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Cshperspect-LNM-A021808 1..15 Downloaded from http://cshperspectives.cshlp.org/ at FACHBIBLIOTHEK KLINIKUM on October 25, 2015 - Published by Cold Spring Harbor Laboratory Press Place Cells, Grid Cells, and Memory May-Britt Moser, David C. Rowland, and Edvard I. Moser Centre for Neural Computation, Kavli Institute for Systems Neuroscience, Norwegian University of Science and Technology, 7489 Trondheim, Norway Correspondence: [email protected] The hippocampal system is critical for storage and retrieval of declarative memories, includ- ing memories for locations and events that take place at those locations. Spatial memories place high demands on capacity. Memories must be distinct to be recalled without interfer- ence and encoding must be fast. Recent studies have indicated that hippocampal networks allow for fast storage of large quantities of uncorrelated spatial information. The aim of the this article is to review and discuss some of this work, taking as a starting point the discovery of multiple functionally specialized cell types of the hippocampal–entorhinal circuit, such as place, grid, and border cells. We will show that grid cells provide the hippocampus with a metric, as well as a putative mechanism for decorrelation of representations, that the forma- tion of environment-specific place maps depends on mechanisms for long-term plasticity in the hippocampus, and that long-term spatiotemporal memory storage may depend on offline consolidation processes related to sharp-wave ripple activity in the hippocampus. The mul- titude of representations generated through interactions between a variety of functionally specialized cell types in the entorhinal–hippocampal circuit may be at the heart of the mechanism for declarative memory formation. he scientific study of human memory started Tolman, a rigorous program for identifying the Twith Herman Ebbinghaus, who initiated the laws of animal learning was initiated. By the quantitative investigation of associative mem- middle of the 20th century, a language for asso- ory processes as they take place (Ebbinghaus ciative learning processes had been developed, 1885). Ebbinghaus described the conditions and many of the fundamental relationships be- that influence memory formation and he deter- tween environment and behavior had been de- mined several basic principles of encoding and scribed. What was completely missing, though, recall, such as the law of frequency and the effect was an understanding of the neural activity of time on forgetting. With Ebbinghaus, higher underlying the formation of the memory. The mental functions were brought to the laborato- behaviorists had deliberately shied away from ry. In parallel with the human learning tradition physiological explanations because of the in- that Ebbinghaus started, a new generation of tangible nature of neural activity at that time. experimental psychologists described the laws Then the climate began to change. Karl of associative learning in animals. With behav- Lashley had shown that lesions in the cerebral iorists like Pavlov, Watson, Hull, Skinner, and cortex had predictable effects on behavior in Editors: Eric R. Kandel, Yadin Dudai, and Mark R. Mayford Additional Perspectives on Learning and Memory available at www.cshperspectives.org Copyright # 2015 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a021808 Cite this article as Cold Spring Harb Perspect Biol 2015;7:a021808 1 Downloaded from http://cshperspectives.cshlp.org/ at FACHBIBLIOTHEK KLINIKUM on October 25, 2015 - Published by Cold Spring Harbor Laboratory Press M.-B. Moser et al. animals (Lashley 1929, 1950), and Donald Hebb grid, border, and head direction cells, each with introduced concepts and ideas to account for distinct roles in the representation of space and complex brain functions at the neural circuit spatial memory. In this article, we shall discuss level, many of which have retained a place in potential mechanisms by which these cell types, modern neuroscience (Hebb 1949). Both Lash- particularly place and grid cells, in conjunction ley and Hebb searched for the engram, but with synaptic plasticity, may form the basis of a they found no specific locus for it. A significant mammalian system for fast high-capacity de- turning point was reached when Scoville and clarative memory. Milner (1957) reported severe loss of memory in an epileptic patient, patient H.M., after bilat- PLACE CELLS, SYNAPTIC PLASTICITY, eral surgical removal of the hippocampal for- AND MEMORY mation and the surrounding medial temporal lobe areas. “After operation this young man The growing interest in hippocampal function could no longer recognize the hospital staff and memory led John O’Keefe and John Dos- nor find his way to the bathroom, and he seemed trovsky (O’Keefe and Dostrovsky 1971) and Jim to recall nothing of the day-to-day events of his Ranck (Ranck 1973) to introduce methods for hospital life.”This tragic misfortune inspired de- recording activity from hippocampal neurons cades of research on the function of the hippo- in awake and freely moving animals. Using min- campus in memory. H.M.’s memory impair- iaturized electrodes for extracellular single-cell ment could be reproduced in memory tasks in recording, they were able to show reliable links animals and studies of H.M., as well as labora- between neural activity and behavior. The most tory animals, pointed to a critical role for the striking relationship was noted by O’Keefe and hippocampus in declarative memory—memo- Dostrovsky, who found that hippocampal cells ry, which, in humans, can be consciously re- responded specifically to the current location of called and declared, such as memories of expe- the animal. They called these cells “place cells” riences and facts (Milner et al. 1968; Mishkin (Fig. 1). Different place cells were found to have 1978; Cohen and Squire 1980; Squire 1992; Cor- different firing locations,or placefields (O’Keefe kin 2002). What was missing from these early 1976). Place was mapped nontopographically in studies, however, was a way to address the neu- the sense that place fields of neighboring cells ronal mechanisms that led information to be were no more similar than those of cells that stored as memory. were far apart (O’Keefe 1976; Wilson and Mc- The aim of this article is to show how studies Naughton 1993), although the size of the fir- of hippocampal neuronal activity during the ing fields increased from dorsal to ventral hip- past few decades have brought us to a point at pocampus (Jung et al. 1994; Kjelstrup et al. which a mechanistic basis of memory forma- 2008). The combination of cells that were active tion is beginning to surface. An early landmark at each location in the environment was unique, in this series of investigations was the discovery despite the lack of location topography, leading of place cells, cells that fire selectively at one or O’Keefe and Nadel (1978) to suggest that the few locations in the environment. At first, these hippocampus is the locus of the brain’s internal cells seemed to be part of the animal’s instanta- map of the spatial environment, a manifestation neous representation of location, independent of the cognitive map proposed from purely be- of memory, but gradually, over the course of havioral experiments by Edward Tolmanseveral several decades, it has become clear that place decades earlier (Tolman 1948). cells express current as well as past and future The discovery of place cells changed the way locations. In many ways, place cells can be used many experimental neuroscientists thought as readouts of the memories that are stored in about hippocampal functions. Clinical studies the hippocampus. More recent work has also starting with patient H.M. pointed to a role shown that place cells are part of a wider net- for the hippocampus in declarative memory work of spatially modulated neurons, including (Squire 1992), but the fact that hippocampal 2 Cite this article as Cold Spring Harb Perspect Biol 2015;7:a021808 Downloaded from http://cshperspectives.cshlp.org/ at FACHBIBLIOTHEK KLINIKUM on October 25, 2015 - Published by Cold Spring Harbor Laboratory Press Place Cells, Grid Cells, and Memory Grid Place Figure 1. Grid cells and place cells. (Left) A grid cell from the entorhinal cortex of the rat brain. The black trace shows the trajectory of a foraging rat in part of a 1.5-m-diameter-wide square enclosure. Spike locations of the grid cell are superimposed in red on the trajectory. Each red dot corresponds to one spike. Blue equilateral triangles have been drawn on top of the spike distribution to illustrate the regular hexagonal structure of the grid pattern. (Right) Grid cell and place cell. (Top) Trajectory with spike locations, as in the left part. (Bottom) Color- coded rate map with red showing high activity and blue showing low activity. Grid cells are thought to provide much, but not all, of the entorhinal spatial input to place cells. neurons were so strongly modulated by location many semantic memories (Buzsa´ki and Moser suggested that space was primary. Moreover, for 2013). the most part, place cells represented current A role for place cells in hippocampal mem- space, not as expected if the function of the hip- ory was apparent already in the earliest studies pocampus was purely mnemonic. Reconciling of place cells. It was shown in these studies that space and memory functions remained a chal- ensembles of place cells represent not only the lenge for several decades after the discovery of animal’s current location but also locations that place cells. the animal had visited earlier. In maze tasks, A framework that accounts for both lines of place cells fired when the animal made errors, observation has now emerged. Converging evi- as if the animal was in the location where the cell dence has suggested that hippocampal neurons fired normally (O’Keefe and Speakman 1987). respond also to nonspatial features of the envi- In spatial alternation tasks, firing patterns re- ronment, such as odors (Eichenbaum et al.
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