The representation of space in the brain
Graphical abstract
Section snippets
Spatial representations in the brain
The study of how organisms are able to navigate their environment is in many ways the study of survival; all animals must navigate to find mates, shelter, food and water. For wild animals this often means navigating large expanses of land, perhaps also with limited cues. For example, Peters (1978) reports that in wooded areas masked by snow, wolves often take long, complex, winding, unplanned paths when hunting − but they can still return directly to the distant location of their pups.
The hippocampus
Initial interest in the hippocampus was sparked by the observed impact of hippocampal damage, both accidental and intentional, on behaviour. One of the most influential cases in this respect was that of a patient, Henry Molaison, known for many years only as patient H.M., who suffered from epileptic seizures which were found to arise from structures in his medial temporal lobe. In 1953 surgeons removed, bilaterally, H.M.’s hippocampal formation and a number of adjacent structures (Corkin et
Place cells
The excitement generated by the case report of patient H.M. led researchers to embark upon electrophysiological investigations of the hippocampus. When O’Keefe and Dostrovsky (1971) took advantage of a newly developed technique to record single, complex spiking (Fox and Ranck, 1975, Ranck, 1973), pyramidal (Henze et al., 2000) neurons in the rat hippocampus (Fig. 1A and Fig. 2) they found that the firing rate of many of these cells was modulated purely by spatial location (Fig. 1B), and named
Head direction cells
The discovery of head direction (HD) cells came about in the aftermath of the original place cell report, when researchers were still trying to understand the source of their spatial firing. Ranck, 1985, Ranck, 1984 reported finding, in the dorsal presubiculum of the rat, cells that were modulated by the facing direction of the head, and a detailed description of the activity of these ‘head direction’ cells was published shortly after (Taube et al., 1990a, Taube et al., 1990b, Taube et al., 1987
Grid cells
Unlike place cells in the hippocampus, many cells in the mEC fire in multiple discrete and regularly spaced locations which form a triangular lattice or tessellated grid (Fig. 1D). These ‘grid cells’ are found close to the border between the mEC and postrhinal cortex (Fyhn et al., 2004, Hafting et al., 2005) and in the pre- and parasubiculum (Boccara et al., 2010)(Fig. 2). Like place cells, the firing of grid cells is partially dictated by external cues; when distal landmarks are rotated, grid
Interneurons
Interneurons are a morphologically diverse class of typically high firing-rate neurons that use the inhibitory transmitter gamma-Aminobutyric acid (GABA). They usually form local networks of neurons that mostly control their neighbours via short-range, inhibitory connections, and for a long time were thought only to have the relatively uninteresting role of modulating local network activity so as to prevent runaway excitation and epileptic seizures. It is now thought that some of them may have
Extrahippocampal place cells
This review is primarily concerned with spatial representations in the brain other than the ‘big three’ cell types, the simplest examples of which are perhaps neurons analogous to place cells in brain areas outside the hippocampus (HPC). For example; both Quirk et al. (1992) and Hargreaves et al. (2005) reported finding cells resembling hippocampal place cells in the medial entorhinal cortex (mEC): the same structure where grid cells can predominantly be found (Fig. 3). However, it is not known
Boundary/border cells
Perhaps the relatively unique spatial representation in the hippocampus is due to the variety of spatial inputs that project there. For example, another widely researched, but often overlooked cell type responds purely to environmental boundaries (Fig. 4) − these cells have a complex relationship with both place and grid cells that is still not greatly understood. Early observations demonstrated that hippocampal place cell firing often appears to be determined, at least partly, by the geometric
Object cells
Recognising if a stimulus is novel or familiar is often crucial to an animal’s survival and this is true as much of object recognition as it is of recognising an immediate threat − confusing a slice of pizza for your hat may result in a short period of embarrassment but it's easy to see how faulty or non-existent object recognition such as this could escalate quickly to be a life or death matter, especially for animals. Furthermore, the recognition and memory of objects may underlie features of
Goal cells
Similar to object recognition, the representation of spatial and nonspatial goals is a fundamental requirement of survival. Rarely do we navigate without a specific goal in mind, even if it is only a subgoal on a longer journey or a simple place of regular interest such as the supermarket. Without a representation of the supermarket however you would need to walk aimlessly until randomly finding it every time you needed to buy milk. It is true that rats do not need to buy milk very often, but
Conjunctive cells
So far we have seen examples of cells with specific representations of space, however, many cells in the brain do not form a pure representation such as this, especially those cells in structures associated with integrative processes. Many cells encode a number of environmental, spatial or behavioural features simultaneously and are thus termed ‘conjunctive cells’. Concentrating on those cells that conjunctively encode spatial features, many of these are found in the medial entorhinal cortex,
Movement- or action-sensitive cells
So far in this review we have focused on those cells that encode an animal’s spatial location: however, movement through space is a critical part of spatial processing, and many cells in the brain encode movement, or encode space conjunctively with movement. Self-motion information can be used to estimate spatial location through path integration processes if a known reference point is provided (Mittelstaedt and Mittelstaedt, 1980). As such, self-motion information is generally concerned with
Conclusion
The study of the neural encoding of space began with the discovery (albeit spread across 30 years) of a triumvirate of spatially modulated neurons: the place cells, head direction cells and grid cells. Studies of the network in which these neurons are embedded has revealed many more cells that have firing properties relevant to spatial encoding (See Fig. 8 for a summary “wiring diagram”). Some of the response profiles are conjunctive, making activity sometimes difficult to decipher, and it
Future research
We have covered many different cell types so far discovered in a variety of different brain regions, but the question of how spatial cognition is supported is far from resolved. For instance, interneurons are spread throughout the brain and as we have seen here, may contribute significantly to the spatial modulation of many other cell types (Hangya et al., 2010). Neural network models, deep learning projects and major collaborative research such as the Human Brain Project all require data
Acknowledgment
This work was supported by a grant from the Wellcome Trust (103896AIA) to KJ.
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