Path integration is essential for spatial navigation. Experimental studies have identified neural correlates for path integration, but exactly how the neural system accomplishes this computation remains unresolved. Here, we adopt recurrent neural networks (RNNs) trained to perform a path integration task to explore this issue. After training, we borrow neuroscience prior knowledge and methods to unfold the black box of the trained model, including: clarifying neuron types based on their receptive fields, dissecting information flows between neuron groups by pruning their connections, and analyzing internal dynamics of neuron groups using the attractor framework. Intriguingly, we uncover a hierarchical information processing pathway embedded in the RNN model, along which velocity information of an agent is first forwarded to band cells, band and grid cells then coordinate to carry out path integration, and finally grid cells output the agent location. Inspired by the RNN-based study, we construct a neural circuit model, in which band cells form one-dimensional (1D) continuous attractor neural networks (CANNs) and serve as upstream neurons to support downstream grid cells to carry out path integration in the 2D space. Our study challenges the conventional view of considering grid cells as the principal velocity integrator, and supports a neural circuit model with the hierarchy of band and grid cells.

Attractor neural networks consider that neural information is stored as stationary states of a dynamical system formed by a large number of interconnected neurons. The attractor property empowers a neural system to encode information robustly, but it also incurs the difficulty of rapid update of network states, which can impair information update and search in the brain. To overcome this difficulty, a solution is to include adaptation in the attractor network dynamics, whereby the adaptation serves as a slow negative feedback mechanism to destabilize what are otherwise permanently stable states. In such a way, the neural system can, on one hand, represent information reliably using attractor states, and on the other hand, perform computations wherever rapid state updating is involved. Previous studies have shown that continuous attractor neural networks with adaptation (A-CANNs) exhibit rich dynamical behaviors accounting for various brain functions. In this review, we present a comprehensive view of the rich diverse dynamics of A-CANNs. Moreover, we provide a unified mathematical framework to understand these different dynamical behaviors and briefly discuss their biological implications.

Hippocampal place cells of freely moving rodents display an intriguing temporal organization in their responses known as `theta phase precession', in which individual neurons fire at progressively earlier phases in successive theta cycles as the animal traverses the place fields. Recent experimental studies found that in addition to phase precession, many place cells also exhibit accompanied phase procession, but the underlying neural mechanism remains unclear. Here, we propose a neural circuit model to elucidate the generation of both kinds of phase shift in place cells' firing. Specifically, we consider a continuous attractor neural network (CANN) with feedback inhibition, which is inspired by the reciprocal interaction between the hippocampus and the medial septum. The feedback inhibition induces intrinsic mobility of the CANN which competes with the extrinsic mobility arising from the external drive. Their interplay generates an oscillatory tracking state, that is, the network bump state (resembling the decoded virtual position of the animal) sweeps back and forth around the external moving input (resembling the physical position of the animal). We show that this oscillatory tracking naturally explains the forward and backward sweeps of the decoded position during the animal's locomotion. At the single neuron level, the forward and backward sweeps account for, respectively, theta phase precession and procession. Furthermore, by tuning the feedback inhibition strength, we also explain the emergence of bimodal cells and unimodal cells, with the former having co-existed phase precession and procession, and the latter having only significant phase precession. We hope that this study facilitates our understanding of hippocampal temporal coding and lays foundation for unveiling their computational functions.

The brain performs probabilistic Bayesian inference to interpret the external world. The sampling-based view assumes that the brain represents the stimulus posterior distribution via samples of stochastic neuronal responses. Although the idea of sampling-based inference is appealing, it faces a critical challenge of whether stochastic sampling is fast enough to match the rapid computation of the brain. In this study, we explore how latent stimulus sampling can be accelerated in neural circuits. Specifically, we consider a canonical neural circuit model called continuous attractor neural networks (CANNs) and investigate how sampling-based inference of latent continuous variables is accelerated in CANNs. Intriguingly, we find that by including noisy adaptation in the neuronal dynamics, the CANN is able to speed up the sampling process significantly. We theoretically derive that the CANN with noisy adaptation implements the efficient sampling method called Hamiltonian dynamics with friction, where noisy adaption effectively plays the role of momentum. We theoretically analyze the sampling performances of the network and derive the condition when the acceleration has the maximum effect. Simulation results confirm our theoretical analyses. We further extend the model to coupled CANNs and demonstrate that noisy adaptation accelerates the sampling of the posterior distribution of multivariate stimuli. We hope that this study enhances our understanding of how Bayesian inference is realized in the brain.

Lévy flights describe a special class of random walks whose step sizes satisfy a power-law tailed distribution. As being an efficientsearching strategy in unknown environments, Lévy flights are widely observed in animal foraging behaviors. Recent studies further showed that human cognitive functions also exhibit the characteristics of Lévy flights. Despite being a general phenomenon, the neural mechanism at the circuit level for generating Lévy flights remains unresolved. Here, we investigate how Lévy flights can be achieved in attractor neural networks. To elucidate the underlying mechanism clearly, we first study continuous attractor neural networks (CANNs), and find that noisy neural adaptation, exemplified by spike frequency adaptation (SFA) in this work, can generate Lévy flights representing transitions of the network state in the attractor space. Specifically, the strength of SFA defines a travelling wave boundary, below which the network state displays local Brownian motion, and above which the network state displays long-jump motion. Noises in neural adaptation causes the network state to intermittently switch between these two motion modes, manifesting the characteristics of Lévy flights. We further extend the study to a general attractor neural network, and demonstrate that our model can explain the Lévy-flight phenomenon observed during free memory retrieval of humans. We hope that this study will give us insight into understanding the neural mechanism for optimal information processing in the brain.