A Topological Paradigm for Hippocampal Spatial Map Formation Using Persistent Homology

PLoS Computational Biology

Volumn 8, Issue 8, 2012, Pages

  Dabaghian, Y ^a,b   Memoli F ^c,d   Frank, L ^e   Carlsson, G ^c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Rice University   (United States)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY OF ADELAIDE   (Australia)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BRAIN; COMPUTATION THEORY; TOPOLOGY;

BRAIN REGIONS; CO-FIRING; FIELD SIZE; FIRING RATES; GEOMETRIC INFORMATION; INFORMATION DISTANCE; MAP FORMATION; MENTAL MAPS; PERSISTENT HOMOLOGY; SPATIAL MAPS;

NEURONS;

ALGEBRAIC TOPOLOGY; ALGORITHM; ARTICLE; COMPUTER PROGRAM; COMPUTER SIMULATION; HIPPOCAMPAL SPATIAL MAP; HIPPOCAMPUS; LEARNING; MATHEMATICS; NERVOUS SYSTEM FUNCTION; NEURONAL FIRING; PERSISTENT HOMOLOGY THEORY; SPATIAL DISCRIMINATION; SPATIAL LEARNING; THEORY;

ANIMALIA; RATTUS;

EID: 84866088345     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002581     Document Type: Article

References (47)

1. 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.
2. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. New York: Clarendon Press; Oxford University Press. xiv, 570 pp.
3. Zhang K, Ginzburg I, McNaughton BL, Sejnowski TJ, (1998) Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J Neurophysiol 79: 1017-1044.
4. McNaughton BL, Barnes CA, O'Keefe J, (1983) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52: 41-49.
5. Brown EN, Frank LM, Tang D, Quirk MC, Wilson MA, (1998) A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J Neurosci 18: 7411-7425.
6. Best PJ, White AM, Minai A, (2001) Spatial processing in the brain: the activity of hippocampal place cells. Annu Rev Neurosci 24: 459-486.
7. O'Keefe J, Burgess N, (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381: 425-428.
8. Curto C, Itskov V, (2008) Cell groups reveal structure of stimulus space. PLoS Comput Biol 4: e1000205.
9. Igelnik B (2011) Computational modeling and simulation of intellect: current state and future perspectives. Hershey, PA: Information Science Reference. xxix, 655 p. p.
10. Hatcher A (2002) Algebraic topology. Cambridge; New York: Cambridge University Press. xii, 544 p. p.
11. 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.
12. Gothard KM, Skaggs WE, McNaughton BL, (1996) Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J Neurosci 16: 8027-8040.
13. Gothard KM, Skaggs WE, Moore KM, McNaughton BL, (1996) Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J Neurosci 16: 823-835.
14. Diba K, Buzsaki G, (2008) Hippocampal network dynamics constrain the time lag between pyramidal cells across modified environments. J Neurosci 28: 13448-13456.
15. Dubrovin BA, Fomenko AT, Novikov SP (1992) Modern geometry-methods and applications. New York: Springer-Verlag. 432 p p.
16. Buzsaki G, (2005) Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15: 827-840.
17. Buzsaki G, (2002) Theta oscillations in the hippocampus. Neuron 33: 325-340.
18. Lisman JE, (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20: 38-43.
19. Huxter JR, Senior TJ, Allen K, Csicsvari J, (2008) Theta phase-specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat Neurosci 11: 587-594.
20. O'Keefe J, Recce ML, (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3: 317-330.
21. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA, (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6: 149-172.
22. Frank LM, Stanley GB, Brown EN, (2004) Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 24: 7681-7689.
23. Davidson TJ, Kloosterman F, Wilson MA, (2009) Hippocampal replay of extended experience. Neuron 63: 497-507.
24. Zomorodian AJ (2005) Topology for computing. Cambridge, UK; New York: Cambridge University Press. xiii, 243 p. p.
25. D'Hooge R, De Deyn PP, (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 36: 60-90.
26. Morris RG, Garrud P, Rawlins JN, O'Keefe J, (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297: 681-683.
27. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, et al. (1996) Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199: 173-185.
28. Abusaad I, MacKay D, Zhao J, Stanford P, Collier DA, et al. (1999) Stereological estimation of the total number of neurons in the murine hippocampus using the optical disector. J Comp Neurol 408: 560-566.
29. Samsonovich A, McNaughton BL, (1997) Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17: 5900-5920.
30. Eckert MJ, Bilkey DK, Abraham WC, (2010) Altered plasticity in hippocampal CA1, but not dentate gyrus, following long-term environmental enrichment. J Neurophysiol 103: 3320-3329.
31. Eckert MJ, Abraham WC, (2010) Physiological effects of enriched environment exposure and LTP induction in the hippocampus in vivo do not transfer faithfully to in vitro slices. Learn Mem 17: 480-484.
32. Fenton AA, Kao HY, Neymotin SA, Olypher A, Vayntrub Y, et al. (2008) Unmasking the CA1 ensemble place code by exposures to small and large environments: more place cells and multiple, irregularly arranged, and expanded place fields in the larger space. J Neurosci 28: 11250-11262.
33. Karlsson MP, Frank LM, (2008) Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J Neurosci 28: 14271-14281.
34. Shen J, Barnes CA, McNaughton BL, Skaggs WE, Weaver KL, (1997) The effect of aging on experience-dependent plasticity of hippocampal place cells. J Neurosci 17: 6769-6782.
35. Cacucci F, Yi M, Wills TJ, Chapman P, O'Keefe J, (2008) Place cell firing correlates with memory deficits and amyloid plaque burden in Tg2576 Alzheimer mouse model. Proc Natl Acad Sci U S A 105: 7863-7868.
36. Nithianantharajah J, Hannan AJ, (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7: 697-709.
37. White AM, Best PJ, (2000) Effects of ethanol on hippocampal place-cell and interneuron activity. Brain Res 876: 154-165.
38. Matthews DB, Simson PE, Best PJ, (1996) Ethanol alters spatial processing of hippocampal place cells: a mechanism for impaired navigation when intoxicated. Alcohol Clin Exp Res 20: 404-407.
39. Moser EI Open field trajectory data is freely available from http://www.ntnu.no/cbm/moser/gridcell, data accessed in 2011.
40. Brown EN, Barbieri R, Ventura V, Kass RE, Frank LM, (2002) The time-rescaling theorem and its application to neural spike train data analysis. Neural Comput 14: 325-346.
41. Mizumori SJ (2008) Hippocampal place fields: relevance to learning and memory. Oxford; New York: Oxford University Press. xx, 409 p. p.
42. Aleksandrov PS (1965) Elementary concepts of topology. New York: F. Ungar Pub. Co. 63 p. p.
43. Munkres JR (2000) Topology. Upper Saddle River, NJ: Prentice Hall. xvi, 537 p. p.
44. Dubrovin BA, Fomenko AT, Novikov SP (1984) Modern geometry-methods and applications. New York: Springer-Verlag.
45. de Silva V, Carlsson G (2004) Topological estimation using witness complexes. In: Alexa M, and Rusinkiewicz, S., editor. Proc IEEE Eurographics Symposium on Point-Based Graphics. Zürich. pp. 157-166.
46. Edelsbrunner H, Letscher D, Zomorodian A, (2002) Topological Persistence and Simplification. Discrete Comput Geom 28: 511-533.
47. Zomorodian A, Carlsson G, (2005) Computing persistent homology. Discrete Comput Geom 33: 249-274.