Robin Hayman

Specific evidence of low-dimensional continuous attractor dynamics in grid cells

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.

Context-specific acquisition of location discrimination by hippocampal place cells.

The spatially localized firing of rodent hippocampal place cells is strongly determined by the local geometry of the environment. Over time, however, the cells can acquire additional inputs, including inputs from more distal cues. This is manifest as a change in firing pattern (‘remapping’) when the new inputs are manipulated. Place cells also reorganize their firing in response to non‐geometric changes in ‘context’, such as a change in the colour or odour of the environment. The present study investigated whether the new inputs acquired by place cells in one context were still available to the cells when they expressed their altered firing patterns in a new context. We found that the acquired information did not transfer to the new context, suggesting that the context inputs and the acquired inputs must interact somewhere upstream of the place cells themselves. We present a model of one possible such interaction, and of how such an interaction could be modified by experience in a Hebbian manner, thus explaining the context specificity of the new learning.

How Heterogeneous Place Cell Responding Arises From Homogeneous Grids—A Contextual Gating Hypothesis

How entorhinal grids generate hippocampal place fields remains unknown. The simplest hypothesis—that grids of different scales are added together—cannot explain a number of place field phenomena, such as (1) Summed grids form a repeating, dispersed activation pattern whereas place fields are focal and nonrepeating; (2) Grid cells are active in all environments but place cells only in some, and (3) Partial environmental changes cause either heterogeneous (“partial”) remapping in place cells whereas they result in all‐or‐nothing “realignment” remapping in grid cells. We propose that this dissociation between grid cell and place cell behavior arises in the entorhinal‐dentate projection. By our view, the grid‐cell/place‐cell projection is modulated by context, both organizationally and activationally. Organizationally, we propose that when the animal first enters a new environment, the relatively homogeneous input from the grid cells becomes spatially clustered by Hebbian processes in the dendritic tree so that inputs active in the same context and having overlapping fields come to terminate on the same sub‐branches of the tree. Activationally, when the animal re‐enters the now‐familiar environment, active contextual inputs select (by virtue of their clustered terminations) which parts of the dendritic tree, and therefore which grid cells, drive the granule cell. Assuming this pattern of projections, our model successfully produces focal hippocampal place fields that remap appropriately to contextual changes.

Place Field Repetition and Purely Local Remapping in a Multicompartment Environment

Hippocampal place cells support spatial memory using sensory information from the environment and self-motion information to localize their firing fields. Currently, there is disagreement about whether CA1 place cells can use pure self-motion information to disambiguate different compartments in environments containing multiple visually identical compartments. Some studies report that place cells can disambiguate different compartments, while others report that they do not. Furthermore, while numerous studies have examined remapping, there has been little examination of remapping in different subregions of a single environment. Is remapping purely local or do place fields in neighboring, unaffected, regions detect the change? We recorded place cells as rats foraged across a 4-compartment environment and report 3 new findings. First, we find that, unlike studies in which rats foraged in 2 compartments, place fields showed a high degree of spatial repetition with a slight degree of rate-based discrimination. Second, this repetition does not diminish with extended experience. Third, remapping was found to be purely local for both geometric change and contextual change. Our results reveal the limited capacity of the path integrator to drive pattern separation in hippocampal representations, and suggest that doorways may play a privileged role in segmenting the neural representation of space.

Horizontal biases in rats' use of three-dimensional space

Highlights ► Rat spatial behaviour was compared between horizontal and vertical dimensions. ► In both foraging and detour tasks, rats preferred horizontal over vertical movements. ► Rats also preferred routes where the horizontal leg occurred first rather than last. ► A horizontal bias is energetically adaptive and may reflect a parallel encoding bias. ► The preference for horizontal-first routes may reflect temporal effort discounting.

Geometric Cues Influence Head Direction Cells Only Weakly in Nondisoriented Rats

The influential hypothesis that environmental geometry is critical for spatial orientation has been extensively tested behaviorally, and yet findings have been conflicting. Head direction (HD) cells, the neural correlate of the sense of direction, offer a window into the processes underlying directional orientation and may help clarify the issue. In the present study, HD cells were recorded as rats foraged in enclosures of varying geometry, with or without simultaneous manipulation of landmarks and self-motion cues (path integration). All geometric enclosures had single-order rotational symmetry and thus completely polarized the environment. They also had unique features, such as corners, which could, in principle, act as landmarks. Despite these strongly polarizing geometric cues, HD cells in nondisoriented rats never rotated with these shapes. In contrast, when a cue card (white or gray) was added to one wall, HD cells readily rotated with the enclosure. When path integration was disrupted by disorienting the rat, HD cells rotated with the enclosure even without the landmark. Collectively, these findings indicate that geometry exerts little or no influence on heading computations in nondisoriented rats, but it can do so in disoriented rats. We suggest that geometric processing is only a weak influence, providing a backup system for heading calculations and recruited only under conditions of disorientation.

Neural encoding of large-scale three-dimensional space-properties and constraints.

How the brain represents represent large-scale, navigable space has been the topic of intensive investigation for several decades, resulting in the discovery that neurons in a complex network of cortical and subcortical brain regions co-operatively encode distance, direction, place, movement etc. using a variety of different sensory inputs. However, such studies have mainly been conducted in simple laboratory settings in which animals explore small, two-dimensional (i.e., flat) arenas. The real world, by contrast, is complex and three dimensional with hills, valleys, tunnels, branches, and—for species that can swim or fly—large volumetric spaces. Adding an additional dimension to space adds coding challenges, a primary reason for which is that several basic geometric properties are different in three dimensions. This article will explore the consequences of these challenges for the establishment of a functional three-dimensional metric map of space, one of which is that the brains of some species might have evolved to reduce the dimensionality of the representational space and thus sidestep some of these problems.

Allocentric directional processing in the rodent and human retrosplenial cortex

Head direction (HD) cells in the rodent brain have been investigated for a number of years, providing us with a detailed understanding of how the rodent brain codes for allocentric direction. Allocentric direction refers to the orientation of the external environment, independent of one’s current (egocentric) orientation. The presence of neural activity related to allocentric directional coding in humans has also been noted but only recently directly tested. Given the current status of both fields, it seems beneficial to draw parallels between this rodent and human research. We therefore discuss how findings from the human retrosplenial cortex (RSC), including its “translational function” (converting egocentric to allocentric information) and ability to code for permanent objects, compare to findings from the rodent RSC. We conclude by suggesting critical future experiments that derive from a cross-species approach to understanding the function of the human RSC.

Grid cells on steeply sloping terrain: evidence for planar rather than volumetric encoding.

Neural encoding of navigable space involves a network of structures centered on the hippocampus, whose neurons –place cells – encode current location. Input to the place cells includes afferents from the entorhinal cortex, which contains grid cells. These are neurons expressing spatially localized activity patches, or firing fields, that are evenly spaced across the floor in a hexagonal close-packed array called a grid. It is thought that grids function to enable the calculation of distances. The question arises as to whether this odometry process operates in three dimensions, and so we queried whether grids permeate three-dimensional (3D) space – that is, form a lattice – or whether they simply follow the environment surface. If grids form a 3D lattice then this lattice would ordinarily be aligned horizontally (to explain the usual hexagonal pattern observed). A tilted floor would transect several layers of this putative lattice, resulting in interruption of the hexagonal pattern. We model this prediction with simulated grid lattices, and show that the firing of a grid cell on a 40°-tilted surface should cover proportionally less of the surface, with smaller field size, fewer fields, and reduced hexagonal symmetry. However, recording of real grid cells as animals foraged on a 40°-tilted surface found that firing of grid cells was almost indistinguishable, in pattern or rate, from that on the horizontal surface, with if anything increased coverage and field number, and preserved field size. It thus appears unlikely that the sloping surface transected a lattice. However, grid cells on the slope displayed slightly degraded firing patterns, with reduced coherence and slightly reduced symmetry. These findings collectively suggest that the grid cell component of the metric representation of space is not fixed in absolute 3D space but is influenced both by the surface the animal is on and by the relationship of this surface to the horizontal, supporting the hypothesis that the neural map of space is “multi-planar” rather than fully volumetric.

A framework for three-dimensional navigation research

We have argued that the neurocognitive representation of large-scale, navigable three-dimensional space is anisotropic, having different properties in vertical versus horizontal dimensions. Three broad categories organize the experimental and theoretical issues raised by the commentators: (1) frames of reference, (2) comparative cognition, and (3) the role of experience. These categories contain the core of a research program to show how three-dimensional space is represented and used by humans and other animals.