Dendrites of dentate gyrus granule cells contribute to pattern separation by controlling sparsity

Hippocampus

Volumn 27, Issue 1, 2017, Pages 89-110

  Chavlis, Spyridon ^a,b   Petrantonakis, Panagiotis C ^a   Poirazi, Panayiota ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

Author keywords

computational model; hippocampus; memory; network model

Indexed keywords

ARTICLE; CELL GROWTH; COMPUTER SIMULATION; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS GRANULAR LAYER; EXCITABILITY; FIRING RATE; KOLMOGOROV SMIRNOV TEST; NETWORK LEARNING; PATTERN SEPARATION; PRIORITY JOURNAL; RANK SUM TEST; SYNAPSE; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; DENTATE GYRUS; HUMAN; MEMORY; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; COMPUTER SIMULATION; DENDRITES; DENTATE GYRUS; DISCRIMINATION (PSYCHOLOGY); HUMANS; MEMORY; MODELS, NEUROLOGICAL;

EID: 85002368657     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22675     Document Type: Article

References (84)

1. Aimone JB, Deng W, Gage FH. 2010. Adult neurogenesis: Integrating theories and separating functions. Trends Cogn Sci 14:325–337.
2. Aimone JB, Deng W, Gage FH. 2011. Resolving new memories: A critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70:589–596.
3. Ally BA, Hussey EP, Ko PC, Molitor RJ. 2013. Pattern separation and pattern completion in Alzheimer's disease: Evidence of rapid forgetting in amnestic mild cognitive impairment. Hippocampus 23:1246–1258.
4. Amaral DG, Ishizuka N, Claiborne B. 1990. Neurons, numbers and the hippocampal network. Prog Brain Res 83:1–11.
5. Amaral DG, Scharfman HE, Lavenex P. 2007. The dentate gyrus: Fundamental neuroanatomical organization (dentate gyrus for dummies). In: Scharfman HE, editor. The Dentate Gyrus: A Comprehensive Guide to Structure, Function, and Clinical Implications, Vol163. Amsterdam: Elsevier B.V. pp 3–22.
6. Aradi I, Holmes WR. 1999. Role of multiple calcium and calcium-dependent conductances in regulation of hippocampal dentate granule cell excitability. J Comput Neurosci 6:215–235.
7. Bakker A, Kirwan CB, Miller M, Stark CEL. 2008. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319:1640–1642.
8. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P. 2001. Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21:2687−2698.
9. Bolz L, Heigele S, Bischofberger J. 2015. Running improves pattern separation during novel object recognition. Brain Plast 1:129–141.
10. Brette R, Gerstner W. 2005. Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. J Neurophysiol 94:3637–3642.
11. Brette R, Goodman DFM. 2011. Vectorized algorithms for spiking neural network simulation. Neural Comput 23:1503–1535.
12. Buckmaster PS, Jongen-Rêlo AL. 1999. Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19:9519–9529.
13. Burkitt AN. 2006. A review of the integrate-and-fire neuron model: I. Homogeneous synaptic input. Biol Cybern 95:1–19.
14. Chiang PH, Wu PY, Kuo TW, Liu YC, Chan CF, Chien TC, Cheng JK, Huang YY, Chiu C, Di, Lien CC. 2012. GABA Is depolarizing in hippocampal dentate granule cells of the adolescent and adult rats. J Neurosci 32:62–67.
15. Claiborne BJ, Amaral DG, Cowan WM. 1990. Quantitative, three-dimensional analysis of granule cell dendrites in the rat dentate gyrus. J Comp Neurol 302:206–219.
16. Coultrip R, Granger R, Lynch G. 1992. A cortical model of winner-take-all competition via lateral inhibition. Neural Netw 5:47–54.
17. Danielson NB, Kaifosh P, Zaremba JD, Lovett-Barron M, Tsai J, Denny CA, Balough EM, Goldberg AR, Drew LJ, Hen R, Losonczy A, Kheirbek MA. 2016. Distinct contribution of adult-born hippocampal granule cells to context encoding. Neuron 90:101–112.
18. Das T, Ivleva EI, Wagner AD, Stark CEL, Tamminga CA. 2014. Loss of pattern separation performance in schizophrenia suggests dentate gyrus dysfunction. Schizophr Res 159:193–197.
19. Deng W, Aimone JB, Gage FH. 2010. New neurons and new memories: How does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11:339–350.
20. Einstein G, Buranosky R, Crain BJ. 1994. Dendritic pathology of granule cells in Alzheimer's disease is unrelated to neuritic plaques. J Neurosci 14:5077–5088.
21. Engin E, Zarnowska ED, Benke D, Tsvetkov E, Sigal M, Keist R, Bolshakov VY, Pearce RA, Rudolph U. 2015. Tonic inhibitory control of dentate gyrus granule cells by 5-containing GABAA receptors reduces memory interference. J Neurosci 35:13698–13712.
22. Erevitt BS, Skrondal A. 2010. The Cambridge Dictionary of Statistics, 4th ed. Cambridge: Cambridge University Press.
23. Eriksson PS. 2003. Neurogenesis and its implications for regeneration in the adult brain. J Rehabil Med 35:17–19.
24. Faghihi F, Moustafa AA. 2015. A computational model of pattern separation efficiency in the dentate gyrus with implications in schizophrenia. Front Syst Neurosci 9:1–12.
25. Geiger JRP, Lübke J, Roth A, Frotscher M, Jonas P. 1997. Submillisecond AMPA receptor-mediated signaling at a principal neuron–interneuron synapse. Neuron 18:1009–1023.
26. Goodman DFM, Brette R. 2009. The brian simulator. Front Neurosci 3:192–197.
27. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806.
28. Hamming RW. 1950. Error detecting and error correcting codes. Bell Syst Tech J 29:147–160.
29. Harney SC, Jones MV. 2002. Pre- and postsynaptic properties of somatic and dendritic inhibition in dentate gyrus. Neuropharmacology 43:584–594.
30. Henze DA, Buzsáki G. 2007. Hilar mossy cells: functional identification and activity in vivo. In: Scharfman HE, editor. The Dentate Gyrus: A Comprehensive Guide to Structure, Function, and Clinical Implications, Vol163. Amsterdam: Elsevier B.V. pp 199–216.
31. Ikrar T, Guo N, He K, Besnard A, Levinson S, Hill A, Lee HK, Hen R, Xu X, Sahay A. 2013. Adult neurogenesis modifies excitability of the dentate gyrus. Front Neural Circuits 7:204.
32. Izhikevich EM. 2003. Simple model of spiking neurons. IEEE Trans Neural Netw 14:1569−1572.
33. Jahr CE, Stevens CF. 1990. Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. J Neurosci 10:3178–3182.
34. Jain S, Yoon SY, Zhu L, Brodbeck J, Dai J, Walker D, Huang Y. 2012. Arf4 determines dentate gyrus-mediated pattern separation by regulating dendritic spine development. PLoS One 7:1–15.
35. Jinde S, Zsiros V, Jiang Z, Nakao K, Pickel J, Kohno K, Belforte JE, Nakazawa K. 2012. Hilar mossy cell degeneration causes transient dentate granule cell hyperexcitability and impaired pattern separation. Neuron 76:1189–1200.
36. Jinde S, Zsiros V, Nakazawa K. 2013. Hilar mossy cell circuitry controlling dentate granule cell excitability. Front Neural Circuits 7:14.
37. Johnston ST, Shtrahman M, Parylak S, Gonçalves JT, Gage FH. 2015. Paradox of pattern separation and adult neurogenesis: A dual role for new neurons balancing memory resolution and robustness. Neurobiol Learn Mem.
38. Jung MW, McNaughton BL. 1993. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:165–182.
39. Kirwan CB, Stark CEL. 2007. Overcoming interference: An fMRI investigation of pattern separation in the medial temporal lobe. Learn Mem 14:625–633.
40. Kneisler TB, Dingledine R. 1995. Spontaneous and synaptic input from granule cells and the perforant path to dentate basket cells in the rat hippocampus. Hippocampus 5:151–164.
41. Krueppel R, Remy S, Beck H. 2011. Dendritic integration in hippocampal dentate granule cells. Neuron 71:512–528.
42. Lacy JW, Yassa MA, Stark SM, Muftuler LT, Stark CEL. 2011. Distinct pattern separation related transfer functions in human CA3/dentate and CA1 revealed using high-resolution fMRI and variable mnemonic similarity. Learn Mem 18:15–18.
43. Larimer P, Strowbridge BW. 2008. Nonrandom local circuits in the dentate gyrus. J Neurosci 28:12212−12223.
44. Leutgeb JK, Leutgeb S, Moser MB, Moser EI. 2007. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961–966.
45. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, McNaughton BL, Moser MB, Moser EI. 2005. Progressive transformation of hippocampal neuronal representations in “morphed” environments. Neuron 48:345–348.
46. Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI. 2004. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305(80–):1295–1298.
47. Lübke J, Frotscher M, Spruston N. 1998. Specialized electrophysiological properties of anatomically identified neurons in the hilar region of the rat fascia dentata. J Neurophysiol 79:1518–1534.
48. Lynch M, Sayin U, Golarai G, Sutula T. 2000. NMDA receptor-dependent plasticity of granule cell spiking in the dentate gyrus of normal and epileptic rats. J Neurophysiol 84:2868–2879.
49. Marr D. 1971. Simple memory: A theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262:23–81.
50. Marrone DF, Adams AA, Satvat E. 2011. Increased pattern separation in the aged fascia dentata. Neurobiol Aging 32:2317.e23−2317.e32.
51. Mathern GW, Babb TL, Vickrey BG, Melendez M, Pretorius JK. 1995. The clinical–pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 118:105−118.
52. McNaughton BL, Barnes CA, Mizumori SJY, Green EJ, Sharp PE. 1991. Contribution of granule cells to spatial representations in hippocampal circuits: A puzzle. In: Morrell F, editor. Kindling and Synaptic Plasticity: The Legacy of Graham Goddar. Boston: Springer-Verlag. pp 110–123.
53. Morris RGM. 2006. Elements of a neurobiological theory of hippocampal function: The role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23:2829–2846.
54. Motley SE, Kirwan CB. 2012. A parametric investigation of pattern separation processes in the medial temporal lobe. J Neurosci 32:13076–13084.
55. Myers CE, Scharfman HE. 2009. A role for hilar cells in pattern separation in the dentate gyrus: A computational approach. Hippocampus 19:321–337.
56. Myers CE, Scharfman HE. 2011. Pattern separation in the dentate gyrus: A role for the CA3 backprojection. Hippocampus 21:1190−1215.
57. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Barrera VR, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S. 2012. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188–201.
58. Neuhäuser M. 2011. Nonparametric Statistical Tests: A Computational Approach. New York: CRC Press.
59. Nitz D, McNaughton B. 2004. Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. J Neurophysiol 91:863–872.
60. O'Reilly RC, McClelland JL. 1994. Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade-off. Hippocampus 4:661−682.
61. Olshausen BA, Field DJ. 2004. Sparse coding of sensory inputs. Curr Opin Neurobiol 14:481−487.
62. Petrantonakis PC, Poirazi P. 2014. A compressed sensing perspective of hippocampal function. Front Syst Neurosci 8:1−13.
63. Petrantonakis PC, Poirazi P. 2015. Dentate gyrus circuitry features improve performance of sparse approximation algorithms. PLoS One 10:e0117023.
64. Ratzliff ADH, Howard AL, Santhakumar V, Osapay I, Soltesz I. 2004. Rapid deletion of mossy cells does not result in a hyperexcitable dentate gyrus: Implications for epileptogenesis. J Neurosci 24:2259–2269.
65. Ratzliff AH, Santhakumar V, Howard A, Soltesz I. 2002. Mossy cells in epilepsy: Rigor mortis or vigor mortis?. Trends Neurosci 25:140−144.
66. Rolls ET. 2007. An attractor network in the hippocampus: Theory and neurophysiology. Learn Mem 14:714−731.
67. Roth A, Van Rossum MCW. 2009. Modeling synapses. In: De Shutter E, editor. Computational modeling methods for neuroscientists. Cambridge, MA: MIT Press. pp 139–160.
68. Santhakumar V, Aradi I, Soltesz I. 2005. Role of mossy fiber sprouting and mossy cell loss in hyperexcitability: A network model of the dentate gyrus incorporating cell types and axonal topography. J Neurophysiol 93:437−453.
69. Santoro A. 2013. Reassessing pattern separation in the dentate gyrus. Front Behav Neurosci 7:1−4.
70. Satvat E, Schmidt B, Argraves M, Marrone DF, Markus EJ. 2011. Changes in task demands alter the pattern of zif268 expression in the dentate gyrus. J Neurosci 31:7163–7167.
71. Scheff SW, Price DA. 2003. Synaptic pathology in Alzheimer's disease: A review of ultrastructural studies. Neurobiol Aging 24:1029–1046.
72. Schmidt-Hieber C, Bischofberger J. 2010. Fast sodium channel gating supports localized and efficient axonal action potential initiation. J Neurosci 30:10233–10242.
73. Schmidt-Hieber C, Jonas P, Bischofberger J. 2007. Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J Neurosci 27:8430–8441.
74. Sik A, Penttonen M, Buzsaki G. 1997. lnterneurons in the hippocampal dentate gyrus: An in vivo intracellular study. Eur J Neurosci 9:573−588.
75. Sloviter RS, Lømo T. 2012. Updating the lamellar hypothesis of hippocampal organization. Front Neural Circuits 6:102.
76. Small SA, Chawla MK, Buonocore M, Rapp PR, Barnes CA. 2004. Imaging correlates of brain function in monkeys and rats isolates a hippocampal subregion differentially vulnerable to aging. Proc Natl Acad Sci USA 101:7181–7186.
77. Squire LR, Stark CEL, Clark RE. 2004. The medial temporal lobe. Annu Rev Neurosci 27:279−306.
78. Tejada J, Roque AC. 2014. Computational models of dentate gyrus with epilepsy-induced morphological alterations in granule cells. Epilepsy Behav 38:63–70.
79. Treves A, Rolls ET. 1994. Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374−391.
80. Treves A, Tashiro A, Witter MP, Moser EI. 2008. What is the mammalian dentate gyrus good for? Neuroscience 154:1155−1172.
81. West MJ, Kawas CH, Martin LJ, Troncoso JC. 2006. The CA1 region of the human hippocampus is a hot spot in Alzheimer's disease. Ann N Y Acad Sci 908:255–259.
82. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482−497.
83. Yassa MA, Stark CEL. 2011. Pattern separation in the hippocampus. Trends Neurosci 34:515−525.
84. Yim MY, Hanuschkin A, Wolfart J. 2015. Intrinsic rescaling of granule cells restores pattern separation ability of a dentate gyrus network model during epileptic hyperexcitability. Hippocampus 25:297−308.