Allocentric directional processing in the rodent and human retrosplenial cortex

Copyright © 2014 Knight and Hayman. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these termsHead 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 RSCPeer reviewedFinal Published versio

Entorhinal Neurons Exhibit Cue Locking in Rodent VR

The regular firing pattern exhibited by medial entorhinal (mEC) grid cells of locomoting rodents is hypothesized to provide spatial metric information relevant for navigation. The development of virtual reality (VR) for head-fixed mice confers a number of experimental advantages and has become increasingly popular as a method for investigating spatially-selective cells. Recent experiments using 1D VR linear tracks have shown that some mEC cells have multiple fields in virtual space, analogous to grid cells on real linear tracks. We recorded from the mEC as mice traversed virtual tracks featuring regularly spaced repetitive cues and identified a population of cells with multiple firing fields, resembling the regular firing of grid cells. However, further analyses indicated that many of these were not, in fact, grid cells because: (1) when recorded in the open field they did not display discrete firing fields with six-fold symmetry; and (2) in different VR environments their firing fields were found to match the spatial frequency of repetitive environmental cues. In contrast, cells identified as grid cells based on their open field firing patterns did not exhibit cue locking. In light of these results we highlight the importance of controlling the periodicity of the visual cues in VR and the necessity of identifying grid cells from real open field environments in order to correctly characterize spatially modulated neurons in VR experiments

Entorhinal neurons exhibit cue locking in rodent VR

The regular firing pattern exhibited by medial entorhinal (mEC) grid cells of locomoting rodents is hypothesized to provide spatial metric information relevant for navigation. The development of virtual reality (VR) for head-fixed mice confers a number of experimental advantages and has become increasingly popular as a method for investigating spatiallyselective cells. Recent experiments using 1D VR linear tracks have shown that some mEC cells have multiple fields in virtual space, analogous to grid cells on real linear tracks. We recorded from the mEC as mice traversed virtual tracks featuring regularly spaced repetitive cues and identified a population of cells with multiple firing fields, resembling the regular firing of grid cells. However, further analyses indicated that many of these were not, in fact, grid cells because: (1) when recorded in the open field they did not display discrete firing fields with six-fold symmetry; and (2) in different VR environments their firing fields were found to match the spatial frequency of repetitive environmental cues. In contrast, cells identified as grid cells based on their open field firing patterns did not exhibit cue locking. In light of these results we highlight the importance of controlling the periodicity of the visual cues in VR and the necessity of identifying grid cells from real open field environments in order to correctly characterize spatially modulated neurons in VR experiments

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 animal

Navigating in a three-dimensional world

The study of spatial cognition has provided considerable insight into how animals (including humans) navigate on the horizontal plane. However, the real world is three-dimensional, having a complex topography including both horizontal and vertical features, which presents additional challenges for representation and navigation. The present article reviews the emerging behavioral and neurobiological literature on spatial cognition in non-horizontal environments. We suggest that three-dimensional spaces are represented in a quasi-planar fashion, with space in the plane of locomotion being computed separately and represented differently from space in the orthogonal axis-a representational structure we have termed "bicoded.” We argue that the mammalian spatial representation in surface-travelling animals comprises a mosaic of these locally planar fragments, rather than a fully integrated volumetric map. More generally, this may be true even for species that can move freely in all three dimensions, such as birds and fish. We outline the evidence supporting this view, together with the adaptive advantages of such a schem

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

Neural encoding of navigable space involves a network of structures centred 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 localised 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 grid cell 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 space – that is, form a lattice – or whether they simply follow the environment surface. If grids form a three-dimensional lattice then a tilted floor should transect several layers of this lattice, resulting in interruption of the hexagonal pattern. We model this prediction with simulated grid lattices and show that on a 40-degree slope the firing of a grid cell should cover proportionally less of the surface, with smaller field size and fewer fields and reduced hexagonal symmetry. However, recording of grid cells as animals foraged on a 40-degree-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 three-dimensional 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

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

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

Rodent spatial cognition studies allow links to be made between neural and behavioural phenomena, and much is now known about the encoding and use of horizontal space. However, the real world is three dimensional, providing cognitive challenges that have yet to be explored. Motivated by neural findings suggesting weaker encoding of vertical than horizontal space, we examined whether rats show a similar behavioural anisotropy when distributing their time freely between vertical and horizontal movements. We found that in two- or three-dimensional environments with a vertical dimension, rats showed a prioritization of horizontal over vertical movements in both foraging and detour tasks. In the foraging tasks, the animals executed more horizontal than vertical movements and adopted a “layer strategy” in which food was collected from one horizontal level before moving to the next. In the detour tasks, rats preferred the routes that allowed them to execute the horizontal leg first. We suggest three possible reasons for this behavioural bias. First, as suggested by Grobety and Schenk [5], it allows minimisation of energy expenditure, inasmuch as costly vertical movements are minimised. Second, it may be a manifestation of the temporal discounting of effort, in which animals value delayed effort as less costly than immediate effort. Finally, it may be that at the neural level rats encode the vertical dimension less precisely, and thus prefer to bias their movements in the more accurately encoded horizontal dimension. We suggest that all three factors are related, and all play a part

Short screening tools for risky drinking in Aboriginal and Torres Strait Islander Australians : Modified AUDIT-C and a new approach

Background Alcohol consumption among Indigenous Australians can involve a stop-start pattern of drinking, with consumption well above recommended guidelines on each occasion. Such intermittent drinking patterns can make screening for risky drinking difficult. This study evaluates the ability of several short alcohol screening tools, contained in the Grog Survey Application, to detect short- or long-term risky drinking as defined by Australian guidelines. Tested tools include a modification of Alcohol Use Disorders Identification Test-Consumption (AUDIT-Cm). Methods Alcohol consumption was assessed in current drinkers in the past year (n = 184) using AUDIT-Cm and using the last four drinking occasions (Finnish method). Sensitivity and specificity were assessed relative to the Finnish method, for how AUDIT-Cm score (3 + for women, 4 + for men), and how subsets of AUDIT-Cm questions (AUDIT-1m and AUDIT-2m; and AUDIT-3mV alone) were able to determine short- or long-term risk from drinking. Responses to AUDIT-Cm were used to calculate the average standard drinks consumed per day, and the frequency at which more than four standard drinks were consumed on single occasions. Finally, shorter versions of the Finnish method (1, 2, or 3 occasions of drinking) were compared to the full Finnish method, by examining the percentage of variance retained by shorter versions. Results AUDIT-Cm has a high sensitivity in detecting at-risk drinking compared with the Finnish method (sensitivity = 99%, specificity = 67%). The combination of AUDIT-1m and AUDIT-2m was able to classify the drinking risk status for all but four individuals in the same way as the Finnish method did. For the Finnish method, two drinking sessions to calculate drinks per drinking occasion, and four to calculate frequency resulted in nearly identical estimates to data on all four of the most recent drinking occasions (r2 = 0.997). Conclusions The combination of AUDIT-1m and AUDIT-2m may offer advantages as a short screening tool, over AUDIT-3mV, in groups where intermittent and high per occasion drinking is common. As an alternative to the full Finnish method, the quantity consumed on the last two occasions and timing of the last four occasions may provide a practical short screening tool