Reading list: cognitive maps, place cells and grid cells

The water maze became famous because it is sensitive to the hippocampus. These papers explain why, from Tolman's idea of a "cognitive map" to the discovery of place cells and grid cells.

Tolman (1948). Cognitive maps in rats and men. Psychological Review 55(4):189-208. doi:10.1037/h0061626
Tolman's classic paper argues that rats learn a map-like representation of their environment rather than simple stimulus-response chains. It summarises latent learning and place-learning experiments and introduced the term 'cognitive map', which underpins later work on spatial navigation.
O'Keefe & Dostrovsky (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research 34(1):171-175. doi:10.1016/0006-8993(71)90358-1
O'Keefe and Dostrovsky recorded single units in the hippocampus of freely moving rats and found cells that fired when the rat was in a particular part of its environment. This short report gave the first evidence for what became known as place cells and the idea of the hippocampus as a spatial map.
O'Keefe (1976). Place units in the hippocampus of the freely moving rat. Experimental Neurology 51(1):78-109. doi:10.1016/0014-4886(76)90055-8
O'Keefe describes in detail hippocampal 'place units' in freely moving rats, whose firing is tied to the animal's location in the environment. The paper characterises their firing fields and established the place-cell description used in later spatial memory research.
Taube et al. (1990). Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. The Journal of Neuroscience 10(2):420-435. doi:10.1523/jneurosci.10-02-00420.1990
Taube, Muller and Ranck describe head-direction cells in the rat postsubiculum, which fire according to the direction the head is pointing in the horizontal plane, independent of location. Position and heading were measured with video tracking of two head-mounted LEDs.
Hafting et al. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052):801-806. doi:10.1038/nature03721
Hafting, Fyhn, Molden, Moser and Moser discovered grid cells in the dorsocaudal medial entorhinal cortex of the rat. These cells fire at the vertices of a regular triangular grid spanning the environment and form a topographically organised spatial map.
Moser et al. (2008). Place Cells, Grid Cells, and the Brain's Spatial Representation System. Annual Review of Neuroscience 31(1):69-89. doi:10.1146/annurev.neuro.31.061307.090723
Moser, Kropff and Moser review how hippocampal place cells and entorhinal grid cells together form the brain's spatial representation system. The review explains how grid cells may support a path-integration-based map of self-location.

O'Keefe & Dostrovsky (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research 34(1):171-175. doi:10.1016/0006-8993(71)90358-1 Classic
O'Keefe and Dostrovsky recorded single units in the hippocampus of freely moving rats and found cells that fired when the rat was in a particular part of its environment. This short report gave the first evidence for what became known as place cells and the idea of the hippocampus as a spatial map.
O'Keefe (1976). Place units in the hippocampus of the freely moving rat. Experimental Neurology 51(1):78-109. doi:10.1016/0014-4886(76)90055-8 Classic
O'Keefe describes in detail hippocampal 'place units' in freely moving rats, whose firing is tied to the animal's location in the environment. The paper characterises their firing fields and established the place-cell description used in later spatial memory research.
Morris et al. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297(5868):681-683. doi:10.1038/297681a0 Classic
Morris, Garrud, Rawlins and O'Keefe found that rats with hippocampal lesions were impaired at finding a hidden platform in the water maze but could still swim to a visible platform. The study linked water maze place navigation to hippocampal function.
O'Keefe & Recce (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3(3):317-330. doi:10.1002/hipo.450030307 Classic
O'Keefe and Recce found that hippocampal place cells fire at progressively earlier phases of the theta rhythm as the rat moves through the place field. This 'phase precession' showed that place cells carry spatial information in the timing of their spikes as well as their firing rate.
O'Keefe & Burgess (1996). Geometric determinants of the place fields of hippocampal neurons. Nature 381(6581):425-428. doi:10.1038/381425a0 Classic
O'Keefe and Burgess recorded the same place cells in rectangular boxes differing only in the length of their walls. Place fields changed shape and position with the geometry, consistent with a model in which fields are built from inputs tuned to distances from the walls.
Burgess et al. (2002). The Human Hippocampus and Spatial and Episodic Memory. Neuron 35(4):625-641. doi:10.1016/s0896-6273(02)00830-9 Classic
Burgess, Maguire and O'Keefe review neuropsychological, behavioural and neuroimaging evidence for the role of the human hippocampus in spatial and episodic memory. Several of the studies discussed use virtual reality to test navigation and memory in humans.
Astur et al. (2002). Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behavioural Brain Research 132(1):77-84. doi:10.1016/s0166-4328(01)00399-0 Classic
Astur, Taylor, Mamelak, Philpott and Sutherland tested patients with unilateral hippocampal resections in a virtual Morris water task. The patients showed severe spatial navigation impairments compared with controls, supporting the task's validity as a hippocampus-dependent test in humans.
Ekstrom et al. (2003). Cellular networks underlying human spatial navigation. Nature 425(6954):184-188. doi:10.1038/nature01964 Classic
Ekstrom and colleagues recorded single neurons in patients navigating a virtual town. Cells in the hippocampus responded at specific locations, providing direct evidence for place-like coding in humans during virtual navigation.
Hafting et al. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052):801-806. doi:10.1038/nature03721 Classic
Hafting, Fyhn, Molden, Moser and Moser discovered grid cells in the dorsocaudal medial entorhinal cortex of the rat. These cells fire at the vertices of a regular triangular grid spanning the environment and form a topographically organised spatial map.
Moser et al. (2008). Place Cells, Grid Cells, and the Brain's Spatial Representation System. Annual Review of Neuroscience 31(1):69-89. doi:10.1146/annurev.neuro.31.061307.090723 Classic
Moser, Kropff and Moser review how hippocampal place cells and entorhinal grid cells together form the brain's spatial representation system. The review explains how grid cells may support a path-integration-based map of self-location.
Garthe et al. (2009). Adult-Generated Hippocampal Neurons Allow the Flexible Use of Spatially Precise Learning Strategies. PLoS ONE 4(5):e5464. doi:10.1371/journal.pone.0005464 Classic
Garthe, Behr and Kempermann analysed water maze search strategies in mice with reduced adult hippocampal neurogenesis. They classified swim paths into strategies and found that new neurons were needed for the flexible use of precise spatial strategies, especially after the goal moved.
Harvey et al. (2009). Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461(7266):941-946. doi:10.1038/nature08499 Classic
Harvey and colleagues combined whole-cell recordings in head-restrained mice with a virtual linear track. They identified the subthreshold membrane dynamics of hippocampal place cells during virtual navigation.

If you want the methods behind these measures, HVS Image keeps a list of citations for its analyses and methods.

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