Everyday, we make our way out of our beds to the bathroom or drive home from work or school all without getting lost or relying on our devices for navigation. It has become second nature to interact with these spaces and the objects within them to such an extent that that these interactions happen without much thought. There is, however, an integrated network of systems contributing to spatial cognition, allowing us to navigate through the space around us, a skill which has evolutionarily become essential to the survival of both humans, and other organisms. The following will explore the neural mechanisms contributing to the formation of cognitive maps in non-human organisms, including the role of the hippocampus and specialised cells, and examine some of the questions which remain in our quest to understand where we are. Part two of this work will explore the correlates of these mechanisms in the human brain.
A brief history of space and time
Although the notion of a cognitive map was proposed by Tolmon in 1948 , it was O’Keefe and Dostrovsky’s discovery of the hippocampal place cells  in rodents that provided the necessary evidence to fuel research into cognitive maps. Their paper analyzed data of recordings from a small group of cells in the rodent hippocampus, demonstrating their responses to particular locations. An example of this is shown in Figure 1, where it is evident that different place cells in the CA1 region of the hippocampus fire only at certain areas . Further research resulted in O’Keefe and Nadel’s groundbreaking book “The Hippocampus as a Cognitive Map”, which drawing on the experimental evidence and case studies from the 20th century, confirmed that place cells within the hippocampus were the fundamental mechanism behind spatial coding in animals. This subsequently proposed that Tolman's idea of a cognitive map, allowing extrinsic environmental phenomena to be mapped internally, formed through the action of these place cells . They went on to assert that this cognitive map followed a Euclidean coordinate system, and it was the relationship between the objects in the animal’s environment encoded within this map which allowed animals to navigate. However, subsequent work over the next few decades raised various questions over what made place cells fire, as it became increasingly clear that the spatial fields in the hippocampus did not rely on conventional sensory input, since they even fired in the absence of light. This notion was not widely accepted in the scientific community as sufficient evidence over the mechanism was not available. It was a result of Ranck’s accidental discovery of the head direction cells in the subiculum , which were observed to fire at particular directions the animal was facing, that the cognitive map hypothesis became much more feasible, providing a possible mechanism behind the creation of spatial fields.
As the 1990s saw a shift from the allocentric hypothesis to an idiothetic one, it became commonly accepted that the integration of inputs from both the angular and linear velocity of the head provided feedback on the displacement and orientation of the animal from a given starting point, also referred to as path integration . Despite this and many other exciting developments, there still remain significant gaps pertaining to both the origin of spatial fields and the exact brain regions involved.
The Role of the Hippocampus
The hippocampus, albeit overshadowed in humans by the frontal and temporal association areas, accounts for around 10% of cortical volume in many mammals . Aside from its significant volume, the hippocampus is widely recognised as a key component for the formation of both spatial and episodic memory (the ability to recall personal events) . Hence, the cognitive map within the hippocampus, rather than being exclusively a spatial map, also encodes nonspatial information, providing a temporal context to the overall cognitive map . Consequently, rather than being a birds eye view of the local environment, it is a collection of memory systems which represent the external environment internally. This cognitive map is then utilised by the animal through its retrieval of past experience and its use of predicting capabilities, such as exploratory behaviour .
A contextual approach to examining cognitive maps also reveals further detail into the way in which these cognitive maps are woven into the animal’s behaviour. The sensitivity of place cells to temporal context  suggests that the hippocampus is able to create and store multiple overlapping maps, activated one at a time, yet which work together depending on the context of the behaviour being carried out. Consequently, if a novel environment is encountered or adjustments are made to a familiar one, new maps can be created or existing ones changed through hippocampal interactions. The latter process, termed remapping , was still being studied in the 1990s, which still saw exclusive focus on cells in the CA1 of the dorsal, as researchers working in the field were convinced that cognitive maps were of hippocampal origin. However, Menno Witter’s 1989 review on various theoretical and experimental studies regarding entorhinal-hippocampal mechanisms, which identified the topographically arranged interaction between the hippocampus and the entorhinal cortex,  prompted research into other potential origins. Although the medial entorhinal cortex (MEC) had been studied previously as an unsuccessful candidate for the origin of place cells , a revisit to this area in the early 21st century revitalized research in the role the dorsal MEC in the origin of the cognitive map .
Targeting the MECled to the discovery of grid cells: a neuron type similar to place cells in the specificity of their firing fields. However, unlike place cells, grid cells have numerous firing fields distributed throughout the animal’s environment . Another finding was that the firing fields of each cell formed a hexagonal grid over the space surrounding the animal . The role of these cells seemed paramount to the path integration model, as they revealed information about self-motion (ie distance travelled and time elapsed since start of motion) . Research also showed that unlike place cells, which were subject to extreme remapping, a single map from grid cells could be applied to multiple contexts and spaces, and therefore external objects were not required to ascertain the animal’s position . Since path integration relies on navigation based on a starting point, grid cells appear to be the primary candidates for the mechanism behind this form of navigation. It is only when the environment is resized or stretched that the spacing of the grid is altered, suggesting the presence of an overriding mechanism where disruptive external cues could take over the path integration mechanism . For example, the grid patterns generated by grid cells tend to fall apart in the absence of light , suggesting that some external cues are crucial to grid cell dynamics. While this raises questions over the importance of grid cells in navigation, there remain significant gaps in our understanding, and further research is required to fully comprehend the exact role of grid cells. In addition to path integration, activity of grid cells within the MEC has been observed in both spatial and nonspatial contexts which are not related to navigation. For example, a grid pattern is observed in humans in the representation of two-dimensional abstract knowledge, reiterating the nonspatial cognitive maps which exist in the brain .
In the years which followed the discovery of grid cells, an abundance of other functional cell types have been identified in the rodent brain, including border cells in the entorhinal cortex, which incorporate the fixed characteristics of the environment into the fields of both place and grid cells . The challenge which remains is understanding the dynamic interaction between these specialised cells, and how they provide the information on self-motion required to carry out path-integration, and ultimately enable navigation. We still have no clear understanding of how cognitive maps are used. Although the distinct firing patterns of these cells have been recorded and studied, the enabling of these patterns remains to be discovered. This also extends to our lack of understanding of the impact of hippocampal output on the neocortex: how is this abundant range of sensory information used in the neocortex, and are there cells in the cortex which are responsible for this integration? Furthermore, research is needed to understand how this sensory information is integrated in planning and decision-making behaviour, to gain insight into the practical use of cognitive maps. Previous research has only studied cognitive maps in an enclosed, local environment, and as a result we have no understanding of how cognitive maps are represented in larger three-dimensional environments, such as the organism’s own habitat, and how navigation takes place in these environments, including whether path integration still applies. If future experiments allow such spaces to be observed, we may finally gain an understanding of the significance of cognitive maps. As has been stressed in this article, there is an abundance of research which speculates cognitive maps are means of processing higher cognitive information, and further research is indeed required to study cognitive maps in other contexts than navigation. Consequently, despite having a vast amount of information on the components of the systems involved, it is once again the interaction of these systems which remains elusive to us, as tends to be the case in many areas of neuroscience research.
This article has examined some of the key findings in spatial mapping, including the evolution of our initial hippocampal view to a more global approach in our investigation of the mapping of the external environment in the rodent brain, along with the various specialised cells which have been discovered. Although significant gaps in our knowledge remain, especially in the interactions of these functional cells, new research regularly emerges and will continue to do so in the years to come.
The systems discussed have all been discovered through experiments carried out in non-human mammals, and although some anatomical areas are unanimous amongst all mammals, such as the hippocampus, there are significant differences which question whether cognitive maps are formed and retained in a similar manner, and whether they are crucial for spatial navigation. A review of cognitive maps in humans requires a detailed review of some key experiments which have been conducted, and this will be revisited in part two of this article in the following issue.
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