While rats offer a unique opportunity to study social behavior in a well-characterized and tractable model system, most descriptions tend to be subjective, anecdotal, or derived from a narrow set of behavioral assays. Extending a recently developed 3D tracking method to multiple animals (social-DANNCE), we provide an unbiased and quantitative description of social interactions in rats and pinpoint social deficits in rat models of autism spectrum disorder (ASD).
Neuroscience has long been an essential driver of progress in artificial intelligence (AI). We propose that to accelerate progress in AI, we must invest in fundamental research in NeuroAI. A core component of this is the embodied Turing test, which challenges AI animal models to interact with the sensorimotor world at skill levels akin to their living counterparts. The embodied Turing test shifts the focus from those capabilities like game playing and language that are especially well-developed or uniquely human to those capabilities – inherited from over 500 million years of evolution – that are shared with all animals. Building models that can pass the embodied Turing test will provide a roadmap for the next generation of AI.
The ability to sequence movements in response to new task demands enables rich and adaptive behavior. However, such flexibility is computationally costly and can result in halting performances. Practicing the same motor sequence repeatedly can render its execution precise, fast and effortless, that is, ‘automatic’. The basal ganglia are thought to underlie both types of sequence execution, yet whether and how their contributions differ is unclear. We parse this in rats trained to perform the same motor sequence instructed by cues and in a self-initiated overtrained, or ‘automatic,’ condition. Neural recordings in the sensorimotor striatum revealed a kinematic code independent of the execution mode. Although lesions reduced the movement speed and affected detailed kinematics similarly, they disrupted high-level sequence structure for automatic, but not visually guided, behaviors. These results suggest that the basal ganglia are essential for ‘automatic’ motor skills that are defined in terms of continuous kinematics, but can be dispensable for discrete motor sequences guided by sensory cues.
How motor cortex contributes to motor sequence execution is much debated, with studies supporting disparate views. Here we probe the degree to which motor cortex’s engagement depends on task demands, specifically whether its role differs for highly practiced, or ‘automatic’, sequences versus flexible sequences informed by external events. To test this, we trained rats to generate three-element motor sequences either by overtraining them on a single sequence or by having them follow instructive visual cues. Lesioning motor cortex revealed that it is necessary for flexible cue-driven motor sequences but dispensable for single automatic behaviors trained in isolation. However, when an automatic motor sequence was practiced alongside the flexible task, it became motor cortex-dependent, suggesting that subcortical consolidation of an automatic motor sequence is delayed or prevented when the same sequence is produced also in a flexible context. A simple neural network model recapitulated these results and explained the underlying circuit mechanisms. Our results critically delineate the role of motor cortex in motor sequence execution, describing the condition under which it is engaged and the functions it fulfills, thus reconciling seemingly conflicting views about motor cortex’s role in motor sequence generation.
The sensorimotor arm of the basal ganglia is a major part of the mammalian motor control network, yet whether it is essential for generating natural behaviors or specialized for learning and controlling motor skills is unclear. We examine this by contrasting contributions of the sensorimotor striatum (rodent dorsolateral striatum, DLS) to spontaneously expressed species-typical behaviors versus those adapted for a task. In stark contrast to earlier work implicating DLS in the control of acquired skills, bilateral lesions had no discernable effects on the expression or detailed kinematics of species-typical behaviors, such as grooming, rearing, or walking. To probe the neural correlates underlying this dissociation, we compared DLS activity across the behavioral domains. While neural activity reflected the kinematics of both learned and species-typical behaviors, the coding schemes were very different. Taken together, we did not find evidence for the basal ganglia circuit being required for species-typical behaviors; rather, our results suggest that it monitors ongoing movement and learns to alter its output to shape skilled behaviors in adaptive and task-specific ways.
How an established behavior is retained and consistently produced by a nervous system in constant flux remains a mystery. One possible solution to ensure long-term stability in motor output is to fix the activity patterns of single neurons in the relevant circuits. Alternatively, activity in single cells could drift over time provided that the population dynamics are constrained to produce the same behavior. To arbitrate between these possibilities, we recorded single-unit activity in motor cortex and striatum continuously for several weeks as rats performed stereotyped motor behaviors—both learned and innate. We found long-term stability in single neuron activity patterns across both brain regions. A small amount of drift in neural activity, observed over weeks of recording, could be explained by concomitant changes in task-irrelevant aspects of the behavior. These results suggest that long-term stable behaviors are …
Neuroscience has long been an important driver of progress in artificial intelligence (AI). We propose that to accelerate progress in AI, we must invest in fundamental research in NeuroAI.
As the old adage goes: practice makes perfect. Yet, the neural mechanisms by which rote repetition transforms a halting behavior into a fluid, effortless, and “automatic” action are not well understood. Here we consider the possibility that well-practiced motor sequences, which initially rely on higher-level decision-making circuits, become wholly specified in lower-level control circuits. We review studies informing this idea, discuss the constraints on such shift in control, and suggest approaches to pinpoint circuit-level changes associated with motor sequence learning.
Social interaction is a core component of animal behavior, and the tracking and quantification of spontaneous social behavior presents several challenges in both computer vision and interpretation. We extend a recently developed technique for 3D kinematic tracking of single animals (DANNCE) to capture the 3D poses of freely interacting animals by tracking animal identity and refining keypoint labeling networks to maintain accuracy during touching and occlusion. Using this approach, we have acquired a rich dataset of interactions across pairings from autism spectrum disorder (ASD) knockout rats and their normal counterparts. We use a dynamical embedding approach to parse animal movement throughout solitary and social contexts to find behaviors or 'gestures' which are preferentially expressed in the social context, and timestamp periods of behavioral synchronization during interaction. We find that social exchanges differ between ASD and control animals, and preliminary analysis of these interactions in the Cntnap2 rat model suggests that epochs of synchronized behaviors are dominated by aggressive behaviors in ASD pairs and more canonical play-fighting behavior in wild type animals.
The ability to sequence movements in response to new task demands enables rich and adaptive behavior. Such flexibility, however, is computationally costly and can result in halting performances. Practicing the same motor sequence repeatedly can render its execution precise, fast, and effortless, i.e., 'automatic'. The basal ganglia are thought to underlie both modes of sequence execution, yet whether and how their contributions differ is unclear. We parse this in rats trained to perform the same motor sequence in response to cues and in an overtrained, or 'automatic', condition. Neural recordings in the sensorimotor striatum revealed a kinematic code independent of execution mode. While lesions affected the detailed kinematics similarly across modes, they disrupted high-level sequence structure for automatic, but not visually-guided, behaviors. These results suggest that the basal ganglia contribute to learned movement kinematics and are essential for 'automatic' motor skills but can be dispensable for sensory-guided motor sequences.
The acquisition and execution of motor skills are mediated by a distributed motor network, spanning cortical and subcortical brain areas. The sensorimotor striatum is an important cog in this network, yet the roles of its two main inputs, from motor cortex and thalamus, remain largely unknown. To address this, we silenced the inputs in rats trained on a task that results in highly stereotyped and idiosyncratic movement patterns. While striatal-projecting motor cortex neurons were critical for learning these skills, silencing this pathway after learning had no effect on performance. In contrast, silencing striatal-projecting thalamus neurons disrupted the execution of the learned skills, causing rats to revert to species-typical pressing behaviors and preventing them from relearning the task. These results show distinct roles for motor cortex and thalamus in the learning and execution of motor skills and suggest that their interaction in the striatum underlies experience-dependent changes in subcortical motor circuits.
Understanding the biological basis of social and collective behaviors in animals is a key goal of the life sciences, and may yield important insights for engineering intelligent multi-agent systems. A critical step in understanding the mechanisms underlying social behaviors is a precise readout of the full 3D pose of interacting animals. While approaches for multi-animal pose estimation are beginning to emerge, they remain challenging to compare due to the lack of standardized benchmark datasets for multi-animal 3D pose estimation. Here we introduce the PAIR-R24M (Paired Acquisition of Interacting Rats) dataset for multi-animal 3D pose estimation, which contains 21.5 million frames of RGB video and 3D ground-truth motion capture of dyadic interactions in laboratory rats. PAIR-R24M contains data from 18 distinct pairs of rats across diverse behaviors, from 30 different viewpoints. The data are temporally contiguous and annotated with 11 behavioral categories, and 3 interaction behavioral categories, using a multi-animal extension of a recently developed behavioral segmentation approach. We used a novel multi-animal version of the recently published DANNCE network to establish a strong baseline for multi-animal 3D pose estimation without motion capture. These recordings are of sufficient resolution to allow us to examine cross-pair differences in social interactions, and identify different conserved patterns of social interaction across rats.
The basal ganglia are known to influence action selection and modulation of movement vigor, but whether and how they contribute to specifying the kinematics of learned motor skills is not understood. Here, we probe this question by recording and manipulating basal ganglia activity in rats trained to generate complex task-specific movement patterns with rich kinematic structure. We find that the sensorimotor arm of the basal ganglia circuit is crucial for generating the detailed movement patterns underlying the acquired motor skills. Furthermore, the neural representations in the striatum, and the control function they subserve, do not depend on inputs from the motor cortex. Taken together, these results extend our understanding of the basal ganglia by showing that they can specify and control the fine-grained details of learned motor skills through their interactions with lower-level motor circuits.
Comprehensive descriptions of animal behavior require precise three-dimensional (3D) measurements of whole-body movements. Although two-dimensional approaches can track visible landmarks in restrictive environments, performance drops in freely moving animals, due to occlusions and appearance changes. Therefore, we designed DANNCE to robustly track anatomical landmarks in 3D across species and behaviors. DANNCE uses projective geometry to construct inputs to a convolutional neural network that leverages learned 3D geometric reasoning. We trained and benchmarked DANNCE using a dataset of nearly seven million frames that relates color videos and rodent 3D poses. In rats and mice, DANNCE robustly tracked dozens of landmarks on the head, trunk, and limbs of freely moving animals in naturalistic settings. We extended DANNCE to datasets from rat pups, marmosets, and chickadees, and demonstrate quantitative profiling of behavioral lineage during development.
Animal pose estimation from video data is an important step in many biological studies, but current methods struggle in complex environments where occlusions are common and training data is scarce. Recent work has demonstrated improved accuracy with deep neural networks, but these methods often do not incorporate prior distributions that could improve localization. Here we present GIMBAL: a hierarchical von Mises-Fisher-Gaussian model that improves upon deep networks’ estimates by leveraging spatiotemporal constraints. The spatial constraints come from the animal’s skeleton, which induces a curved manifold of keypoint configurations. The temporal constraints come from the postural dynamics, which govern how angles between keypoints change over time. Importantly, the conditional conjugacy of the model permits simple and efficient Bayesian inference algorithms. We assess the model on a unique experimental dataset with video of a freely-behaving rodent from multiple viewpoints and ground-truth motion capture data for 20 keypoints. GIMBAL extends existing techniques, and in doing so offers more accurate estimates of keypoint positions, especially in challenging contexts.
In mammalian animal models, high-resolution kinematic tracking is restricted to brief sessions in constrained environments, limiting our ability to probe naturalistic behaviors and their neural underpinnings. To address this, we developed CAPTURE (Continuous Appendicular and Postural Tracking Using Retroreflector Embedding), a behavioral monitoring system that combines motion capture and deep learning to continuously track the 3D kinematics of a rat’s head, trunk, and limbs for week-long timescales in freely behaving animals. CAPTURE realizes 10- to 100-fold gains in precision and robustness compared with existing convolutional network approaches to behavioral tracking. We demonstrate CAPTURE’s ability to comprehensively profile the kinematics and sequential organization of natural rodent behavior, its variation across individuals, and its perturbation by drugs and disease, including identifying perseverative grooming states in a rat model of fragile X syndrome. CAPTURE significantly expands the range of behaviors and contexts that can be quantitatively investigated, opening the door to a new understanding of natural behavior and its neural basis.
To generate adaptive behaviors, animals must learn from their interactions with the environment. Describing the algorithms that govern this learning process and how they are implemented in the brain is a major goal of neuroscience. Careful and controlled observations of animal learning by Thorndike, Pavlov and others, now more than a century ago, identified intuitive rules by which animals (including humans) can learn from their experiences by associating sensory stimuli and motor actions with rewards. But going from explaining learning in simple paradigms to deciphering how complex problems are solved in rich and dynamic environments has proven difficult (Figure 1). Recently, this effort has received help from computer scientists and engineers hoping to emulate intelligent adaptive behaviors in machines. Inspired by the animal behavior literature, pioneers in artificial intelligence developed a rigorous and mathematically principled framework within which reward-based learning can be formalized and studied. Not only has the field of reinforcement learning become a boon to machine learning and artificial intelligence, it has also provided a theoretical foundation for biologists interested in deciphering how the brain implements reinforcement learning algorithms. The ability of reinforcement learning agents to solve complex, high-dimensional learning problems has been dramatically enhanced by using deep neural networks (deep reinforcement learning, Figure 1). Indeed, aided by ever-increasing computational resources, deep reinforcement learning algorithms can now outperform human experts on a host of well-defined complex tasks …
Though the temporal precision of neural computation has been studied intensively, a data-driven determination of this precision remains a fundamental challenge. Reproducible spike patterns may be obscured on single trials by uncontrolled temporal variability in behavior and cognition and may not be time locked to measurable signatures in behavior or local field potentials (LFP). To overcome these challenges, we describe a general-purpose time warping framework that reveals precise spike-time patterns in an unsupervised manner, even when these patterns are decoupled from behavior or are temporally stretched across single trials. We demonstrate this method across diverse systems: cued reaching in nonhuman primates, motor sequence production in rats, and olfaction in mice. This approach flexibly uncovers diverse dynamical firing patterns, including pulsatile responses to behavioral events, LFP-aligned oscillatory spiking, and even unanticipated patterns, such as 7 Hz oscillations in rat motor cortex that are not time locked to measured behaviors or LFP.
Parallel developments in neuroscience and deep learning have led to mutually productive exchanges, pushing our understanding of real and artificial neural networks in sensory and cognitive systems. However, this interaction between fields is less developed in the study of motor control. In this work, we develop a virtual rodent as a platform for the grounded study of motor activity in artificial models of embodied control. We then use this platform to study motor activity across contexts by training a model to solve four complex tasks. Using methods familiar to neuroscientists, we describe the behavioral representations and algorithms employed by different layers of the network using a neuroethological approach to characterize motor activity relative to the rodent's behavior and goals. We find that the model uses two classes of representations which respectively encode the task-specific behavioral strategies and task-invariant behavioral kinematics. These representations are reflected in the sequential activity and population dynamics of neural subpopulations. Overall, the virtual rodent facilitates grounded collaborations between deep reinforcement learning and motor neuroscience.
Trial-to-trial movement variability can both drive motor learning and interfere with expert performance, suggesting benefits of regulating it in context-specific ways. Here we address whether and how the brain regulates motor variability as a function of performance by training rats to execute ballistic forelimb movements for reward. Behavioral datasets comprising millions of trials revealed that motor variability is regulated by two distinct processes. A fast process modulates variability as a function of recent trial outcomes, increasing it when performance is poor and vice versa. A slower process tunes the gain of the fast process based on the uncertainty in the task's reward landscape. Simulations demonstrated that this regulation strategy optimizes reward accumulation over a wide range of time horizons, while also promoting learning. Our results uncover a sophisticated algorithm implemented by the brain to adaptively regulate motor variability to improve task performance. VIDEO ABSTRACT.
