Spatial and ethological memory
Professor of Cognitive Neuroscience
Tel: +44 20 3108 8004 (EA Karen Fergus)
The hippocampus and amygdala, both members of the limbic system in the temporal lobes, provide two distinct types of memory. The hippocampal formation underpins spatial memory, providing long-term memories for locations and a neural mechanism for supporting navigation and exploration. In contrast amygdala provides short-term memories for ecologically significant information such as an interaction with a particular conspecific or the consumption of a particular food. Our current research is directed toward unraveling the role of the entorhinal cortex and hippocampus in spatial memory and understanding the mechanisms underlying short-term memories in the amygdala.
We employ a range of technologies including tetrode and high density neuropixels electrophysiological probes, two photon imaging in conjunction with virtual reality environment, and novel maze tasks to study the spatial correlates of hippocampal and medial entorhinal cortical cells. Figure 1 shows the fields of 12 entorhinal grid cells recorded 47 days after implantation of a neuropixels probe.
In recent work we have shown that the grid structure is not uniform across the whole of a nonhomogeneous environment such as a trapezoid and that single fields can be manipulated by the movement of nearby walls of the enclosure. Figure 2 shows that the symmetrical grid pattern recorded from a grid cell in a square is distorted and much less gridlike in the trapezoid. This finding calls into question how useful the grid system is for providing a metric for the cognitive map and suggests that the grids are more responsive to the shape of the enclosure than had previously been suspected.
Cells in the amygdala respond selectively to stimuli of ethological significance such as a conspecific or a specific food, and continue to fire after the removal of that stimulus for periods of minutes. We are trying to understand the mechanism underlying this short-term response and to understand its function. Does it provide a memory of the event or does it provide some other type of signal for example enabling other areas of the brain to consolidate information stored at the time of an important ethological event.
- Group Members
- Selected Publications
- O'Keefe J & Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34: 171-175. First description of hippocampal place cells and suggestion that the hippocampus was a spatial map.
- O'Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exptl. Neurol., 51: 78-109. More extensive description of place cells elaborating upon the suggestions in O’Keefe and Dostrovsky 1971.
- O'Keefe J & Nadel L (1978) The Hippocampus as a Cognitive Map, Clarendon Press, Oxford. On- line version, http://www.cognitivemap.net/. Full description of the cognitive map theory and the evidence from anatomy, physiology, and behavioural studies in support. Highly cited monograph now available on the Internet.
- Morris RGM, Garrud P, Rawlins JNP & O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature, 297: 681-683. Demonstration of a deficit in learning the Morris water maze following hippocampal lesions.
- O'Keefe J & Speakman A (1987) Single unit activity in the rat hippocampus during a spatial memory task. Exp. Brain Res., 68: 1-27. Demonstration of a correlation between place cell activity and the animal’s behaviour in a spatial memory task.
- O'Keefe J & Recce M (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3: 317-330. Description of hippocampal phase precession effect, strong evidence for temporal coding in the nervous system.
- O'Keefe J & Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature, 381, 425-428. Demonstrated that the walls of the environment had an important influence on the shape of place cells.
- Wills T, Lever C, Cacucci F, Burgess N & O'Keefe J (2005) Attractor dynamics in the hippocampal representation of the local environment. Science 308: 873-876. Attractor-like mechanisms in the plasticity demonstrated by hippocampal place cells.
- Burgess N, Barry C & O'Keefe J (2007) An Oscillatory Interference Model of Grid Cell Firing. Hippocampus 17:801-12. Theory of grid cell formation.
- Wills TJ, Cacucci F, Burgess N & O’Keefe J (2010) Development of the hippocampal cognitive map in preweaning rats. Science 328:1573-1576. Development of place, head direction and grid cells in the first 3 weeks of life.
- Krupic J, Burgess N & O’Keefe J (2012) Neural representations of location composed of spatially periodic bands. Science 337: 853-857. Demonstration that grid cells are part of a larger set of spatially periodic cells and utility of Fourier analysis in describing this larger set.
- Chen G, King J, Burgess N & O'Keefe J (2013) How vision and movement combine in the hippocampal place code. Proceedings of the National Academy of Sciences 110, 378–383. Used virtual reality technology to control the activity of place cells and to demonstrate the decisive ability of landmark and path integration inputs.
- Krupic J, Bauza M, Burton S, Barry C and O’Keefe J (2015) Grid cell symmetry is shaped by environmental geometry. Nature 518(7538):232-5. doi: 10.1038/nature14153. Demonstration that grid cell symmetry can be broken by the shape of the environment , therefore placing limits on their providing the universal Cartesian metric for the cognitive map.