imaging (VSDI) to measure V1 population responses while macaque monkeys performed a detection task under varying levels of target-background similarity. Paradoxically, we find that during an initial transient phase, V1 responses to the target are enhanced, rather than suppressed, by target-background similarity. This effect reverses in the second phase of the response, so that in this phase V1 signals are positively correlated with the behavioral effect of similarity. Finally, we show that a simple model with delayed divisive normalization can qualitatively account for our findings. Overall, our results support the hypothesis that a nonlinear gain control mechanism in V1 contributes to perceptual similarity masking.

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The brain's remarkable properties arise from the collective activity of millions of neurons. Widespread application of dimensionality reduction to multi-neuron recordings implies that neural dynamics can be approximated by low-dimensional "latent" signals reflecting neural computations. However, can such low-dimensional representations truly explain the vast range of brain activity, and if not, what is the appropriate resolution and scale of recording to capture them? Imaging neural activity at cellular resolution and near-simultaneously across the mouse cortex, we demonstrate an unbounded scaling of dimensionality with neuron number in populations up to 1 million neurons. Although half of the neural variance is contained within sixteen dimensions correlated with behavior, our discovered scaling of dimensionality corresponds to an ever-increasing number of neuronal ensembles without immediate behavioral or sensory correlates. The activity patterns underlying these higher dimensions are fine grained and cortex wide, highlighting that large-scale, cellular-resolution recording is required to uncover the full substrates of neuronal computations.

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While neurostimulation technologies are rapidly approaching clinical applications for sensorimotor disorders, the impact of electrical stimulation on network dynamics is still unknown. Given the high degree of shared processing in neural structures, it is critical to understand if neurostimulation affects functions that are related to, but not targeted by, the intervention. Here, we approach this question by studying the effects of electrical stimulation of cutaneous afferents on unrelated processing of proprioceptive inputs. We recorded intraspinal neural activity in four monkeys while generating proprioceptive inputs from the radial nerve. We then applied continuous stimulation to the radial nerve cutaneous branch and quantified the impact of the stimulation on spinal processing of proprioceptive inputs via neural population dynamics. Proprioceptive pulses consistently produce neural trajectories that are disrupted by concurrent cutaneous stimulation. This disruption propagates to the somatosensory cortex, suggesting that electrical stimulation can perturb natural information processing across the neural axis.

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The brain's remarkable properties arise from collective activity of millions of neurons. Widespread application of dimensionality reduction to multi-neuron recordings implies that neural dynamics can be approximated by low-dimensional "latent" signals reflecting neural computations. However, what would be the biological utility of such a redundant and metabolically costly encoding scheme and what is the appropriate resolution and scale of neural recording to understand brain function? Imaging the activity of one million neurons at cellular resolution and near-simultaneously across mouse cortex, we demonstrate an unbounded scaling of dimensionality with neuron number. While half of the neural variance lies within sixteen behavior-related dimensions, we find this unbounded scaling of dimensionality to correspond to an ever-increasing number of internal variables without immediate behavioral correlates. The activity patterns underlying these higher dimensions are fine-grained and cortex-wide, highlighting that large-scale recording is required to uncover the full neural substrates of internal and potentially cognitive processes.

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How do neural codes adjust to track time across a range of resolutions, from milliseconds to multi-seconds, as a function of the temporal frequency at which events occur? To address this question, we studied time-modulated cells in the striatum and the hippocampus, while macaques categorized three nested intervals within the sub-second or the supra-second range (up to 1, 2, 4, or 8 s), thereby modifying the temporal resolution needed to solve the task. Time-modulated cells carried more information for intervals with explicit timing demand, than for any other interval. The striatum, particularly the caudate, supported the most accurate temporal prediction throughout all time ranges. Strikingly, its temporal readout adjusted non-linearly to the time range, suggesting that the striatal resolution shifted from a precise millisecond to a coarse multi-second range as a function of demand. This is in line with monkey's behavioral latencies, which indicated that they tracked time until 2 s but employed a coarse categorization strategy for durations beyond. By contrast, the hippocampus discriminated only the beginning from the end of intervals, regardless of the range. We propose that the hippocampus may provide an overall poor signal marking an event's beginning, whereas the striatum optimizes neural resources to process time throughout an interval adapting to the ongoing timing necessity.

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Objective.The proliferation of multi-unit cortical recordings over the last two decades, especially in macaques and during motor-control tasks, has generated interest in neural 'population dynamics': the time evolution of neural activity across a group of neurons working together. A good model of these dynamics should be able to infer the activity of unobserved neurons within the same population and of the observed neurons at future times. Accordingly, Pandarinath and colleagues have introduced a benchmark to evaluate models on these two (and related) criteria: four data sets, each consisting of firing rates from a population of neurons, recorded from macaque cortex during movement-related tasks.Approach.Since this is a discriminative-learning task, we hypothesize that general-purpose architectures based on recurrent neural networks (RNNs) trained with masking can outperform more 'bespoke' models. To capture long-distance dependencies without sacrificing the autoregressive bias of recurrent networks, we also propose a novel, hybrid architecture ('TERN') that augments the RNN with self-attention, as in transformer networks.Main results.Our RNNs outperform all published models on all four data sets in the benchmark. The hybrid architecture improves performance further still. Pure transformer models fail to achieve this level of performance, either in our work or that of other groups.Significance.We argue that the autoregressive bias imposed by RNNs is critical for achieving the highest levels of performance, and establish the state of the art on the neural latents benchmark. We conclude, however, by proposing that the benchmark be augmented with an alternative evaluation of latent dynamics that favors generative over discriminative models like the ones we propose in this report.

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It has been proposed that the nervous system has the capacity to generate a wide variety of movements because it reuses some invariant code. Previous work has identified that dynamics of neural population activity are similar during different movements, where dynamics refer to how the instantaneous spatial pattern of population activity changes in time. Here, we test whether invariant dynamics of neural populations are actually used to issue the commands that direct movement. Using a brain-machine interface (BMI) that transforms rhesus macaques' motor-cortex activity into commands for a neuroprosthetic cursor, we discovered that the same command is issued with different neural-activity patterns in different movements. However, these different patterns were predictable, as we found that the transitions between activity patterns are governed by the same dynamics across movements. These invariant dynamics are low dimensional, and critically, they align with the BMI, so that they predict the specific component of neural activity that actually issues the next command. We introduce a model of optimal feedback control (OFC) that shows that invariant dynamics can help transform movement feedback into commands, reducing the input that the neural population needs to control movement. Altogether our results demonstrate that invariant dynamics drive commands to control a variety of movements and show how feedback can be integrated with invariant dynamics to issue generalizable commands.

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Neural population dynamics provide a key computational framework for understanding information processing in the sensory, cognitive, and motor functions of the brain. They systematically depict complex neural population activity, dominated by strong temporal dynamics as trajectory geometry in a low-dimensional neural space. However, neural population dynamics are poorly related to the conventional analytical framework of single-neuron activity, the rate-coding regime that analyzes firing rate modulations using task parameters. To link the rate-coding and dynamic models, we developed a variant of state-space analysis in the regression subspace, which describes the temporal structures of neural modulations using continuous and categorical task parameters. In macaque monkeys, using two neural population datasets containing either of two standard task parameters, continuous and categorical, we revealed that neural modulation structures are reliably captured by these task parameters in the regression subspace as trajectory geometry in a lower dimension. Furthermore, we combined the classical optimal-stimulus response analysis (usually used in rate-coding analysis) with the dynamic model and found that the most prominent modulation dynamics in the lower dimension were derived from these optimal responses. Using those analyses, we successfully extracted geometries for both task parameters that formed a straight geometry, suggesting that their functional relevance is characterized as a unidimensional feature in their neural modulation dynamics. Collectively, our approach bridges neural modulation in the rate-coding model and the dynamic system, and provides researchers with a significant advantage in exploring the temporal structure of neural modulations for pre-existing datasets.

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In addition to long-timescale rewiring, synapses in the brain are subject to significant modulation that occurs at faster timescales that endow the brain with additional means of processing information. Despite this, models of the brain like recurrent neural networks (RNNs) often have their weights frozen after training, relying on an internal state stored in neuronal activity to hold task-relevant information. In this work, we study the computational potential and resulting dynamics of a network that relies solely on synapse modulation during inference to process task-relevant information, the multi-plasticity network (MPN). Since the MPN has no recurrent connections, this allows us to study the computational capabilities and dynamical behavior contributed by synapses modulations alone. The generality of the MPN allows for our results to apply to synaptic modulation mechanisms ranging from short-term synaptic plasticity (STSP) to slower modulations such as spike-time dependent plasticity (STDP). We thoroughly examine the neural population dynamics of the MPN trained on integration-based tasks and compare it to known RNN dynamics, finding the two to have fundamentally different attractor structure. We find said differences in dynamics allow the MPN to outperform its RNN counterparts on several neuroscience-relevant tests. Training the MPN across a battery of neuroscience tasks, we find its computational capabilities in such settings is comparable to networks that compute with recurrent connections. Altogether, we believe this work demonstrates the computational possibilities of computing with synaptic modulations and highlights important motifs of these computations so that they can be identified in brain-like systems.

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How do patterns of neural activity in the motor cortex contribute to the planning of a movement? A recent theory developed for single movements proposes that the motor cortex acts as a dynamical system whose initial state is optimized during the preparatory phase of the movement. This theory makes important yet untested predictions about preparatory dynamics in more complex behavioral settings. Here, we analyze preparatory activity in non-human primates planning not one but two movements simultaneously. As predicted by the theory, we find that parallel planning is achieved by adjusting preparatory activity within an optimal subspace to an intermediate state reflecting a trade-off between the two movements. The theory quantitatively accounts for the relationship between this intermediate state and fluctuations in the animals' behavior down at the trial level. These results uncover a simple mechanism for planning multiple movements in parallel and further point to motor planning as a controlled dynamical process.

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Stellate ganglia within the intrathoracic cardiac control system receive and integrate central, peripheral, and cardiopulmonary information to produce postganglionic cardiac sympathetic inputs. Pathological anatomical and structural remodeling occurs within the neurons of the stellate ganglion (SG) in the setting of heart failure (HF). A large proportion of SG neurons function as interneurons whose networking capabilities are largely unknown. Current therapies are limited to targeting sympathetic activity at the cardiac level or surgical interventions such as stellectomy, to treat HF. Future therapies that target the SG will require understanding of their networking capabilities to modify any pathological remodeling. We observe SG networking by examining cofluctuation and specificity of SG networked activity to cardiac cycle phases. We investigate network processing of cardiopulmonary transduction by SG neuronal populations in porcine with chronic pacing-induced HF and control subjects during extended in-vivo extracellular microelectrode recordings. We find that information processing and cardiac control in chronic HF by the SG, relative to controls, exhibits: (i) more frequent, short-lived, high magnitude cofluctuations, (ii) greater variation in neural specificity to cardiac cycles, and (iii) neural network activity and cardiac control linkage that depends on disease state and cofluctuation magnitude.

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The theory of predictive processing posits that the brain computes expectations to process information predictively. Empirical evidence in support of this theory, however, is scarce and largely limited to sensory areas. Here, we report a precise and adaptive mechanism in the frontal cortex of non-human primates consistent with predictive processing of temporal events. We found that the speed of neural dynamics is precisely adjusted according to the average time of an expected stimulus. This speed adjustment, in turn, enables neurons to encode stimuli in terms of deviations from expectation. This lawful relationship was evident across multiple experiments and held true during learning: when temporal statistics underwent covert changes, neural responses underwent predictable changes that reflected the new mean. Together, these results highlight a precise mathematical relationship between temporal statistics in the environment and neural activity in the frontal cortex that may serve as a mechanism for predictive temporal processing.

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Across a range of motor and cognitive tasks, cortical activity can be accurately described by low-dimensional dynamics unfolding from specific initial conditions on every trial. These "preparatory states" largely determine the subsequent evolution of both neural activity and behavior, and their importance raises questions regarding how they are, or ought to be, set. Here, we formulate motor preparation as optimal anticipatory control of future movements and show that the solution requires a form of internal feedback control of cortical circuit dynamics. In contrast to a simple feedforward strategy, feedback control enables fast movement preparation by selectively controlling the cortical state in the small subspace that matters for the upcoming movement. Feedback but not feedforward control explains the orthogonality between preparatory and movement activity observed in reaching monkeys. We propose a circuit model in which optimal preparatory control is implemented as a thalamo-cortical loop gated by the basal ganglia.

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Computation of expected values (i.e., probability × magnitude) seems to be a dynamic integrative process performed by the brain for efficient economic behavior. However, neural dynamics underlying this computation is largely unknown. Using lottery tasks in monkeys (Macaca mulatta, male; Macaca fuscata, female), we examined (1) whether four core reward-related brain regions detect and integrate probability and magnitude cued by numerical symbols and (2) whether these brain regions have distinct dynamics in the integrative process. Extraction of the mechanistic structure of neural population signals demonstrated that expected value signals simultaneously arose in the central orbitofrontal cortex (cOFC; medial part of area 13) and ventral striatum (VS). Moreover, these signals were incredibly stable compared with weak and/or fluctuating signals in the dorsal striatum and medial OFC. Temporal dynamics of these stable expected value signals were unambiguously distinct: sharp and gradual signal evolutions in the cOFC and VS, respectively. These intimate dynamics suggest that the cOFC and VS compute the expected values with unique time constants, as distinct, partially overlapping processes.SIGNIFICANCE STATEMENT Our results differ from those of earlier studies suggesting that many reward-related regions in the brain signal probability and/or magnitude and provide a mechanistic structure for expected value computation employed in multiple neural populations. A central part of the orbitofrontal cortex (cOFC) and ventral striatum (VS) can simultaneously detect and integrate probability and magnitude into an expected value. Our empirical study on these neural population dynamics raises a possibility that the cOFC and VS cooperate on this computation with unique time constants as distinct, partially overlapping processes.

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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.

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Flexible behavior requires restraint of actions that are no longer appropriate. This behavioral inhibition critically relies on frontal cortex - basal ganglia circuits. Within the basal ganglia, the globus pallidus pars externa (GPe) has been hypothesized to mediate selective proactive inhibition: being prepared to stop a specific action, if needed. Here we investigate population dynamics of rat GPe neurons during preparation-to-stop, stopping, and going. Rats selectively engaged proactive inhibition towards specific actions, as shown by slowed reaction times (RTs). Under proactive inhibition, GPe population activity occupied state-space locations farther from the trajectory followed during normal movement initiation. Furthermore, the state-space locations were predictive of distinct types of errors: failures-to-stop, failures-to-go, and incorrect choices. Slowed RTs on correct proactive trials reflected starting bias towards the alternative action, which was overcome before progressing towards action initiation. Our results demonstrate that rats can exert cognitive control via strategic adjustments to their GPe network state.

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In the 1960s, Evarts first recorded the activity of single neurons in motor cortex of behaving monkeys (Evarts, 1968). In the 50 years since, great effort has been devoted to understanding how single neuron activity relates to movement. Yet these single neurons exist within a vast network, the nature of which has been largely inaccessible. With advances in recording technologies, algorithms, and computational power, the ability to study these networks is increasing exponentially. Recent experimental results suggest that the dynamical properties of these networks are critical to movement planning and execution. Here we discuss this dynamical systems perspective and how it is reshaping our understanding of the motor cortices. Following an overview of key studies in motor cortex, we discuss techniques to uncover the "latent factors" underlying observed neural population activity. Finally, we discuss efforts to use these factors to improve the performance of brain-machine interfaces, promising to make these findings broadly relevant to neuroengineering as well as systems neuroscience.

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