Slowness and Sparseness Lead to Place, Head-Direction, and Spatial-View Cells

Franzius, Mathias and Sprekeler, Henning and Wiskott, Prof. Dr. Laurenz (2007) Slowness and Sparseness Lead to Place, Head-Direction, and Spatial-View Cells. [Journal (Paginated)]

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We present a model for the self-organized formation of place cells, head-direction cells, and spatial-view cells in the hippocampal formation based on unsupervised learning on quasi-natural visual stimuli. The model comprises a hierarchy of Slow Feature Analysis (SFA) nodes, which were recently shown to reproduce many properties of complex cells in the early visual system. The system extracts a distributed grid-like representation of position and orientation, which is transcoded into a localized place-field, head-direction, or view representation, by sparse coding. The type of cells that develops depends solely on the relevant input statistics, i.e., the movement pattern of the simulated animal. The numerical simulations are complemented by a mathematical analysis that allows us to accurately predict the output of the top SFA layer

Item Type:Journal (Paginated)
Additional Information:This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Keywords:Place Cell, Head Direction Cell, Spatial View Cell, Grid Cell, SFA, Hierarchical Model, Slowness, Sparse Coding
Subjects:Neuroscience > Computational Neuroscience
Computer Science > Machine Vision
Biology > Theoretical Biology
ID Code:5711
Deposited By:Franzius, Mathias
Deposited On:12 Sep 2007
Last Modified:11 Mar 2011 08:56

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Select the SEEK icon to attempt to find the referenced article. If it does not appear to be in cogprints you will be forwarded to the paracite service. Poorly formated references will probably not work.

# Berkes P, Wiskott L (2005) Slow feature analysis yields a rich repertoire of complex cell properties. J Vision 5: 579–602. Find this article online

# 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. Find this article online

# Taube JS, Muller RU, Ranck JB (1990) Head direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 2: 420–435. Find this article online

# Hafting T, Fyhn M, Molden S, Moser M, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436: 801–806. Find this article online

# Rolls ET (1999) Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9: 467–480. Find this article online

# Rolls ET (2006) Neurophysiological and computational analyses of the primate presubiculum, subiculum and related areas. Behav Brain Res 174: 289–303. Find this article online

# Hori E, Nishio Y, Kazui K, Umeno K, Tabuchi E, et al. (2005) Place-related neural responses in the monkey hippocampal formation in a virtual space. Hippocampus 15: 991–996. Find this article online

# O'Keefe J (2007) Hippocampal neurophysiology in the behaving animal Oxford: Oxford University Press. pp. 475–548.

# Sharp EP, Blair HT, Cho J (2001) The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci 24: 289–294. Find this article online

# Taube JS, Bassett JP (2003) Persistent neural activity in head direction cells. Cereb Cortex 13: 1162–1172. Find this article online

# Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, et al. (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15: 7079–7094. Find this article online

# Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, et al. (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312: 758–762. Find this article online

# Knierim JJ, Kudrimoti HS, McNaughton BL (1995) Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15: 1648–1659. Find this article online

# Jeffery KJ, O'Keefe JM (1999) Learned interaction of visual and idiothetic cues in the control of place field orientation. Exp Brain Res 127: 151–161. Find this article online

# Save E, Nerad L, Poucet B (2000) Contribution of multiple sensory information to place field stability in hippocampal place cells. Hippocampus 10: 64–76. Find this article online

# Földiak P (1991) Learning invariance from transformation sequences. Neural Comput 3: 194–200. Find this article online

# Mitchison G (1991) Removing time variation with the anti-hebbian differential synapse. Neural Comput 3: 312–320. Find this article online

# Stone JV, Bray A (1995) A learning rule for extracting spatio-temporal invariances. Network-Comp Neural 6: 429–436. Find this article online

# Wiskott L (1998) Learning invariance manifolds. In: Niklasson L, Bodén M, Ziemke T, editors. London: Springer. pp. 555–560.

# Wiskott L, Sejnowski T (2002) Slow feature analysis: Unsupervised learning of invariances. Neural Comput 14: 715–770. Find this article online

# Olshausen BA, Field DJ (2004) Sparse coding of sensory inputs. Curr Opin Neurobiol 481–487.

# Hashimoto W (2003) Quadratic forms in natural images. Network-Comp Neural 14: 765–788. Find this article online

# Sprekeler H, Michaelis C, Wiskott L (2007) Slowness: An objective for spike-timing-plasticity? PLoS Comput Biol 3: 112. Find this article online

# Picard R, Graczyk C, Mann S, Wachman J, Picard L, et al. (2002) Vision texture Available: Accessed 25 July 2007.

# Hughes A (1978) A schematic eye for the rat. Vision Res 19: 569–588. Find this article online

# Blaschke T, Wiskott L (2004) Cubica: Independent component analysis by simultaneous third- and fourth-order cumulant diagonalization. IEEE T Signal Process 52: 1250–1256. Find this article online

# Franzius M, Vollgraf R, Wiskott L (2007) From grids to places. J Comput Neurosci 22: 297–299. Find this article online

# Berkes P, Zito T (2005) Modular toolkit for data processing (version 2.0) Available: Accessed 25 July 2007.

# Wiskott L (2003) Slow feature analysis: A theoretical analysis of optimal free responses. Neural Comput 15: 2147–2177. Find this article online

# Muller RU, Kubie JL, Ranck JB (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7: 1935–1950. Find this article online

# Muller R (1996) A quarter of a century of place cells. Neuron 17: 813–822. Find this article online

# Rolls ET, Xiang J, Franco L (2005) Object, space, and object-space representations in the primate hippocampus. J Neurophysiol 94: 833–844. Find this article online

# Muller RU, Bostock E, Taube JS, Kubie JL (1994) On the directional firing properties of hippocampal place cells. J Neurosci 14: 7235–7251. Find this article online

# Cacucci F, Lever C, Wills TJ, Burgess N, Keefe JO (2004) Theta-modulated place-by-direction cells in the hippocampal formation in the rat. J Neurosci 24: 8265–8277. Find this article online

# Sharp PE (1996) Multiple spatial/behavioral correlates for cells in the rat postsubiculum: Multiple regression analysis and comparison to other hippocampal areas. Cereb Cortex 6: 238–259. Find this article online

# Stackman RW, Zugaro MB (2005) Self-motion cues and resolving intermodality conflicts: Head direction cells, place cells, and behavior. In: Wiener SI, Taube JS Head direction cells and the neural mechanisms of spatial orientation Cambridge (Massachusetts): MIT Press. pp. 137–162.

# Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL (1995) A model of the neural basis of the rat's sense of direction. In: Tesauro G, Touretzky DS, Leen TK Advances in neural information processing systems 7 Cambridge (Massachusetts): MIT Press. pp. 173–180.

# Kayser C, Einhäuser W, Dümmer O, König P, Körding K (2001) Extracting slow subspaces from natural videos leads to complex cells. Lect Notes Comput Sci 1075–1080.

# Lörincz A, Buzsáki G (2000) Two-phase computational model training long-term memories in the entorhinal-hippocampal region. Ann N Y Acad Sci 911: 83–111. Find this article online

# Oja E, Karhunen J (1995) Signal separation by nonlinear hebbian learning. In: Palaniswami M, Attikiouzel Y, Marks RJ II, Fogel D, Fukuda T Computational intelligence: A dynamic system perspective New York: IEEE Press. pp. 83–97.

# Redish AD (1999) Beyond the cognitive map—From place cells to episodic memory Cambridge (Massachusetts): MIT Press.

# McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the “cognitive map.” Nat Rev Neurosci 7: 663–678. Find this article online

# Wyss R, König P, Verschure P (2006) A model of the ventral visual system based on temporal stability and local memory. PLoS Biology 4: 120. Find this article online

# Sharp EP (1991) Computer simulation of hippocampal place cells. Psychobiology 19: 103–115. Find this article online

# Fuhs MC, Redish AD, Touretzky DS (1998) A visually driven hippocampal place cell model. In: Bower J Computational neuroscience: Trends in research New York: Plenum Publishing. pp. 101–106.

# Brunel N, Trullier O (1998) Plasticity of directional place fields in a model of rodent CA3. Hippocampus 8: 651–665. Find this article online

# de Araujo IET, Rolls ET, Stringer SM (2001) A view model which accounts for the spatial fields of hippocampal primate spatial view cells and rat place cells. Hippocampus 11: 699–706. Find this article online

# Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7: 1951–1968. Find this article online

# Gavrilov VV, Wiener SI, Berthoz A (1998) Discharge correlates of hippocampal complex spike neurons in behaving rats passively displaced on a mobile robot. Hippocampus 8: 475–490. Find this article online

# Song EY, Kim YB, Kim YH, Jung MW (2005) Role of active movement in place-specific firing of hippocampal neurons. Hippocampus 15: 8–17. Find this article online


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