Notes on "The hippocampus, memory and place cells: is it spatial memory or a memory space?", Eichenbaum et al., Neuron, vol 23, pp 209-226, 1999
I found this paper at just the right time in terms of my research. When looking at navigation tasks for robots, and when trying to derive inspiration and lessons from natural systems, one cannot get far without coming across place cells. Place cells are neurons located in the hippocampus (although there are possibly also cells in other brain regions with somewhat similar behaviours?), and are so named because they can be observed to fire when the animal under observation is in a specific location is its environment. This observation is very robust in rats in particular (although other species have been used), and has led to the now pervasive view that place cells form the basis of a cognitive map - i.e. a map of the environment upon which cognitive operations may be performed (such as planning for e.g.). These maps may essentially be seen as allocentric 2-D coordinate representations of the environment - a property which every computational model of place cell functionality has inherited. It is interesting to note however that while this has been become generally accepted theory in the animal sciences, neurospychologists who study memory in primates and humans have been very slow to take on the theory. This is mainly due to the contention of the former that the hippocampus is dedicated to spatial memory in rodents (the aforementioned cognitive map), whereas in humans, the global memory deficits shown by hippocampal lesions in humans is well known, casting doubt on the solely spatial memory proposition.
The aim of the paper is to review the evidence and put forward a theory of place cell function which is consistent with both camps. The classic literature on place cells in rats is first reviewed (mainly work by O'Keefe at al). Single neuron (extracellular) recordings are the most common means of measuring place cell activity. As mentioned, it has been well documented that these fire when the rat is in specific locations in the environment. However, as was noted in the initial experiments concerning the existence of these cells, but which has in subsequent studies been largely ignored, place cells also fire for non-spatial cues, which clearly isn't consistent with the cognitive map theory of place cell functionality. Additionally, subsequent studies looking for further evidence in support of the cognitive map theory, namely homogeneity and continuityof spatial representations and the binding of spatial representations in a cohesive framework, found evidence against cognitive maps. First off, evidence points to the fact that place-fields of plac cells do not provide a continuous map: clustering of place fields occur, indicating the over-representation of some spatial areas with respect to others. Secondly, it appears as though place cells involve a collection of independant representations, each encoding the spatial relations between some subset of cues. These three points against the cognitive map theory, along with some others, indicate the need for a rethink on this subject.
The authors duly oblige with an alternative account: instead of a cognitive map solely tied to spatial stimuli, there exists a memory space: individual hippocampal cells encode regularitie present in the animals every experience, including spatial and non-spatial cues and behavioural actions. On a side note, this appears to me to be consistent with the idea of "fast" or "one-shot" learning in the hippocampus, and "slow" learning in the neocortex. It also seems to be not inconsistent with Fusters overlapping cortical hierarchies and distributed neural representations theory, upon which I have written in previous posts.
According to this theory, different specialities of neuons arise in the hippocampus as a direct result of the different possible combinations of inputs and input weights, and the history of coactive inputs (essentially hebbian learning, I believe...), and where these inputs are derived from (from which part of the cortex, or brain). This new theory thus leads to an alternative explanation as to the activity of place cells: instead of being a cognitive map as described previously, they may be characterised as a set of activations along a temporal sequence as the rat moves in different trial episodes. This would also apply to the learning and performance of other non-spatial tasks, which would thus account for place cell activity for non-spatial cues. Given this account, the hippocampus is thus perceived to be central to the functioning of episodic memory.
The paper concludes with the observation that this model can be distinguished from spatial mapping theories in that it proposes a set of mechanisms which account for both spatial and non-spatial memory dependant on the hippocampus. From the point of view of the first to sentences of this post, and my observation on this models relation to Fusters cortical hierarchies, it seems possible (or not-impossible as I'd prefer to say) that navigation can be described in terms of associative links, instead of having to rely on an internally generated cognitive map.