Specific evidence of low-dimensional continuous attractor dynamics in grid cells
TL;DR: Results from novel environments suggest cell-cell structure is not inherited from hippocampal or external sensory inputs and substantiate the general hypothesis that the brain computes using low-dimensional continuous attractors.
Abstract: We examined simultaneously recorded spikes from multiple rat grid cells, to explain mechanisms underlying their activity. Among grid cells with similar spatial periods, the population activity was confined to lie close to a two-dimensional (2D) manifold: grid cells differed only along two dimensions of their responses and otherwise were nearly identical. Relationships between cell pairs were conserved despite extensive deformations of single-neuron responses. Results from novel environments suggest such structure is not inherited from hippocampal or external sensory inputs. Across conditions, cell-cell relationships are better conserved than responses of single cells. Finally, the system is continually subject to perturbations that, were the 2D manifold not attractive, would drive the system to inhabit a different region of state space than observed. These findings have strong implications for theories of grid-cell activity and substantiate the general hypothesis that the brain computes using low-dimensional continuous attractors.
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TL;DR: It is shown that removal of perineuronal nets leads to lower inhibitory spiking activity, and reduces grid cells’ ability to create stable representations of a novel environment, and that PNN removal in entorhinal cortex distorted spatial representations in downstream hippocampal neurons.
Abstract: Grid cells are part of a widespread network which supports navigation and spatial memory. Stable grid patterns appear late in development, in concert with extracellular matrix aggregates termed perineuronal nets (PNNs) that condense around inhibitory neurons. It has been suggested that PNNs stabilize synaptic connections and long-term memories, but their role in the grid cell network remains elusive. We show that removal of PNNs leads to lower inhibitory spiking activity, and reduces grid cells' ability to create stable representations of a novel environment. Furthermore, in animals with disrupted PNNs, exposure to a novel arena corrupted the spatiotemporal relationships within grid cell modules, and the stored representations of a familiar arena. Finally, we show that PNN removal in entorhinal cortex distorted spatial representations in downstream hippocampal neurons. Together this work suggests that PNNs provide a key stabilizing element for the grid cell network.
935 citations
TL;DR: It is argued that spatial-processing principles in the hippocampalentorhinal region provide a geometric code to map information domains of cognitive spaces for high-level cognition and discuss recent evidence for this proposal.
Abstract: The hippocampal formation has long been suggested to underlie both memory formation and spatial navigation. We discuss how neural mechanisms identified in spatial navigation research operate across information domains to support a wide spectrum of cognitive functions. In our framework, place and grid cell population codes provide a representational format to map variable dimensions of cognitive spaces. This highly dynamic mapping system enables rapid reorganization of codes through remapping between orthogonal representations across behavioral contexts, yielding a multitude of stable cognitive spaces at different resolutions and hierarchical levels. Action sequences result in trajectories through cognitive space, which can be simulated via sequential coding in the hippocampus. In this way, the spatial representational format of the hippocampal formation has the capacity to support flexible cognition and behavior.
360 citations
TL;DR: It is now possible to investigate how specialized cell types of hippocampal–entorhinal systems work together, and spatial mapping may become one of the first cognitive functions to be understood in mechanistic detail.
Abstract: Since the first place cell was recorded and the cognitive-map theory was subsequently formulated, investigation of spatial representation in the hippocampal formation has evolved in stages. Early studies sought to verify the spatial nature of place cell activity and determine its sensory origin. A new epoch started with the discovery of head direction cells and the realization of the importance of angular and linear movement-integration in generating spatial maps. A third epoch began when investigators turned their attention to the entorhinal cortex, which led to the discovery of grid cells and border cells. This review will show how ideas about integration of self-motion cues have shaped our understanding of spatial representation in hippocampal-entorhinal systems from the 1970s until today. It is now possible to investigate how specialized cell types of these systems work together, and spatial mapping may become one of the first cognitive functions to be understood in mechanistic detail.
344 citations
TL;DR: This Review uses grid cells in the medial entorhinal cortex as a gateway to understand network computation at a stage of cortical processing in which firing patterns are shaped not primarily by incoming sensory signals but to a large extent by the intrinsic properties of the local circuit.
Abstract: One of the grand challenges in neuroscience is to comprehend neural computation in the association cortices, the parts of the cortex that have shown the largest expansion and differentiation during mammalian evolution and that are thought to contribute profoundly to the emergence of advanced cognition in humans. In this Review, we use grid cells in the medial entorhinal cortex as a gateway to understand network computation at a stage of cortical processing in which firing patterns are shaped not primarily by incoming sensory signals but to a large extent by the intrinsic properties of the local circuit.
283 citations
TL;DR: It is argued that this factorized representation facilitates the generalization of a previously learned structure to new objects in the form of a code factorized into sequence position and sequence identity.
271 citations
Cites background from "Specific evidence of low-dimensiona..."
...Remapping experiments suggests that entorhinal cells encode structural knowledge explicitly—divorced from sensory representations—thereby enabling the same relational constraints to be applied to different sensory environments (Fyhn et al., 2007; Whittington et al., 2018; Yoon et al., 2013)....
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TL;DR: A model of a system having a large number of simple equivalent components, based on aspects of neurobiology but readily adapted to integrated circuits, produces a content-addressable memory which correctly yields an entire memory from any subpart of sufficient size.
Abstract: Computational properties of use of biological organisms or to the construction of computers can emerge as collective properties of systems having a large number of simple equivalent components (or neurons). The physical meaning of content-addressable memory is described by an appropriate phase space flow of the state of a system. A model of such a system is given, based on aspects of neurobiology but readily adapted to integrated circuits. The collective properties of this model produce a content-addressable memory which correctly yields an entire memory from any subpart of sufficient size. The algorithm for the time evolution of the state of the system is based on asynchronous parallel processing. Additional emergent collective properties include some capacity for generalization, familiarity recognition, categorization, error correction, and time sequence retention. The collective properties are only weakly sensitive to details of the modeling or the failure of individual devices.
16,652 citations
TL;DR: The dorsocaudal medial entorhinal cortex (dMEC) contains a directionally oriented, topographically organized neural map of the spatial environment, whose key unit is the ‘grid cell’, which is activated whenever the animal's position coincides with any vertex of a regular grid of equilateral triangles spanning the surface of the environment.
Abstract: The ability to find one's way depends on neural algorithms that integrate information about place, distance and direction, but the implementation of these operations in cortical microcircuits is poorly understood. Here we show that the dorsocaudal medial entorhinal cortex (dMEC) contains a directionally oriented, topographically organized neural map of the spatial environment. Its key unit is the 'grid cell', which is activated whenever the animal's position coincides with any vertex of a regular grid of equilateral triangles spanning the surface of the environment. Grids of neighbouring cells share a common orientation and spacing, but their vertex locations (their phases) differ. The spacing and size of individual fields increase from dorsal to ventral dMEC. The map is anchored to external landmarks, but persists in their absence, suggesting that grid cells may be part of a generalized, path-integration-based map of the spatial environment.
3,445 citations
TL;DR: It is demonstrated that rats can rapidly learn to locate an object that they can never see, hear, or smell provided it remains in a fixed spatial location relative to distal room cues.
2,496 citations
TL;DR: Parallel recording methods outlined here make possible the study of the dynamics of neuronal interactions during unique behavioral events, which suggests that new spatial information creates conditions in the hippocampal circuitry that are conducive to the synaptic modification presumed to be involved in learning.
Abstract: Ensemble recordings of 73 to 148 rat hippocampal neurons were used to predict accurately the animals' movement through their environment, which confirms that the hippocampus transmits an ensemble code for location. In a novel space, the ensemble code was initially less robust but improved rapidly with exploration. During this period, the activity of many inhibitory cells was suppressed, which suggests that new spatial information creates conditions in the hippocampal circuitry that are conducive to the synaptic modification presumed to be involved in learning. Development of a new population code for a novel environment did not substantially alter the code for a familiar one, which suggests that the interference between the two spatial representations was very small. The parallel recording methods outlined here make possible the study of the dynamics of neuronal interactions during unique behavioral events.
2,227 citations
TL;DR: Theoretical studies suggest that the medial entorhinal cortex might perform some of the essential underlying computations by means of a unique, periodic synaptic matrix that could be self-organized in early development through a simple, symmetry-breaking operation.
Abstract: The hippocampal formation can encode relative spatial location, without reference to external cues, by the integration of linear and angular self-motion (path integration). Theoretical studies, in conjunction with recent empirical discoveries, suggest that the medial entorhinal cortex (MEC) might perform some of the essential underlying computations by means of a unique, periodic synaptic matrix that could be self-organized in early development through a simple, symmetry-breaking operation. The scale at which space is represented increases systematically along the dorsoventral axis in both the hippocampus and the MEC, apparently because of systematic variation in the gain of a movement-speed signal. Convergence of spatially periodic input at multiple scales, from so-called grid cells in the entorhinal cortex, might result in non-periodic spatial firing patterns (place fields) in the hippocampus.
1,747 citations