To determine whether entorhinal spatial representations are continuous or fragmented, we recorded neural activity in grid cells while rats ran through a stack of interconnected, zig-zagged compartments of equal shape and orientation (a hairpin maze). The distribution of spatial firing fields was markedly similar across all compartments in which running occurred in the same direction, implying that the grid representation was fragmented into repeating submaps. Activity at neighboring positions was least correlated at the transitions between different arms, indicating that the map split regularly at the turning points. We saw similar discontinuities among place cells in the hippocampus. No fragmentation was observed when the rats followed similar trajectories in the absence of internal walls, implying that stereotypic behavior alone cannot explain the compartmentalization. These results indicate that spatial environments are represented in entorhinal cortex and hippocampus as a mosaic of discrete submaps that correspond to the geometric structure of the space.
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O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971).
O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford University Press, New York, 1978).
Muller, R.U., Kubie, J.L. & Ranck, J.B. Jr. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935–1950 (1987).
Wilson, M.A. & McNaughton, B.L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055–1058 (1993).
Kjelstrup, K.B. et al. Finite scale of spatial representation in the hippocampus. Science 321, 140–143 (2008).
Leutgeb, S., Leutgeb, J.K., Treves, A., Moser, M.B. & Moser, E.I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 1295–1298 (2004).
Bostock, E., Muller, R.U. & Kubie, J.L. Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1, 193–205 (1991).
Colgin, L.L., Moser, E.I. & Moser, M.B. Understanding memory through hippocampal remapping. Trends Neurosci. 31, 469–477 (2008).
Muller, R.U. & Kubie, J.L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951–1968 (1987).
Wood, E.R., Dudchenko, P.A. & Eichenbaum, H. The global record of memory in hippocampal neuronal activity. Nature 397, 613–616 (1999).
Pastalkova, E., Itskov, V., Amarasingham, A. & Buzsaki, G. Internally generated cell assembly sequences in the rat hippocampus. Science 321, 1322–1327 (2008).
Hampson, R.E., Heyser, C.J. & Deadwyler, S.A. Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat. Behav. Neurosci. 107, 715–739 (1993).
Wood, E.R., Dudchenko, P.A., Robitsek, R.J. & Eichenbaum, H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623–633 (2000).
Frank, L.M., Brown, E.N. & Wilson, M. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169–178 (2000).
Markus, E.J. et al. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci. 15, 7079–7094 (1995).
Young, B.J., Fox, G.D. & Eichenbaum, H. Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task. J. Neurosci. 14, 6553–6563 (1994).
Touretzky, D.S. & Redish, A.D. Theory of rodent navigation based on interacting representations of space. Hippocampus 6, 247–270 (1996).
Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M. & Tanila, H. The hippocampus, memory and place cells: is it spatial memory or a memory space? Neuron 23, 209–226 (1999).
Sharp, P.E. Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: Comparison with hippocampal place cells. Behav. Brain Res. 85, 71–92 (1997).
Taube, J.S. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181–207 (2007).
Taube, J.S., Muller, R.U. & Ranck, J.B. Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420–435 (1990).
Ranck, J.B. Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. in Electrical Activity of the Archicortex (eds G. Buzsaki & C.H. Vanderwolf) 217–220 (Akademiai Kiado, Budapest, 1985).
Sargolini, F. et al. Conjunctive representation of position, direction and velocity in entorhinal cortex. Science 312, 758–762 (2006).
Fyhn, M., Molden, S., Witter, M.P., Moser, E.I. & Moser, M.B. Spatial representation in the entorhinal cortex. Science 305, 1258–1264 (2004).
Hafting, T., Fyhn, M., Molden, S., Moser, M.B. & Moser, E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806 (2005).
Taube, J.S., Muller, R.U. & Ranck, J.B. Head-direction cells recorded from the postsubiculum in freely moving rats. 2. Effects of environmental manipulations. J. Neurosci. 10, 436–447 (1990).
Johnson, A., Seeland, K. & Redish, A.D. Reconstruction of the postsubiculum head direction signal from neural ensembles. Hippocampus 15, 86–96 (2005).
Hargreaves, E.L., Yoganarasimha, D. & Knierim, J.J. Cohesiveness of spatial and directional representations recorded from neural ensembles in the anterior thalamus, parasubiculum, medial entorhinal cortex and hippocampus. Hippocampus 17, 826–841 (2007).
Yoganarasimha, D., Yu, X. & Knierim, J.J. Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J. Neurosci. 26, 622–631 (2006).
Fyhn, M., Hafting, T., Treves, A., Moser, M.B. & Moser, E.I. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446, 190–194 (2007).
Moser, E.I. & Moser, M.B. A metric for space. Hippocampus 18, 1142–1156 (2008).
Redish, A.D., McNaughton, B.L. & Barnes, C.A. Place cell firing shows an inertia-like process. Neurocomputing 32, 235–241 (2000).
McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I. & Moser, M.B. Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663–678 (2006).
McNaughton, B.L., Barnes, C.A. & O'Keefe, J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely moving rats. Exp. Brain Res. 52, 41–49 (1983).
Hafting, T., Fyhn, M., Bonnevie, T., Moser, M.B. & Moser, E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 453, 1248–1252 (2008).
Hasselmo, M.E. Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18, 1213–1229 (2008).
O'Keefe, J. & Burgess, N. Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425–428 (1996).
Barry, C., Hayman, R., Burgess, N. & Jeffery, K.J. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10, 682–684 (2007).
Cheng, K. A purely geometric module in the rat's spatial representation. Cognition 23, 149–178 (1986).
McGregor, A., Hayward, A.J., Pearce, J.M. & Good, M.A. Hippocampal lesions disrupt navigation based on the shape of the environment. Behav. Neurosci. 118, 1011–1021 (2004).
Jones, P.M., Pearce, J.M., Davies, V.J., Good, M.A. & McGregor, A. Impaired processing of local geometric features during navigation in a water maze following hippocampal lesions in rats. Behav. Neurosci. 121, 1258–1271 (2007).
Pearce, J.M., Good, M.A., Jones, P.M. & McGregor, A. Transfer of spatial behavior between different environments: implications for theories of spatial learning and for the role of the hippocampus in spatial learning. J. Exp. Psychol. Anim. Behav. Process. 30, 135–147 (2004).
Gothard, K.M., Skaggs, W.E. & McNaughton, B.L. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J. Neurosci. 16, 8027–8040 (1996).
Redish, A.D., Rosenzweig, E.S., Bohanick, J.D., McNaughton, B.L. & Barnes, C.A. Dynamics of hippocampal ensemble activity realignment: time versus space. J. Neurosci. 20, 9298–9309 (2000).
Biegler, R. Possible uses of path integration in animal navigation. Anim. Learn. Behav. 28, 257–277 (2000).
Samsonovich, A. & McNaughton, B.L. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900–5920 (1997).
McNaughton, B.L. et al. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol. 199, 173–185 (1996).
Whishaw, I.Q. Place learning in hippocampal rats and the path integration hypothesis. Neurosci. Biobehav. Rev. 22, 209–220 (1998).
Solstad, T., Boccara, C., Kropff, E., Moser, M.B. & Moser, E.I. Representation of geometric borders in the entorhinal cortex. Science 322, 1865–1868 (2008).
Savelli, F., Yoganarasimha, D. & Knierim, J.J. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 1270–1282 (2008).
We thank A.M. Amundgård, I. Hammer, K. Haugen, K. Jenssen, R. Skjerpeng and H. Waade for technical assistance and T. Bonnevie and G. Pfühl for help with animal training. We thank A.D. Redish and members of the Kavli Institute for Systems Neuroscience and the Centre for the Biology of Memory for useful discussions. This work was supported by the Kavli Foundation and a Centre of Excellence grant from the Norwegian Research Council.
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Derdikman, D., Whitlock, J., Tsao, A. et al. Fragmentation of grid cell maps in a multicompartment environment. Nat Neurosci 12, 1325–1332 (2009). https://doi.org/10.1038/nn.2396
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