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ANRV346-NE31-04 ARI 14 May 2008 7:9 ANNUAL Place Cells, Grid Cells, REVIEWS Further Click here for quick links to Annual Reviews content online, and the Brain’s Spatial including: • Other articles in this volume Representation System • Top cited articles • Top downloaded articles • Our comprehensive search Edvard I. Moser,1 Emilio Kropff,1,2 and May-Britt Moser1 1Kavli Institute for Systems Neuroscience and Centre for the Biology of Memory, Norwegian University of Science and Technology, 7489 Trondheim, Norway 2Cognitive Neuroscience Sector, International School for Advanced Studies, Trieste, Italy; email: [email protected] Annu. Rev. Neurosci. 2008. 31:69–89 Key Words Annu. Rev. Neurosci. 2008.31:69-89. Downloaded from www.annualreviews.org First published online as a Review in Advance on hippocampus, entorhinal cortex, path integration, attractor, memory, Access provided by University of Arizona - Library on 03/10/15. For personal use only. February 19, 2008 phase precession The Annual Review of Neuroscience is online at neuro.annualreviews.org Abstract This article’s doi: More than three decades of research have demonstrated a role for 10.1146/annurev.neuro.31.061307.090723 hippocampal place cells in representation of the spatial environment in Copyright c 2008 by Annual Reviews. the brain. New studies have shown that place cells are part of a broader All rights reserved circuit for dynamic representation of self-location. A key component of 0147-006X/08/0721-0069$20.00 this network is the entorhinal grid cells, which, by virtue of their tessel- lating firing fields, may provide the elements of a path integration–based neural map. Here we review how place cells and grid cells may form the basis for quantitative spatiotemporal representation of places, routes, and associated experiences during behavior and in memory. Because these cell types have some of the most conspicuous behavioral correlates among neurons in nonsensory cortical systems, and because their spatial firing structure reflects computations internally in the system, studies of entorhinal-hippocampal representations may offer considerable insight into general principles of cortical network dynamics. 69 ANRV346-NE31-04 ARI 14 May 2008 7:9 past three decades that indicates the presence Contents of a preconfigured or semipreconfigured brain system for representation and storage of self- INTRODUCTION .................. 70 location relative to the external environment. PLACE CELLS AND THE In agreement with the general ideas of Kant, HIPPOCAMPAL MAP ............ 70 place cells and grid cells in the hippocampal GRID CELLS AND THE and entorhinal cortices may determine how we ENTORHINAL MAP ............. 71 perceive and remember our position in the en- SENSORY CUES AND PATH vironment as well as the events we experience INTEGRATION .................. 72 in that environment. THEORETICAL MODELS OF GRID FORMATION.......... 72 PLACE FIELDS MAY BE PLACE CELLS AND THE EXTRACTED FROM HIPPOCAMPAL MAP GRID FIELDS .................... 75 The experimental study of spatial representa- PLACE CELLS AND tions in the brain began with the discovery of HIPPOCAMPAL MEMORY ...... 76 place cells. More than 35 years ago, O’Keefe SEQUENCE CODING IN PLACE & Dostrovsky (1971) reported spatial recep- CELLS AND GRID CELLS ...... 78 tive fields in complex-spiking neurons in the rat REPLAY AND PREPLAY IN PLACE hippocampus, which are likely to be pyramidal CELL ENSEMBLES .............. 79 cells (Henze et al. 2000). These place cells fired SPATIAL MAPS INCLUDE MORE whenever the rat was in a certain place in the THAN HIPPOCAMPUS AND local environment (the place field of the cell; ENTORHINAL CORTEX ........ 80 Figure 1a). Neighboring place cells fired at dif- DEVELOPMENT OF THE ferent locations such that, throughout the hip- SPATIAL REPRESENTATION pocampus, the entire environment was repre- SYSTEM.......................... 80 sented in the activity of the local cell population CONCLUSION ..................... 81 (O’Keefe 1976, Wilson & McNaughton 1993). The same place cells participated in represen- Annu. Rev. Neurosci. 2008.31:69-89. Downloaded from www.annualreviews.org tations for different environments, but the re- Access provided by University of Arizona - Library on 03/10/15. For personal use only. lationship of the firing fields differed from one INTRODUCTION setting to the next (O’Keefe & Conway 1978). Questions about how we perceive space and Inspired by Tolman(1948), who suggested that our place in that space have engaged episte- local navigation is guided by internal “cognitive mologists for centuries. Although the British maps” that flexibly represent the overall spa- empiricists of the seventeenth and eighteenth tial relationships between landmarks in the en- centuries thought that all knowledge about the vironment, O’Keefe & Nadel (1978) proposed world was ultimately derived from sensory im- that place cells are the basic elements of a dis- pressions, Kant argued that some ideas exist as a tributed noncentered map-like representation. priori intuitions, independent of specific experi- Place cells were suggested to provide the ani- ence. One of these ideas is the concept of space, mal with a dynamic, continuously updated rep- which he considered an innate organizing prin- resentation of allocentric space and the animal’s ciple of the mind, through which the world is, own position in that space. We now have abun- and must be, perceived. With the birth of exper- dant evidence from a number of mammalian imental psychology and neuroscience a century species demonstrating that the hippocampus later, the organization and development of spa- plays a key role in spatial representation tial behavior and cognition could be analyzed and spatial memory (Nadel 1991, Rolls 1999, experimentally. We review evidence from the Ekstrom et al. 2003, Ulanovsky & Moss 2007), 70 Moser · Kropff · Moser ANRV346-NE31-04 ARI 14 May 2008 7:9 although new evidence suggests that position is ab only one of several facets of experience stored in the hippocampal network (Eichenbaum et al. 1999, Leutgeb et al. 2005b). GRID CELLS AND THE ENTORHINAL MAP All subfields of the hippocampal region con- tain place-modulated neurons, but the most distinct firing fields are found in the CA ar- eas (Barnes et al. 1990). On the basis of the apparent amplification of spatial signals from Figure 1 the entorhinal cortex to the CA fields (Quirk Place cell in the hippocampus (a) and grid cell in the medial entorhinal cortex (MEC) ( ). Spike locations ( ) are superimposed on the animal’s trajectory in et al. 1992), many investigators thought, until b red the recording enclosure (black). Whereas most place cells have a single firing recently, that place signals depended primarily location, the firing fields of a grid cell form a periodic triangular matrix tiling on computations within the hippocampal net- the entire environment available to the animal. work. This view was challenged by the observa- tion that spatial firing persisted in CA1 neurons after removal of intrahippocampal inputs from nal reference axis), and phase (xy displacement the dentate gyrus (McNaughton et al. 1989) and relative to an external reference point). Al- CA3 (Brun et al. 2002). This raised the possibil- though cells in the same part of the MEC ity that spatial signals were conveyed to CA1 by have similar grid spacing and grid orientation, the direct perforant-path projections from layer the phase of the grid is nontopographic, i.e., III of the entorhinal cortex. Projection neurons the firing vertices of colocalized grid cells ap- in layers II and III of the medial entorhinal cor- pear to be shifted randomly, just like the fields tex (MEC) were subsequently shown to exhibit of neighboring place cells in the hippocam- sharply tuned spatial firing, much like place cells pus. The spacing increases monotonically from in the hippocampus, except that each cell had dorsomedial to ventrolateral locations in MEC Annu. Rev. Neurosci. 2008.31:69-89. Downloaded from www.annualreviews.org multiple firing fields (Fyhn et al. 2004). The (Hafting et al. 2005, Solstad et al. 2007), mir- Access provided by University of Arizona - Library on 03/10/15. For personal use only. many fields of each neuron formed a periodic roring the increase in size of place fields along triangular array, or grid, that tiled the entire the dorsoventral axis of the hippocampus ( Jung environment explored by the animal (Hafting et al. 1994, Maurer et al. 2005, Kjelstrup et al. et al. 2005) (Figure 1b). Such grid cells collec- 2007). Cells in different parts of the MEC may tively signaled the rat’s changing position with also have different grid orientations (Hafting a precision similar to that of place cells in the et al. 2005), but the underlying topography, if hippocampus (Fyhn et al. 2004). The graphics there is one, has not been established. Thus, paper–like shape of the grid immediately indi- we do not know whether the entorhinal map cated grid cells as possible elements of a met- has discrete subdivisions. The entorhinal cor- ric system for spatial navigation (Hafting et al. tex has several architectonic features sugges- 2005), with properties similar to that of the al- tive of a modular arrangement, such as periodic locentric map proposed for the hippocampus bundling of pyramidal cell dendrites and axons more than 25 years earlier (O’Keefe & Nadel and cyclic variations in the density of immuno- 1978). cytochemical markers (Witter & Moser 2006), How do grid representations map onto the but whether the anatomical cell
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