Navigating Cognition

 

Science  09 Nov 2018: Vol. 362, Issue 6415, p. 654

Navigating cognition: Spatial codes for human thinking

Jacob L. S. Bellmund, et.al.

Kavli Institute for Systems Neuroscience, Centre for Neural Computation, The Egil and Pauline Braathen and Fred Kavli Centre for Cortical Microcircuits, NTNU, Norwegian University of Science and Technology, Trondheim, Norway.

Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, Netherlands.

Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.

Department of Philosophy and Cognitive Science, Lund University, Lund, Sweden.

Centre for Artificial Intelligence, University of Technology Sydney, Sydney, Australia.

[paraphrase]

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.

This account builds on the capabilities of the hippocampus for associative binding to link event representations into relational networks and has offered a counterpole to an exclusively spatial-processing view of the hippocampus. Episodic memories can be formed by linking successive event representations and episodic trajectories into ensemble patterns stored in hippocampal networks for subsequent retrieval. Recent advances demonstrate a hippocampal involvement in flexible cognition beyond the domains of navigation and memory.

Space codes as a representational format for cognition

We describe domain-general core coding principles from spatial navigation research that have the potential to support a wider span of cognitive functions. Specifically, we propose that the hippocampal-entorhinal system represents experience in cognitive spaces. A cognitive space is thought to be spanned by a set of quality dimensions, which can be closely related to sensory inputs but also comprise abstract features. A given stimulus can be located in a cognitive space according to its set of feature values along a set of quality dimensions. Each dimension is equipped with an underlying metric and follows geometric constraints satisfying the mathematical notions of betweenness and equidistance.

From spatial navigation to cognitive spaces

In the mammalian brain, positional information is conveyed by the spatially constrained firing of place cells and grid cells during spatial navigation.    Place cells in the hippocampus are preferentially active when the animal occupies a certain position within the environment: the cell’s receptive field or place field. The firing fields of the population of place cells are thought to cover the entire environment, thereby providing a map-like representation of the animal’s surroundings. Although the firing of a place cell is usually restricted to one place in a small environment,    grid cells in the medial entorhinal cortex (EC), one synapse from the hippocampus, exhibit multiple firing fields located at the vertices of equilateral triangles    tiling the entire environment. These regular, six-fold symmetric firing patterns are assumed to support spatial navigation by providing a coordinate system of the environment. The entorhinal grid system is assigned a key role in path integration and vector navigation.

Intracranial recordings in patients navigating virtual reality environments established the existence of place cells and grid cells in humans. The six-fold symmetry of grid cell firing has been translated to noninvasive functional magnetic resonance imaging (fMRI) in healthy volunteers, where grid-like hexadirectional signals have been observed in the EC during navigation. The brain’s spatial navigation system further includes head direction cells conveying information about the animal’s head direction, goal and goal direction cells signaling egocentric directions to navigational goals, speed cells sensitive to running speed, and border or boundary vector cells responding to borders in the environment.

The firing of place and grid cells conveys positional information to navigate Euclidean space. We hypothesize that the spatially constrained firing of place cells and the metric provided by the entorhinal grid system might provide a domain-general mechanism to map dimensions of experience. In this framework, the activity of place cells can be conceived as indexing locations in a cognitive space    spanned by the entorhinal grid system. Three further neural coding mechanisms identified in spatial navigation studies illustrate how the hippocampal-entorhinal system may support a core mechanism of mapping cognitive spaces. First, the firing fields of place and grid cells    increase in size     along the dorsoventral axis of the rodent hippocampus in line with mapping of cognitive spaces at different levels of granularity for multiscale representations of knowledge hierarchies or nested conceptual information. Second, the ability of place cells to undergo global remapping allows the flexible formation of a multitude of uncorrelated maps for different cognitive spaces, which can be reinstated via attractor dynamics. Third, sequential activity of place cells and grid cells during replay and theta oscillations enables the simulation of trajectories through different locations in a cognitive space for adaptive cognition and behavior.

A continuous map of experience

The spatially constrained firing of place and grid cells provides a continuous code for the dimensions of space, in which neighboring positions have similar representations due to partially overlapping firing fields across the population of cells. We build on findings that the continuous code of spatially selective cells maps dimensions of experience beyond Euclidean space, which affords flexible cognition via the formation of cognitive spaces.

Unlike in rodents, the visual system has evolved to be the dominant source of sensory information in primates. During visual exploration of naturalistic images, neurons in the primate EC encode gaze position with six-fold symmetric firing patterns that are the hallmark of grid cell firing during navigation.

Next to its role in parsing sensory information, this spatial mapping mechanism might also encode a dimension inherent to all experience: time. During space-clamped running throughout a temporal delay, so-called time cells preferentially fire at specific time points. The populations of these time cells in the hippocampus and EC overlap substantially with the populations of place and grid cells, respectively, which suggests that cells in these regions might exhibit mixed selectivity for space and time.

Together, these findings suggest that the firing of functionally defined cell types in the hippocampal-entorhinal system prevails across task-relevant dimensions to map dimensions of experience in cognitive spaces. Stimuli are arranged in a spatial format where similarity between positions is reflected in the distance along the dimensions    spanning the cognitive space. The representation of cognitive spaces allows not only associative or transitive inference, accounted for via overlapping relational networks in the realm of relational memory theory, but also generalization and inference to novel stimuli and situations.

Flexible formation of stable cognitive spaces via remapping and attractor dynamics

The hippocampus has been shown to contribute to a variety of cognitive domains. If the hippocampal-entorhinal system maps multitudes of cognitive spaces, this system needs to exert remarkable flexibility in terms of the dimensions it can represent, as well as an ability to rapidly switch between cognitive spaces. This flexibility is demonstrated by the capacity of hippocampal place cells to undergo global remapping. These relationships are maintained not only between environmental contexts but also across behavioral states, with essentially identical cross-correlation patterns exhibited by populations of grid cells and other medial entorhinal cells during free foraging, slow-wave sleep (SWS), or rapid–eye movement (REM) sleep.

Remapping-like behavior of hippocampal cells has also been observed for time cells encoding temporal intervals during the delay of a memory-based discrimination task.

Conclusion

In this theoretical article, we propose cognitive spaces as a primary representational format for information processing in the brain. Combining key mechanisms identified in systems neuroscience and concepts from cognitive science and philosophy, we developed a cognitive neuroscience framework for processing and representing information in cognitive spaces in the hippocampal-entorhinal system.    Place and grid cells might have evolved to represent not only navigable space, but to also map dimensions of experience spanning cognitive spaces governed by geometric principles. In these cognitive spaces, stimuli can be located based on their values along the feature dimensions mapped by place and grid cells. These spatially specific cells provide a continuous code that allows similar stimuli to occupy neighboring positions in cognitive space, encoded by overlapping population responses. In this framework, concepts are represented by convex regions of similar stimuli. The multiscale spatial code along the long axis of the hippocampal formation enables representing stimuli at different granularities for both generalization and maintenance of fine details in hierarchical knowledge structures.    Ever-changing demands requiring the flexible mapping of different dimensions of relevance are met by the capacity of the hippocampus to remap to flexibly form cognitive spaces for which the low-dimensional entorhinal grid code might provide a stable metric. An established mapping of a cognitive space might be reinstated via attractor dynamics and pattern completion to provide stable representations of familiar dimensions. Experiencing a sequence of stimuli results in a trajectory through cognitive space. We propose that sequential hippocampal activity in the form of replay and theta sequences allows simulations of temporally compressed trajectories through cognitive spaces for flexible cognition and adaptive behavior. In sum, we suggest cognitive spaces as a domain-general format for human thinking, thus providing an overarching framework, which can also help to elucidate cognitive breakdown in neurodegenerative diseases and to inform novel architectures in artificial intelligence

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