Unveiling the metric structure of internal representations of space

Frontiers in Neural Circuits

Volumn , Issue APR 2013, 2013, Pages

  Stella, Federico ^a   Cerasti, Erika ^b   Treves, Alessandro ^a  

^a SISSA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

CA3; Decoding; Information theory; Metric space; Neural network; Place cells; Spatial representations

Indexed keywords

ALGORITHM; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DEPTH PERCEPTION; HIPPOCAMPAL CA3 REGION; METRIC SYSTEM; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NORMAL DISTRIBUTION; PERCEPTIVE THRESHOLD; QUANTITATIVE ANALYSIS; SIMULATION; STIMULUS RESPONSE;

EID: 84876036768     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00081     Document Type: Article

References (52)

1. Amaral, D., Ishizuka, N., and Claiborne, B. (1990). Neurons, numbers and the hippocampal network. Progress in brain research 83, 1-11.
2. Averbeck, B., Latham, P., and Pouget, A. (2006). Neural correlations, population coding and computation. Nature reviews. Neuroscience 7, 358-366.
3. Battaglia, F.P., and Treves, A. (1998). Attractor neural networks storing multiple space representations: a model for hippocampal place fields. Physical Review E 58, 7738.
4. Brown, E., Frank, L., Tang, D., Quirk, M., and Wilson, M. (1998). A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. The Journal of neuroscience: the official journal of the Society for Neuroscience 18, 7411-7425.
5. Cerasti, E., and Treves, A. (2010). How informative are spatial CA3 representations established by the dentate gyrus? PLoS computational biology 6.
6. Ciaramelli, E., Lauro-Grotto, R., and Treves, A. (2006). Dissociating episodic from semantic access mode by mutual information measures: evidence from aging and Alzheimer's disease. Journal of physiology, Paris 100, 142-153.
7. Colgin, L., Leutgeb, S., Jezek, K., Leutgeb, J., Moser, E., Mcnaughton, B., and Moser, M.-B. (2010). Attractor-map versus autoassociation based attractor dynamics in the hippocampal network. Journal of neurophysiology 104, 35-50.
8. Curto, C., and Itskov, V. (2008). Cell groups reveal structure of stimulus space. PLoS computational biology 4.
9. Dabaghian, Y., Memoli, F., Frank, L., and Carlsson, G. (2012). A topological paradigm for hippocampal spatial map formation using persistent homology. PLoS computational biology 8.
10. Deneve, S., Latham, P., and Pouget, A. (1999). Reading population codes: a neural implementation of ideal observers. Nature neuroscience 2, 740-745.
11. Dragoi, G., and Tonegawa, S. (2011). Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469, 397-401.
12. Eichenbaum, H., Sauvage, M., Fortin, N., Komorowski, R., and Lipton, P. (2011). Towards a functional organization of episodic memory in the medial temporal lobe. Neuroscience and biobehavioral reviews.
13. Golomb, D., Hertz, J., Panzeri, S., Treves, A., and Richmond, B. (1997). How well can we estimate the information carried in neuronal responses from limited samples? Neural computation 9, 649-665.
14. Gupta, A., Van Der Meer, M.A., Touretzky, D., and Redish, A. (2010). Hippocampal replay is not a simple function of experience. Neuron 65, 695-705.
15. Hamaguchi, K., Hatchett, J., and Okada, M. (2006). Analytic solution of neural network with disordered lateral inhibition. Physical review. E, Statistical, nonlinear, and soft matter physics 73, 51104.
16. Hayman, R., Verriotis, M., Jovalekic, A., Fenton, A., and Jeffery, K. (2011). Anisotropic encoding of three-dimensional space by place cells and grid cells. Nature neuroscience 14, 1182-1188.
17. Kali, S., and Dayan, P. (2000). The involvement of recurrent connections in area CA3 in establishing the properties of place fields: a model. The Journal of neuroscience: the official journal of the Society for Neuroscience 20, 7463-7477.
18. Komorowski, R., Manns, J., and Eichenbaum, H. (2009). Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. The Journal of neuroscience: the official journal of the Society for Neuroscience 29, 9918-9929.
19. Kropff, E., and Treves, A. (2008). The emergence of grid cells: Intelligent design or just adaptation? Hippocampus 18, 1256-1269.
20. Lassalle, J., Bataille, T., and Halley, H. (2000). Reversible inactivation of the hippocampal mossy fiber synapses in mice impairs spatial learning, but neither consolidation nor memory retrieval, in the Morris navigation task. Neurobiology of learning and memory 73, 243-257.
21. Lauro-Grotto, R., Ciaramelli, E., Piccini, C., and Treves, A. (2007). Differential impact of brain damage on the access mode to memory representations: an information theoretic approach. The European journal of neuroscience 26, 2702-2712.
22. Lee, I., and Kesner, R. (2004). Encoding versus retrieval of spatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 14, 66-76.
23. Leutgeb, J., Leutgeb, S., Moser, M.-B., and Moser, E. (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science (New York, N.Y.) 315, 961-966.
24. Leutgeb, S., Leutgeb, J., Barnes, C., Moser, E., Mcnaughton, B., and Moser, M.-B. (2005). Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science (New York, N.Y.) 309, 619-623.
25. Mcnaughton, B., Battaglia, F., Jensen, O., Moser, E., and Moser, M.-B. (2006). Path integration and the neural basis of the 'cognitive map'. Nature reviews. Neuroscience 7, 663-678.
26. Morris, R., Garrud, P., Rawlins, J., and O'keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683.
27. Muller, R., and Stead, M. (1996). Hippocampal place cells connected by Hebbian synapses can solve spatial problems. Hippocampus 6, 709-719.
28. Muller, R., Stead, M., and Pach, J. (1996). The hippocampus as a cognitive graph. The Journal of general physiology 107, 663-694.
29. Naya, Y., and Suzuki, W. (2011). Integrating what and when across the primate medial temporal lobe. Science (New York, N.Y.) 333, 773-776.
30. O'keefe, J., and Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain research 34, 171-175.
31. Panzeri, S., Senatore, R., Montemurro, M., and Petersen, R. (2007). Correcting for the sampling bias problem in spike train information measures. Journal of neurophysiology 98, 1064-1072.
32. Papp, G., Witter, M., and Treves, A. (2007). The CA3 network as a memory store for spatial representations. Learning & memory (Cold Spring Harbor, N.Y.) 14, 732-744.
33. Park, E., Dvorak, D., and Fenton, A. (2011). Ensemble place codes in hippocampus: CA1, CA3, and dentate gyrus place cells have multiple place fields in large environments. PloS one 6.
34. Quian Quiroga, R., and Panzeri, S. (2009). Extracting information from neuronal populations: information theory and decoding approaches. Nature reviews. Neuroscience 10, 173-185.
35. Quiroga, R., Reddy, L., Kreiman, G., Koch, C., and Fried, I. (2005). Invariant visual representation by single neurons in the human brain. Nature 435, 1102-1107.
36. Rolls, E., and Treves, A. (2011). The neuronal encoding of information in the brain. Progress in neurobiology 95, 448-490.
37. Roudi, Y., and Treves, A. (2008). Representing where along with what information in a model of a cortical patch. PLoS computational biology 4.
38. Sammon Jr, J.W. (1969). A nonlinear mapping for data structure analysis. Computers, IEEE Transactions on 100, 401-409.
39. Samsonovich, A., and Mcnaughton, B. (1997). Path integration and cognitive mapping in a continuous attractor neural network model. The Journal of neuroscience: the official journal of the Society for Neuroscience 17, 5900-5920.
40. Singer, A., Karlsson, M., Nathe, A., Carr, M., and Frank, L. (2010). Experience-dependent development of coordinated hippocampal spatial activity representing the similarity of related locations. The Journal of neuroscience: the official journal of the Society for Neuroscience 30, 11586-11604.
41. Stringer, S., Trappenberg, T., Rolls, E., and De Araujo, I. (2002). Self-organizing continuous attractor networks and path integration: one-dimensional models of head direction cells. Network (Bristol, England) 13, 217-242.
42. Tort, A., Komorowski, R., Kopell, N., and Eichenbaum, H. (2011). A mechanism for the formation of hippocampal neuronal firing patterns that represent what happens where. Learning & memory (Cold Spring Harbor, N.Y.) 18, 718-727.
43. Treves (1990). Graded-response neurons and information encodings in autoassociative memories. Physical review. A 42, 2418-2430.
44. Treves, A. (1997). On the perceptual structure of face space. Bio Systems 40, 189-196.
45. Treves, A., Georges-Francois, P., and Panzeri, S. (1998). The metric content of spatial views as represented in the primate hippocampus. NATO ASI SERIES F
46. Treves, A., and Rolls, E. (1992). Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2, 189-199.
47. Tsodyks, M., and Sejnowski, T. (1995). Associative memory and hippocampal place cells. International journal of neural systems 6, 81-86.
48. Ulanovsky, N., and Moss, C. (2011). Dynamics of hippocampal spatial representation in echolocating bats. Hippocampus 21, 150-161.
49. Van Strien, N., Cappaert, N., and Witter, M. (2009). The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nature reviews. Neuroscience 10, 272-282.
50. Wills, T., Lever, C., Cacucci, F., Burgess, N., and O'keefe, J. (2005). Attractor dynamics in the hippocampal representation of the local environment. Science (New York, N.Y.) 308, 873-876.
51. Wilson, M., and Mcnaughton, B. (1993). Dynamics of the hippocampal ensemble code for space. Science (New York, N.Y.) 261, 1055-1058.
52. Wood, E., Dudchenko, P., Robitsek, R., and Eichenbaum, H. (2000). Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623-633.