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Stimuli are represented in the brain by the collective population responses of sensory neurons, and an object presented under varying conditions gives rise to a collection of neural population responses called an ‘object manifold’. Changes in the object representation along a hierarchical sensory system are associated with changes in the geometry of those manifolds, and recent theoretical progress connects this geometry with ‘classification capacity’, a quantitative measure of the ability to support object classification. Deep neural networks trained on object classification tasks are a natural testbed for the applicability of this relation. We show how classification capacity improves along the hierarchies of deep neural networks with different architectures. We demonstrate that changes in the geometry of the associated object manifolds underlie this improved capacity, and shed light on the functional roles different levels in the hierarchy play to achieve it, through orchestrated reduction of manifolds’ radius, dimensionality and inter-manifold correlations. Neural activity space or manifold that represents object information changes across the layers of a deep neural network. Here the authors present a theoretical account of the relationship between the geometry of the manifolds and the classification capacity of the neural networks.

Populations of neurons display an extraordinary diversity in the behaviors they affect and display. Machine learning techniques have recently emerged that allow us to create networks of model neurons that display behaviors of similar complexity. Here we demonstrate the direct applicability of one such technique, the FORCE method, to spiking neural networks. We train these networks to mimic dynamical systems, classify inputs, and store discrete sequences that correspond to the notes of a song. Finally, we use FORCE training to create two biologically motivated model circuits. One is inspired by the zebra finch and successfully reproduces songbird singing. The second network is motivated by the hippocampus and is trained to store and replay a movie scene. FORCE trained networks reproduce behaviors comparable in complexity to their inspired circuits and yield information not easily obtainable with other techniques, such as behavioral responses to pharmacological manipulations and spike timing statistics. FORCE training is a . Here the authors implement FORCE training in models of spiking neuronal networks and demonstrate that these networks can be trained to exhibit different dynamic behaviours.

Neuroscientists today can measure activity from more neurons than ever before, and are facing the challenge of connecting these brain-wide neural recordings to computation and behavior. In the present review, we first describe emerging tools and technologies being used to probe large-scale brain activity and new approaches to characterize behavior in the context of such measurements. We next highlight insights obtained from large-scale neural recordings in diverse model systems, and argue that some of these pose a challenge to traditional theoretical frameworks. Finally, we elaborate on existing modeling frameworks to interpret these data, and argue that the interpretation of brain-wide neural recordings calls for new theoretical approaches that may depend on the desired level of understanding. These advances in both neural recordings and theory development will pave the way for critical advances in our understanding of the brain.Neuroscientists can measure activity from more neurons than ever before, garnering new insights and posing challenges to traditional theoretical frameworks. New frameworks may help researchers use these observations to shed light on brain function.

The authors use recent probabilistic theories of neural computation to argue that confidence and certainty are not identical concepts. They propose precise mathematical definitions for both of these concepts and discuss putative neural representations. When facing uncertainty, adaptive behavioral strategies demand that the brain performs probabilistic computations. In this probabilistic framework, the notion of certainty and confidence would appear to be closely related, so much so that it is tempting to conclude that these two concepts are one and the same. We argue that there are computational reasons to distinguish between these two concepts. Specifically, we propose that confidence should be defined as the probability that a decision or a proposition, overt or covert, is correct given the evidence, a critical quantity in complex sequential decisions. We suggest that the term certainty should be reserved to refer to the encoding of all other probability distributions over sensory and cognitive variables. We also discuss strategies for studying the neural codes for confidence and certainty and argue that clear definitions of neural codes are essential to understanding the relative contributions of various cortical areas to decision making.

Neural generative models can be used to learn complex probability distributions from data, to sample from them, and to produce probability density estimates. We propose a computational framework for developing neural generative models inspired by the theory of predictive processing in the brain. According to predictive processing theory, the neurons in the brain form a hierarchy in which neurons in one level form expectations about sensory inputs from another level. These neurons update their local models based on differences between their expectations and the observed signals. In a similar way, artificial neurons in our generative models predict what neighboring neurons will do, and adjust their parameters based on how well the predictions matched reality. In this work, we show that the neural generative models learned within our framework perform well in practice across several benchmark datasets and metrics and either remain competitive with or significantly outperform other generative models with similar functionality (such as the variational auto-encoder). Brain-inspired neural generative models can be designed to learn complex probability distributions from data. Here the authors propose a neural generative computational framework, inspired by the theory of predictive processing in the brain, that facilitates parallel computing for complex tasks.

Cognitive maps are mental representations of spatial and conceptual relationships in an environment, and are critical for flexible behavior. To form these abstract maps, the hippocampus has to learn to separate or merge aliased observations appropriately in different contexts in a manner that enables generalization and efficient planning. Here we propose a specific higher-order graph structure, clone-structured cognitive graph (CSCG), which forms clones of an observation for different contexts as a representation that addresses these problems. CSCGs can be learned efficiently using a probabilistic sequence model that is inherently robust to uncertainty. We show that CSCGs can explain a variety of cognitive map phenomena such as discovering spatial relations from aliased sensations, transitive inference between disjoint episodes, and formation of transferable schemas. Learning different clones for different contexts explains the emergence of splitter cells observed in maze navigation and event-specific responses in lap-running experiments. Moreover, learning and inference dynamics of CSCGs offer a coherent explanation for disparate place cell remapping phenomena. By lifting aliased observations into a hidden space, CSCGs reveal latent modularity useful for hierarchical abstraction and planning. Altogether, CSCG provides a simple unifying framework for understanding hippocampal function, and could be a pathway for forming relational abstractions in artificial intelligence. Higher-order sequence learning using a structured graph representation - clone-structured cognitive graphs (CSCG) – can explain how the hippocampus learns cognitive maps. CSCG provides novel explanations for transferable schemas and transitive inference in the hippocampus, and for how place cells, splitter cells, lap-cells and a variety of phenomena emerge from the same set of fundamental principles.

Neural activity exhibits complex dynamics related to various brain functions, internal states and behaviors. Understanding how neural dynamics explain specific measured behaviors requires dissociating behaviorally relevant and irrelevant dynamics, which is not achieved with current neural dynamic models as they are learned without considering behavior. We develop preferential subspace identification (PSID), which is an algorithm that models neural activity while dissociating and prioritizing its behaviorally relevant dynamics. Modeling data in two monkeys performing three-dimensional reach and grasp tasks, PSID revealed that the behaviorally relevant dynamics are significantly lower-dimensional than otherwise implied. Moreover, PSID discovered distinct rotational dynamics that were more predictive of behavior. Furthermore, PSID more accurately learned behaviorally relevant dynamics for each joint and recording channel. Finally, modeling data in two monkeys performing saccades demonstrated the generalization of PSID across behaviors, brain regions and neural signal types. PSID provides a general new tool to reveal behaviorally relevant neural dynamics that can otherwise go unnoticed. This work develops PSID, a dynamic modeling method to dissociate and prioritize neural dynamics relevant to a given behavior.

Resting-state network connectivity has been associated with a variety of cognitive abilities, yet it remains unclear how these connectivity properties might contribute to the neurocognitive computations underlying these abilities. We developed a new approach—information transfer mapping—to test the hypothesis that resting-state functional network topology describes the computational mappings between brain regions that carry cognitive task information. Here, we report that the transfer of diverse, task-rule information in distributed brain regions can be predicted based on estimated activity flow through resting-state network connections. Further, we find that these task-rule information transfers are coordinated by global hub regions within cognitive control networks. Activity flow over resting-state connections thus provides a large-scale network mechanism for cognitive task information transfer and global information coordination in the human brain, demonstrating the cognitive relevance of resting-state network topology. Resting-state functional connections have been associated with cognitive abilities but it is unclear how these connections contribute to cognition. Here Ito et al present a new approach, information transfer mapping, showing that task-relevant information can be predicted by estimated activity flow through resting-state networks.

What is the physiological basis of long-term memory? The prevailing view in Neuroscience attributes changes in synaptic efficacy to memory acquisition, implying that stable memories correspond to stable connectivity patterns. However, an increasing body of experimental evidence points to significant, activity-independent fluctuations in synaptic strengths. How memories can survive these fluctuations and the accompanying stabilizing homeostatic mechanisms is a fundamental open question. Here we explore the possibility of memory storage within a global component of network connectivity, while individual connections fluctuate. We find that homeostatic stabilization of fluctuations differentially affects different aspects of network connectivity. Specifically, memories stored as time-varying attractors of neural dynamics are more resilient to erosion than fixed-points. Such dynamic attractors can be learned by biologically plausible learning-rules and support associative retrieval. Our results suggest a link between the properties of learning-rules and those of network-level memory representations, and point at experimentally measurable signatures. How are stable memories maintained in the brain despite significant ongoing fluctuations in synaptic strengths? Here, the authors show that a model consistent with fluctuations, homeostasis and biologically plausible learning rules, naturally leads to memories implemented as dynamic attractors.

During learning, the brain modifies synapses to improve behaviour. In the cortex, synapses are embedded within multilayered networks, making it difficult to determine the effect of an individual synaptic modification on the behaviour of the system. The backpropagation algorithm solves this problem in deep artificial neural networks, but historically it has been viewed as biologically problematic. Nonetheless, recent developments in neuroscience and the successes of artificial neural networks have reinvigorated interest in whether backpropagation offers insights for understanding learning in the cortex. The backpropagation algorithm learns quickly by computing synaptic updates using feedback connections to deliver error signals. Although feedback connections are ubiquitous in the cortex, it is difficult to see how they could deliver the error signals required by strict formulations of backpropagation. Here we build on past and recent developments to argue that feedback connections may instead induce neural activities whose differences can be used to locally approximate these signals and hence drive effective learning in deep networks in the brain.The backpropagation of error (backprop) algorithm is frequently used to train deep neural networks in machine learning, but it has not been viewed as being implemented by the brain. In this Perspective, however, Lillicrap and colleagues argue that the key principles underlying backprop may indeed have a role in brain function.