How Entorhinal Grid Cells May Learn Multiple Spatial Scales from a Dorsoventral Gradient of Cell Response Rates in a Self-organizing Map

PLoS Computational Biology

Volumn 8, Issue 10, 2012, Pages

  Grossberg, Stephen ^a   Pilly, Praveen K ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CONFORMAL MAPPING; CYTOLOGY; SELF ORGANIZING MAPS; SURVEYS;

ENTORHINAL CORTEX; GRID CELLS; HEXAGONAL GRID; LEARN+; MEMBRANE POTENTIAL OSCILLATIONS; MULTIPLE SCALE; PLACE CELL; RESPONSE RATE; SELF-ORGANIZING-MAPS; SPATIAL SCALE;

CELLS;

EID: 84868103019     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002648     Document Type: Article

References (101)

1. Dowding JE, Murphy EC, (1994) Ecology of ship rats (Rattus rattus) in a Kauri (Agathis australis) forest in Northland, New Zealand. NZ J Ecol 18: 19-28.
2. van Strien NM, Cappaert NLM, Witter MP, (2009) The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 10: 272-282.
3. Fyhn M, Molden S, Witter MP, Moser EI, et al. (2004) Spatial representation in the entorhinal cortex. Science 305: 1258-1264.
4. Sargolini F, Fyhn M, Hafting T, McNaughton B, Witter M, et al. (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 321: 58-762.
5. Hafting T, Fyhn M, Molden S, Moser MB, Moser E, (2005) Microstructure of the spatial map in the entorhinal cortex. Nature 436: 801-806.
6. Brun VH, Solstad T, Kjelstrup KB, Fyhn M, Witter MP, et al. (2008) Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18: 1200-1212.
7. O'Keefe J, Burgess N, (2005) Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells. Hippocampus 15: 853-866.
8. Fuhs MC, Touretzky DS, (2006) A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26: 4266-4276.
9. 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.
10. Rolls ET, Stringer SM, Elliot T, (2006) Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Network 17: 447-465.
11. Gorchetchnikov A, Grossberg S, (2007) Space, time, and learning in the hippocampus: How fine spatial and temporal scales are expanded into population codes for behavioral control. Neural Net 20: 182-193.
12. Alonso A, Klink R, (1993) Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J Neurophysiol 70: 128-143.
13. Giocomo L, Zilli E, Fransen E, Hasselmo ME, (2007) Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315: 1719-1722.
14. Yoshida M, Giocomo LM, Boardman I, Hasselmo ME, (2011) Frequency of subthreshold oscillations at different membrane potential voltages in neurons at different anatomical positions on the dorsoventral axis in the rat medial entorhinal cortex. J Neurosci 31: 12683-12694.
15. Giocomo LM, Hasselmo ME, (2008) Time constants of h current in layer II stellate cells differ along the dorsal to ventral axis of medial entorhinal cortex. J Neurosci 28: 9414-9425.
16. Giocomo LM, Hasselmo ME, (2008) Computation by oscillations: Implications of experimental data for theoretical models of grid cells. Hippocampus 18: 1186-1199.
17. Nolan MF, Dudman JT, Dodson PD, Santoro B, (2007) HCN1 channels control resting and active integrative properties of stellate cells from layer II of the entorhinal cortex. J Neurosci 27: 12440-12451.
18. Giocomo LM, Hasselmo ME, (2009) Knock-out of HCN1 subunit flattens dorsal-ventral frequency gradient of medial entorhinal neurons in adult mice. J Neurosci 29: 7625-7630.
19. Garden DLF, Dodson PD, O'Donnell C, White MD, Nolan MF, (2008) Tuning of synaptic integration in the medial entorhinal cortex to the organization of grid cell firing fields. Neuron 60: 875-889.
20. Pilly PK, Grossberg S, (2012) How do spatial learning and memory occur in the brain? Coordinated learning of entorhinal grid cells and hippocampal place cells. J Cogn Neurosci 24: 1031-1054.
21. Burgess N, Barry C, O'Keefe J, (2007) An oscillatory interference model of grid cell firing. Hippocampus 17: 801-812.
22. Hasselmo ME, Giocomo LM, Zilli EA, (2007) Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17: 1252-1271.
23. Mhatre H, Gorchetchnikov A, Grossberg S, (2012) Grid cell hexagonal patterns formed by fast self-organized learning within entorhinal cortex. Hippocampus 22: 320-34.
24. Krupic J, Burgess N, O'Keefe J (2011) Periodic bands are the building blocks of locational firing in the parahippocampal formation [Abstract 729.13]. In: Proceedings of the Annual Conference of the Society for Neuroscience; 12-16 November 2011; Washington, DC, United States. Neuroscience 2011. Available: http://www.abstractsonline.com/Plan/ViewAbstract.aspx?sKey=07c4898f-8c6a-43d0-b307-6374c69a19ac&cKey=ecdb7022-51ff-463c-a23b-1da7e29ffeaa&mKey=8334BE29-8911-4991-8C31-32B32DD5E6C8. Accessed 12 July 2012.
25. Caballero-Bleda M, Witter MP, (1993) Regional and laminar organization of projections from the presubiculum and parasubiculum to the entorhinal cortex: An anterograde tracing study in the rat. J Comp Neurol 328: 115-129.
26. Caballero-Bleda M, Witter MP, (1994) Projections from the presubiculum and the parasubiculum to morphologically characterized entorhial-hippocampal projection neurons in the rat. Exp Brain Res 101: 93-108.
27. Goldberg ME, Hudspeth AJ (2000) The vestibular system. In: Kandel ER, Schwartz JH, Jessell TM, editors. Principles of neural science, 4/e. New York: McGraw-Hill Press. pp. 801-815.
28. Blair H, Sharp P, (1995) Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction. J Neurosci 15: 6260-6270.
29. Skaggs WE, Knierim J, Kudrimoti HS, McNaughton BL, (1995) A model of the neural basis of the rat's sense of direction. Adv Neur In 7: 173-180.
30. Blair H, Sharp P, (1996) Visual and vestibular influences on head direction cells in the anterior thalamus of the rat. Behav Neurosci 10: 643-660.
31. Redish AD, Elga AN, Touretzky DS, (1996) A coupled attractor model of the rodent head direction system. Network-Comp Neural 7: 671-685.
32. Goodridge JP, Touretzky DS, (2000) Modeling attractor deformation in the rodent head-direction system. J Neurophysiol 83: 3402-3410.
33. Boucheny C, Brunel N, Arleo A, (2005) A continuous attractor network model without recurrent excitation: Maintenance and integration in the head direction cell system. J Comput Neurosci 18: 205-227.
34. Song P, Wang XJ, (2005) Angular path integration by moving "hill of activity": A spiking neuron model without recurrent excitation of the head-direction system. J Neurosci 25: 1002-1014.
35. Fortenberry B, Gorchetchnikov A, Grossberg S, (2012) Learned integration of visual, vestibular, and motor cues in multiple brain regions computes head direction during visually-guided navigation. Hippocampus 18doi: 10.1002/hipo.22040.
36. Blair HT, Gupta K, Zhang K, (2008) Conversion of a phase- to a rate-coded position signal by a three-stage model of theta cells, grid cells, and place cells. Hippocampus 18: 1239-1255.
37. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, et al. (2010) Development of the spatial representation system in the rat. Science 328: 1576-1580.
38. Wills TJ, Cacucci F, Burgess N, O'Keefe J, (2010) Development of the hippocampal cognitive map in preweanling rats. Science 328: 1573-1576.
39. Grossberg S, (1973) Contour enhancement, short-term memory, and constancies in reverberating neural networks. Stud Appl Math 52: 213-257.
40. Grossberg S, (1976) Adaptive pattern classification and universal recoding, I: Parallel development and coding of neural feature detectors. Biol Cybern 23: 121-134.
41. Grossberg S, Seitz A, (2003) Laminar development of receptive fields, maps, and columns in visual cortex: The coordinating role of the subplate. Cereb Cortex 13: 852-863.
42. Olson S, Grossberg S, (1998) A neural network model for the development of simple and complex cell receptive fields within cortical maps of orientation and ocular dominance. Neural Netw 11: 189-208.
43. Grossberg S, Williamson JR, (2001) A neural model of how horizontal and interlaminar connections of visual cortex develop into adult circuits that carry out perceptual grouping and learning. Cereb Cortex 11: 37-58.
44. Grossberg S, (1980) How does the brain build a cognitive code? Psychol Rev 87: 1-51.
45. Carpenter GA, Grossberg S, (1987) A massively parallel architecture for a self-organizing neural pattern recognition machine. Comput Vis Graph Image Process 37: 54-115.
46. Purves D (1988) Body and brain: a trophic theory of neural connections. Cambridge: Harvard University Press.
47. Cabelli RJ, Hohn A, Shatz CJ, (1995) Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267: 1662-1666.
48. Cabelli RJ, Shelton DL, Segal RA, Shatz CJ, (1997) Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron 19: 63-76.
49. Royer S, Pare D, (2003) Conservation of total synaptic weight through balanced synaptic depression and potentiation. Nature 422: 518-522.
50. Grossberg S, Schmajuk NA, (1989) Neural dynamics of adaptive timing and temporal discrimination during associative learning. Neural Netw 2: 79-102.
51. Grossberg S, Merrill JWL, (1992) A neural network model of adaptively timed reinforcement learning and hippocampal dynamics. Cognitive Brain Res 1: 3-38.
52. Grossberg S, Merrill JWL, (1996) The hippocampus and cerebellum in adaptively timed learning, recognition, and movement. J Cogn Neurosci 8: 257-277.
53. Klink R, Alonso A, (1997) Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. J Neurophysiol 77: 1813-1828.
54. Shalinsky MH, Magistretti J, Ma L, Alonso AA, (2002) Muscarinic activation of a cation current and associated current noise in entorhinal-cortex layer-II neurons. J Neurophysiol 88: 1197-1211.
55. Woodhall GL, Bailey SJ, Thompson SE, Evans DI, Jones RS, (2005) Fundamental differences in spontaneous synaptic inhibition between deep and superficial layers of the rat entorhinal cortex. Hippocmapus 15: 232-245.
56. Khwaja FA, Alonso AA, Bourque CW, (2007) Ca(2+)-dependent K(+) currents and spike-frequency adaptation in medial entorhinal cortex layer II stellate cells. Hippocampus 17: 1143-1148.
57. Tsanov M, Manahan-Vaughan D, (2007) Intrinsic, light-independent and visual activity-dependent mechanisms cooperate in the shaping of the field response in rat visual cortex. J Neurosci 27: 8422-8429.
58. Gaudiano P, Grossberg S, (1991) Vector associative maps: Unsupervised real-time error-based learning and control of movement trajectories. Neural Netw 4: 147-183.
59. Izhikevich EM (2007) Dynamical systems in neuroscience: The geometry of excitability and bursting. Cambridge: MIT Press.
60. Dickson CT, Magistretti J, Shalinsky MH, Fransen E, Hasselmo ME, et al. (2000) Properties and role of I(h) in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. J Neurophysiol 83: 2562-2579.
61. Lancaster B, Adams PR, (1986) Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. J Neurophysiol 55: 1268-1282.
62. Giocomo LM, Hussaini SA, Zheng F, Kandel ER, et al. (2011) Grid cells use HCN1 channels for spatial scaling. Cell 147: 1159-1170.
63. Barry C, Hayman R, Burgess N, Jeffery K, (2007) Experience-dependent rescaling of entorhinal grids. Nat Neurosci 10: 682-684.
64. Grossberg S (1978) A theory of human memory: Self-organization and performance of sensory-motor codes, maps, and plans. In: Rosen R, Snell F, editors. Progress in theoretical biology, Volume 5. New York: Academic Press. pp. 233-374.
65. Chey J, Grossberg S, Mingolla E, (1998) Neural dynamics of motion processing and speed discrimination. Vision Res 38: 2769-2786.
66. Grossberg S, (1994) 3-D vision and figure-ground separation by visual cortex. Percept Psychophys 55: 48-120.
67. Grossberg S, Myers CW, (2000) The resonant dynamics of speech perception: Interword integration and duration-dependent backward effects. Psychol Rev 107: 735-767.
68. Grossberg S, Kazerounian S, (2011) Laminar cortical dynamics of conscious speech perception: A neural model of phonemic restoration using subsequent context in noise. J Acoust Soc Am 130: 440-460.
69. Dodson PD, Pastoll H, Nolan MF, (2011) Dorsal-ventral organization of theta-like activity intrinsic to entorhinal stellate neurons is mediated by differences in stochastic current fluctuations. J Physiol 589: 2993-3008.
70. Dolorfo CL, Amaral DG, (1998) Entorhinal cortex of the rat: Topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J Comp Neurol 398: 25-48.
71. Jeewajee A, Barry C, O'Keefe J, Burgess N, (2008) Grid cells and theta as oscillatory interference: electophysiological data from freely moving rats. Hippocampus 18: 1175-1185.
72. Boehlen A, Heinemann U, Erchova I, (2010) The range of intrinsic frequencies represented by medial entorhinal cortex stellate cells extends with age. J Neurosci 30: 4585-4589.
73. Bonnevie T, Fyhn M, Hafting T, Derdikman D, Moser EI, et al. (2010) Hippocampal contribution to maintenance of entorhinal grid fields [Abstract 101.4]. In: Proceedings of the Annual Conference of the Society for Neuroscience; 13-17 November 2010; San Diego, CA, United States. Neuroscience 2010. Available: http://www.abstractsonline.com/Plan/ViewAbstract.aspx?sKey=1cdafe8e-ffef-47d1-b94d-72f2a6793390&cKey=a4f1eb94-d3d6-4291-97ce-3a41cc5e99b7&mKey=E5D5C83F-CE2D-4D71-9DD6-FC7231E090FB. Accessed 12 July 2012.
74. Thompson LT, Best PJ, (1990) Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res 509: 299-308.
75. Wilson MA, McNaughton BL, (1993) Dynamics of the hippocampal ensemble code for space. Science 261: 1055-1058.
76. Muller RA, (1996) A quarter of a century of place cells. Neuron 17: 813-822.
77. Frank LM, Stanley GB, Brown EN, (2004) Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 24: 7681-7689.
78. Grossberg S, (1999) The link between brain learning, attention, and consciousness. Conscious Cogn 8: 1-44.
79. Grossberg S, (1976) Adaptive pattern classification and universal recoding, II: Feedback, expectation, olfaction, and illusions. Biol Cybern 23: 187-202.
80. Grossberg S, (2009) Beta oscillations and hippocampal place cell learning during exploration of novel environments. Hippocampus 19: 881-885.
81. Kentros CG, Agniotri NT, Streater S, Hawkins RD, Kandel ER, (2004) Increased attention to spatial context increases both place field stability and spatial memory. Neuron 42: 283-295.
82. Kentros CG, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, et al. (1998) Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280: 2121-2126.
83. Morris RGM, Frey U, (1997) Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Philos T Roy Soc B 1360: 1469-1503.
84. Fransen E, Alonso AA, Dickson CT, Magistretti J, Hasselmo ME, (2004) Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus 14: 368-384.
85. Schreiber S, Erchova I, Heinemann U, Herz AV, (2004) Subthreshold resonance explains the frequency-dependent integration of periodic as well as random stimuli in the entorhinal cortex. J Neurophysiol 92: 408-415.
86. Alonso A, Llinas RR, (1989) Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175-177.
87. Navratilova Z, Giocomo LM, Fellous JM, Hasselmo ME, McNaughton BL, (2012) Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after-spike dynamics. Hippocampus 22: 772-789.
88. MacDonald CJ, Lepage LQ, Eden UT, Eichenbaum H, (2011) Hippocampal "time cells" bridge the gap in memory for discontiguous events. Neuron 71: 737-749.
89. Fiala JC, Grossberg S, Bullock D, (1996) Metabotropic glutamate receptor activation in cerebellar Purkinje cells as substrate for adaptive timing of the classically conditioned eye blink response. J Neurosci 16: 3760-3774.
90. Brown J, Bullock D, Grossberg S, (1999) How the basal ganglia use parallel excitatory and inhibitory learning pathways to selectively respond to unexpected rewarding cues. J Neurosci 19: 10502-10511.
91. Hargreaves EL, Rao G, Lee I, Knierim JJ, (2005) Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308: 1792-1794.
92. Aminoff E, Gronau N, Bar M, (2007) The parahippocampal cortex mediates spatial and nonspatial associations. Cereb Cortex 17: 1493-1503.
93. Kerr KM, Agster KL, Furtak SC, Burwell RD, (2007) Functional neuroanatomy of the parahippocampal region: the lateral and medial entorhinal areas. Hippocampus 17: 697-708.
94. Eichenbaum H, Lipton PA, (2008) Towards a functional organization of the medial temporal lobe memory system: Role of the parahippocampal and medial entorhinal cortical areas. Hippocampus 18: 1314-1324.
95. Tulving E (1972) Episodic and semantic memory. In: Tulving E, Donaldson W, editors. Organization of Memory. New York: Academic Press.
96. Tulving E, Thomson DC, (1973) Encoding specificity and retrieval processes in episodic memory. Psychol Rev 80: 352-373.
97. Tulving E, (1984) Précis of elements of episodic memory. Behav Brain Sci 7: 223-268.
98. Eichenbaum H, Dudchenko P, Wood E, Shapiro M, Tanila H, (1999) The hippocampus, memory and place cells: Is it spatial memory or a memory space? Neuron 23: 209-226.
99. Gaussier P, Banquet JP, Sargolini F, Giovannangeli C, Save E, et al. (2007) A model of grid cells involving extra-hippocampal path integration, and the hippocampal loop. J Integr Neurosci 6: 447-476.
100. Burgess N, (2008) Grid cells and theta as oscillatory interference: theory and predictions. Hippocmapus 18: 1157-1174.
101. Burak Y, Fiete IR, (2009) Accurate path integration in continuous attractor network model of grid cells. PLoS Comput Biol 5: e1000291.