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  • Review Article
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Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation

An Erratum to this article was published on 20 February 2015

Key Points

  • Real-life navigation takes place in large natural environments that are complex and multiscaled. There is a fundamental gap between large-scale navigation and typical laboratory studies of the neurobiology of navigation, in which animals navigate in small boxes. This is a gap in spatial scales, in the richness of sensory information available, and in the techniques used and models proposed for describing small-scale versus large-scale navigation.

  • Spatial cells in the mammalian hippocampal formation include place cells, grid cells, head-direction cells and border (boundary) cells. It is unknown whether and how these neurons contribute to natural navigation on scales beyond a few meters.

  • Bats are excellent animal models for studying spatial cognition, because they are superb navigators, and possess multiple excellent sensory systems, including vision, olfaction and echolocation (biosonar). Bat echolocation is an active-sensing system with high accuracy and dynamic flexibility, which bears surprising similarities to rat whisking and sniffing, with the benefit that bat biosonar can be analysed quantitatively by using the mathematical theory of sonar.

  • Large-scale navigation is likely to be dominated by incoming sensory information rather than by self-motion cues (path integration). Two prominent sensory-based models of place fields, the boundary vector cell (BVC) model and the view-based model, both predict that sensory resolution determines the spatial resolution of place cells.

  • The multiscale character of natural habitats, from small rat burrows and bat caves to large kilometre-scale trajectories, suggests that neural spatial representation by place cells should adapt to this multiscale structure. Three phenomena described in the literature could serve as mechanisms for such multiscale representation: these include the dorsoventral gradient of place-field size in the hippocampus and dorsoventral gradient of grid-spacing in the medial entorhinal cortex, the dynamic adjustment of place-field size to environmental dimensions, and the enhanced precision of spatial representation using population coding.

  • Theoretical models suggested several ways to bridge the gap between spatial representations for 1-m boxes used in laboratory experiments, versus kilometre-scale natural environments. Models of place cells proposed that place fields could rescale according to environmental size, or that place cells can exhibit dozens or hundreds of place fields per neuron; whereas for grid cells, models proposed a combinatorial grid code that could represent simultaneously both small-scale and large geographical environments.

  • Future directions include the need to understand which of these theoretical models best captures the actual neural basis of large-scale navigation, as well as the need to elucidate the neural mechanisms of route planning, re-orienting after losing one's path, and how different maps are stitched together. To answer these questions would require electrophysiological recordings from the hippocampal formation of animals navigating in large-scale, complex naturalistic environments.

Abstract

Spatial orientation and navigation rely on the acquisition of several types of sensory information. This information is then transformed into a neural code for space in the hippocampal formation through the activity of place cells, grid cells and head-direction cells. These spatial representations, in turn, are thought to guide long-range navigation. But how the representations encoded by these different cell types are integrated in the brain to form a neural 'map and compass' is largely unknown. Here, we discuss this problem in the context of spatial navigation by bats and rats. We review the experimental findings and theoretical models that provide insight into the mechanisms that link sensory systems to spatial representations and to large-scale natural navigation.

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Figure 1: Sensory modalities of bats.
Figure 2: Effects of sensory input on spatial representation.
Figure 3: Spatial representations on multiple scales.
Figure 4: Models of large-scale spatial codes.

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Acknowledgements

We thank D. Derdikman, S. Romani, A. Finkelstein, A. Rubin, T. Eliav, G. Ginosar, A. Wallach and R. Paz for helpful comments on the manuscript; D. Sheynikhovich for simulations of the view-based model of place cells; and G. Brodsky for graphics. This work was supported by research grants to N.U. from the European Research Council (ERC–NEUROBAT), the Human Frontiers Science Program (HFSP RGP0062/2009-C), and the Israel Science Foundation (ISF 1017/08 and ISF 1319/13).

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Glossary

Place cells

Hippocampal neurons that become active whenever the animal traverses a specific location in the environment, called the 'place field'. The dimensions of the place field govern the spatial resolution of a single place cell; and together, multiple place cells are thought to represent a mental map of absolute (allocentric) space.

Grid cells

Neurons in the medial entorhinal cortex (and some adjacent regions) that become active whenever the animal traverses one of the vertices of a periodic hexagonal or triangular lattice that tiles the environment.

Head-direction cells

Neurons found in multiple brain areas, which become active whenever the animal's head points to a specific absolute (allocentric) direction, thus providing a compass signal.

Doppler effect

The change in wave frequency for an observer that is moving relative to the wave source. For example, when an ambulance with a siren approaches an observer, a high-pitched sound (high frequency) is heard, but the perceived frequency drops when the ambulance passes and drives away. Bats know their own emitted frequency, and thus can use the perceived shifted frequency of the echo (Doppler shift) to compute the relative velocity of the target.

Magnetosensation

The ability to detect the Earth's magnetic field and use it to compute direction or spatial position. Utilizing magnetosensation for navigation purposes has been described in many animals, including some rodents and bats.

Egocentric coordinates

Coordinates that are given relative to the body axis; for example, '1 km to your left'.

Allocentric coordinates

Coordinates that are independent of the observer's orientation; for example, '1 km North of Tel Aviv'. Also known as absolute-space coordinates.

Border cells

(Also known as boundary cells.) Neurons that become active when the animal is close to a salient border of the environment, thus signalling the environmental geometry.

Distal senses

Senses that provide long-range information to the animal. For rats, vision is the primary distal sense. Bats have two distal senses, echolocation and vision, when considering a small environment like a cave or a room. However, echolocation range is limited to < 100 m, so on a scale of kilometres, echolocation may be classified as proximal, while vision remains a truly distal sense. In both species, olfaction is a proximal sense in enclosed spaces (cave, burrow), but may serve as a distal sense outdoors where winds can carry odours from afar.

Proximal senses

Senses that are restricted to a short range. For rats, somatosensation (whisking) and olfaction are the primary proximal senses.

Dorsoventral axis of the hippocampus

The hippocampus of rats and bats is an elongated, banana-shaped structure, and its long axis is referred to as the dorsoventral axis (or septotemporal axis). Place fields increase in size approximately 10-fold along this axis.

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Geva-Sagiv, M., Las, L., Yovel, Y. et al. Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nat Rev Neurosci 16, 94–108 (2015). https://doi.org/10.1038/nrn3888

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