Kate Jeffery

Learned interaction of visual and idiothetic cues in the control of place field orientation

Abstract In a symmetrical environment (like a square box) hippocampal place cells use a mixture of visual and idiothetic (movement) information to tell them which way the environment is oriented. The present experiment tested the hypothesis that if the visual landmarks were mobile, place cells would learn to disregard these and rely on idiothetic cues instead. Place cells were recorded in a square box surrounded by circular black curtains. A cue card hung on the curtain behind one of the walls to break the fourfold symmetry. The relative influence of this card on the location of place fields was assessed each day by confining the rat on a rotating platter underneath an opaque cover, and then rotating the card and the platter by different amounts, to see whether subsequently recorded place fields had rotated with the card or with the rat. For some rats, these trials had been preceded by trials in which the card had been visibly moved from trial to trial, so that the rats had seen that it was mobile. Other rats received no prior visual information that the card was mobile. In the rats that had previously seen the card move, place fields initially rotated with the card but by the end of five sessions usually rotated with the rat instead. For rats that had never seen the card move, place fields always followed the card. Thus, the cells were able to ”learn” that their preferred directional input, the card, was unreliable. A third group of rats, who were covered only for 30 s while the card was moved, showed mixed behaviour, suggesting a degradation of the idiothetic trace with time.

Directional control of hippocampal place fields

Abstract Pyramidal cells in the rat hippocampus fire whenever the animal is in a particular place, suggesting that the hippocampus maintains a representation of the environment. Receptive fields of place cells (place fields) are largely determined by the distance of the rat from environmental walls. Because these walls are sometimes distinguishable only by their orientation with respect to the outside room, it has been hypothesised that a polarising directional input enables the cells to locate their fields off–centre in an otherwise symmetrical environment. We tested this hypothesis by gaining control of the rat’s internal directional sense, independently of other cues, to see whether manipulating this sense could, by itself, produce a corresponding alteration in place field orientation. Place cells were recorded while rats foraged in a rectangular box, in the absence or presence of external room cues. With room cues masked, slow rotation of the rat and the box together caused the fields to rotate accordingly. Rotating the recording box alone by 180° rarely caused corresponding field rotation, while rotating the rat alone 180° outside the environment and then replacing it in the recording box almost always resulted in a corresponding rotation of the fields. This shows that place field orientation can be controlled by controlling the internal direction-sense of the rat, and it opens the door to psychophysical exploration of the sensory basis of the direction sense. When room cues were present, distal visual cues predominated over internal cues in establishing place field orientation.

Grid Cells Form a Global Representation of Connected Environments.

Summary The firing patterns of grid cells in medial entorhinal cortex (mEC) and associated brain areas form triangular arrays that tessellate the environment [1, 2] and maintain constant spatial offsets to each other between environments [3, 4]. These cells are thought to provide an efficient metric for navigation in large-scale space [5–8]. However, an accurate and universal metric requires grid cell firing patterns to uniformly cover the space to be navigated, in contrast to recent demonstrations that environmental features such as boundaries can distort [9–11] and fragment [12] grid patterns. To establish whether grid firing is determined by local environmental cues, or provides a coherent global representation, we recorded mEC grid cells in rats foraging in an environment containing two perceptually identical compartments connected via a corridor. During initial exposures to the multicompartment environment, grid firing patterns were dominated by local environmental cues, replicating between the two compartments. However, with prolonged experience, grid cell firing patterns formed a single, continuous representation that spanned both compartments. Thus, we provide the first evidence that in a complex environment, grid cell firing can form the coherent global pattern necessary for them to act as a metric capable of supporting large-scale spatial navigation.

An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex

We investigated how landmarks influence the brains computation of head direction and found that in a bidirectionally symmetrical environment, some neurons in dysgranular retrosplenial cortex showed bidirectional firing patterns. This indicates dominance of neural activity by local environmental cues even when these conflicted with the global head direction signal. It suggests a mechanism for associating landmarks to or dissociating them from the head direction signal, according to their directional stability and/or utility.

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.

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.

Purely Translational Realignment in Grid Cell Firing Patterns Following Nonmetric Context Change

Grid cells in entorhinal and parahippocampal cortices contribute to a network, centered on the hippocampal place cell system, that constructs a representation of spatial context for use in navigation and memory. In doing so, they use metric cues such as the distance and direction of nearby boundaries to position and orient their firing field arrays (grids). The present study investigated whether they also use purely nonmetric “context” information such as color and odor of the environment. We found that, indeed, purely nonmetric cues—sufficiently salient to cause changes in place cell firing patterns—can regulate grid positioning; they do so independently of orientation, and thus interact with linear but not directional spatial inputs. Grid cells responded homogeneously to context changes. We suggest that the grid and place cell networks receive context information directly and also from each other; the information is used by place cells to compute the final decision of the spatial system about which context the animal is in, and by grid cells to help inform the system about where the animal is within it.

Multivoxel pattern analysis reveals 3D place information in the human hippocampus

The spatial world is three dimensional (3D) and humans and other animals move both horizontally and vertically within it. Extant neuroscientific studies have typically investigated spatial navigation on a horizontal 2D plane, leaving much unknown about how 3D spatial information is represented in the brain. Specifically, horizontal and vertical information may be encoded in the same or different neural structures with equal or unequal sensitivity. Here, we investigated these possibilities using fMRI while participants were passively moved within a 3D lattice structure as if riding a rollercoaster. Multivoxel pattern analysis was used to test for the existence of information relating to where and in which direction participants were heading in this virtual environment. Behaviorally, participants had similarly accurate memory for vertical and horizontal locations and the right anterior hippocampus (HC) expressed place information that was sensitive to changes along both horizontal and vertical axes. This is suggestive of isotropic 3D place encoding. In contrast, participants indicated their heading direction faster and more accurately when they were heading in a tilted-up or tilted-down direction. This direction information was expressed in the right retrosplenial cortex and posterior HC and was only sensitive to vertical pitch, which could reflect the importance of the vertical (gravity) axis as a reference frame. Overall, our findings extend previous knowledge of how we represent the spatial world and navigate within it by taking into account the important third dimension. SIGNIFICANCE STATEMENT The spatial world is 3D. We can move horizontally across surfaces, but also vertically, going up slopes or stairs. Little is known about how the brain supports representations of 3D space. A key question is whether horizontal and vertical information is equally well represented. Here, we measured fMRI response patterns while participants moved within a virtual 3D environment and found that the anterior hippocampus (HC) expressed location information that was sensitive to the vertical and horizontal axes. In contrast, information about heading direction, found in retrosplenial cortex and posterior HC, favored the vertical axis, perhaps due to gravity effects. These findings provide new insights into how we represent our spatial 3D world and navigate within it.

Grid Cells Encode Local Positional Information

Summary The brain has an extraordinary ability to create an internal spatial map of the external world [1]. This map-like representation of environmental surroundings is encoded through specific types of neurons, located within the hippocampus and entorhinal cortex, which exhibit spatially tuned firing patterns [2, 3]. In addition to encoding space, these neurons are believed to be related to contextual information and memory [4, 5, 6, 7]. One class of such cells is the grid cells, which are located within the entorhinal cortex, presubiculum, and parasubiculum [3, 8]. Grid cell firing forms a hexagonal array of firing fields, a pattern that is largely thought to reflect the operation of intrinsic self-motion-related computations [9, 10, 11, 12]. If this is the case, then fields should be relatively uniform in size, number of spikes, and peak firing rate. However, it has been suggested that this is not in fact the case [3, 13]. The possibility exists that local spatial information also influences grid cells, which—if true—would greatly change the way in which grid cells are thought to contribute to place coding. Accordingly, we asked how discriminable the individual fields of a given grid cell are by looking at the distribution of field firing rates and reproducibility of this distribution across trials. Grid fields were less uniform in intensity than expected, and the pattern of strong and weak fields was spatially stable and recurred across trials. The distribution remained unchanged even after arena rescaling, but not after remapping. This suggests that additional local information is being overlaid onto the global hexagonal pattern of grid cells.

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.