Spatiotemporal Patterns of Granule Cell Activity Revealed by a Large-Scale, Biologically Realistic Model of the Hippocampal Dentate Gyrus

  • Gene J. YuEmail author
  • Phillip J. Hendrickson
  • Dong Song
  • Theodore W. Berger
Part of the Springer Series in Computational Neuroscience book series (NEUROSCI)


Interest in the hippocampus has generated vast amounts of experimental data describing hippocampal properties, including anatomical, morphological, biophysical, and synaptic transmission levels of analysis. However, this wealth of structural and functional detail has not guaranteed insight into higher levels of system operation.

In this chapter, we propose a computational framework that can integrate the available, quantitative information at various levels of organization to construct a three-dimensional, large-scale, biologically realistic, spiking neuronal network model with the goal of representing all major neurons and neuron types, and the synaptic connectivity, found in the rat hippocampus. In this approach, detailed neuron models are constructed using a multi-compartment approach.

Simulations were performed to investigate the role of network architecture on the spatiotemporal patterns of activity generated by the dentate gyrus. The results show that the topographical projection of axons between the entorhinal cortex and the dentate granule cells organizes the postsynaptic population into subgroups of neurons that exhibit correlated firing expressed as spatiotemporal clusters of firing. These clusters may represent a potential “intermediate” level of hippocampal function. Furthermore, the effects of inhibitory and excitatory circuits, and their interactions, on the population granule cell response were explored using dentate basket cells and hilar mossy cells.


Spiking neuronal network model Large-scale Hippocampus Dentate gyrus Entorhinal cortex Compartmental model Anatomical connectivity Population dynamics Spatiotemporal clusters Inhibition Mossy cell associational pathway 



This work was supported by ONR Grant N00014-13-1-0211, NIBIB Grant P41 EB001978, and NIH Grant U01 GM104604. Computation for the work was supported by the University of Southern California Center for High-Performance Computing and Communications (www.usc.ed/hpcc).


  1. Acsády L, Kamondi A, Sík A, Freund TF, Buzsáki G (1998) GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 19:3386–3403CrossRefGoogle Scholar
  2. Acsády L, Katona I, Martínez-Guijarro FJ, Buzsáki G, Freund TF (2000) Unusual target selectivity of perisomatic inhibitory cells in the hilar region of the rat hippocampus. J Neurosci 20:6907–6919CrossRefGoogle Scholar
  3. Aggleton JP, Brown MW (1999) Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22:425–444PubMedCrossRefGoogle Scholar
  4. Andersen P, Bliss TVP, Skrede KK (1971) Lamellar organization of hippocampal excitatory pathways. Exp Brain Res 13:222–238PubMedGoogle Scholar
  5. Andersen P, Silfvenius H, Sundberg SH, Sveen O, Wigström H (1978) Functional characteristics of unmyelinated fibres in the hippocampal cortex. Brain Res 144:11–18PubMedCrossRefGoogle Scholar
  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 6:215–235PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aradi I, Soltesz I (2002) Modulation of network behaviour by changes in variance in interneuronal properties. J Phys 539:227–251Google Scholar
  8. Ascoli GA, Krichmar JL (2000) L-neuron: a modeling tool for the efficient generation and parsimonious description of dendritic morphology. Neurocomputing 32-33:1003–1011CrossRefGoogle Scholar
  9. Ascoli GA, Donohue DE, Halavi M (2007) NeuroMorpho.Org: a central resource for neuronal morphologies. J Neurosci 27:9247–9251PubMedPubMedCentralCrossRefGoogle Scholar
  10. Berger TW, Bassett JL (1992) System properties of the hippocampus. In: Gormezano I, Wasserman EA (eds) Learning and memory: the biological substrates. Lawrence Erlbaum, Hillsdale, pp 275–320Google Scholar
  11. Berger TW, Weisz DJ (1987) Single unit analysis of hippocampal pyramidal and granule cells during classic conditioning of the rabbit nictitating membrane response. In: Gormezano I, Prokasy WF, Thompson RF (eds) Classical conditioning III: behavioral, neurophysiological and neurochemical studies in the rabbit. Lawrence Erlbaum, Hillsdale, pp 217–253Google Scholar
  12. Berger TW, Semple-Rowland S, Bassett JL (1981) Hippocampal polymorph neurons are the cells of origin for ipsilateral association and commissural afferents to the dentate gyrus. Brain Res 215:329–336PubMedCrossRefGoogle Scholar
  13. Berger TW, Rinaldi P, Weisz DJ, Thompson RF (1983) Single unit analysis of different hippocampal cell types during classical conditioning of the rabbit nictitating membrane response. J Neurophysiol 50:1197–1219PubMedCrossRefGoogle Scholar
  14. Berger TW, Berry SD, Thompson RF (1986) Role of the hippocampus in classical conditioning of aversive and appetitive behaviors. In: Isaacson RL, Pribram KH (eds) The hippocampus, vol 4. Plenum, New York, pp 203–239CrossRefGoogle Scholar
  15. Berger TW, Hampson RE, Song D, Goonawardena A, Marmarelis VZ, Deadwyler SA (2011) A cortical neural prosthesis for restoring and enhancing memory. J Neural Eng 8:046017. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Buckmaster PS, Dudek FE (1997) Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol 385:385–404PubMedCrossRefGoogle Scholar
  17. Buckmaster PS, Dudek FE (1999) In vivo intracellular analysis of granule cell axon reorganization in epileptic rats. J Neurophysiol 81:712–721PubMedCrossRefGoogle Scholar
  18. Buckmaster PS, Jongen-Rêlo AL (1999) Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainite-induced epileptic rats. J Neurosci 19:9519–9529PubMedCrossRefGoogle Scholar
  19. Buckmaster PS, Strowbridge BW, Kunkel DD, Schmiege DL, Schwartzkroin PA (1992) Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus 2:349–362PubMedCrossRefGoogle Scholar
  20. Buckmaster PS, Wenzel HJ, Kunkel DD, Schwartzkroin PA (1996) Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 366:271–292CrossRefGoogle Scholar
  21. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823–828PubMedPubMedCentralCrossRefGoogle Scholar
  22. Buhl EH, Cobb SR, Halasy K, Somogyi P (1995) Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7:1989–2004PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cajal SR (1968) The structure of the Ammon’s horn. Charles C. Thomas, SpringfieldGoogle Scholar
  24. Carnevale NT, Hines ML (2006) The NEURON book. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  25. Claiborne BJ, Amaral DG, Cowan WM (1990) Quantitative, three-dimensional analysis of granule cell dendrites in the rat dentate gyrus. J Comp Neurol 302:206–219CrossRefGoogle Scholar
  26. Cohen NJ, Eichenbaum H (1993) Memory, amnesia and the hippocampal system. MIT Press, CambridgeGoogle Scholar
  27. Crain B, Cotman C, Taylor D, Lynch G (1973) A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat. Brain Res 63:195–204PubMedCrossRefGoogle Scholar
  28. De Schutter E, Bower JM (1994) An active membrane model of the cerebellar Purkinje cell I. Simulation of current clamps in slice. J Neurophysiol 71:375–400PubMedCrossRefGoogle Scholar
  29. Desmond NL, Levy WB (1985) Granule cell dendritic spine density in the rat hippocampus varies with spine shape and location. Neurosci Lett 54:219–224PubMedCrossRefGoogle Scholar
  30. 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 398:25–48PubMedCrossRefGoogle Scholar
  31. Douglas RM, McNaughton BL, Goddard GV (1983) Commissural inhibition and facilitation of granule cell discharge in fascia dentata. J Comp Neurol 219:285–294PubMedCrossRefGoogle Scholar
  32. Dyhrfjeld-Johnsen J, Santhakumar V, Morgan RJ, Huerta R, Tsimring L, Soltesz I (2007) Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. J Neurophysol 97:1566–1587CrossRefGoogle Scholar
  33. Eichenbaum H, Wiener SI, Shapiro ML, Cohen NJ (1989) The organization of spatial coding in the hippocampus: a study of neural ensemble activity. J Neurosci 9:2764–2775PubMedCrossRefGoogle Scholar
  34. Foster TC, Barnes CA, Rao G, McNaughton BL (1991) Increase in perforant path quantal size in aged F-344 rats. Neurobiol Aging 12:441–448PubMedCrossRefGoogle Scholar
  35. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gaarskjaer FB (1978) Organization of the mossy fiber system of the rat studied in extended hippocampi I: terminal area related to number of granule and pyramidal cells. J Comp Neurol 178:49–71PubMedCrossRefGoogle Scholar
  37. Gamrani H, Onteniente B, Seguela P, Geffard M, Calas A (1986) Gamma-aminobutyric acid-immunoreactivity in the rat hippocampus: a light and electron microscopic study with anti-GABA antibodies. Brain Res 364:30–38PubMedCrossRefGoogle Scholar
  38. Geiger JRP, Lübke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18:1009–1023CrossRefGoogle Scholar
  39. Gottlieb DI, Cowan WM (1973) Autoradiographic studies of the commissural and ipsilateral association connection of the hippocampus and dentate gyrus of the rat. I. The commissural connections. J Comp Neurol 149:393–421PubMedCrossRefGoogle Scholar
  40. Gulyás AI, Megías M, Emri Z, Freund TF (1999) Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J Neurosci 19:10082–10097CrossRefGoogle Scholar
  41. Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806. CrossRefPubMedGoogle Scholar
  42. Halasy K, Somogyi P (1993) Distribution of GABAergic synapses and their targets in the dentate gyrus of rat: a quantitative immunoelectron microscopic analysis. J Hirnforsch 34:299–308Google Scholar
  43. Hama K, Arii T, Kosaka T (1989) Three-dimensional morphometrical study of dendritic spines of the granule cell in the rat dentate gyrus with HVEM stereo images. J Electron Microsc Tech 12:80–87CrossRefGoogle Scholar
  44. Hampson RE, Simeral JD, Deadwyler SA (1999) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402:610–614PubMedCrossRefGoogle Scholar
  45. Han ZS, Buhl EH, Lörinczi Z, Somogyi P (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5:395–410CrossRefGoogle Scholar
  46. Hasselmo ME (2005) What is the function of hippocampal theta rhythm?—linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 15:936–949. CrossRefPubMedGoogle Scholar
  47. Hendrickson PJ, Yu GJ, Song D, Berger TW (2015) Interactions between inhibitory interneurons and excitatory associational circuitry in determining spatio-temporal dynamics of hippocampal dentate granule cells: a large-scale computational study. Front Syst Neurosci 9.
  48. Hendrickson PJ, Yu GJ, Song D, Berger TW (2016) A million-plus neuron model of the hippocampal dentate gyrus: critical role for topography in determining spatiotemporal network dynamics. IEEE Trans Biomed Eng 63:199–209CrossRefGoogle Scholar
  49. Hines ML, Davison AP, Muller E (2009) NEURON and Python. Front Neuroinform 28.
  50. Hinneburg A, Gabriel H (2007) DENCLUE 2.0: fast clustering based on kernel density estimation. In Proceedings of the 7th international conference on advances in intelligent data analysis, Ljubljana, vol. 4723, pp 70–80Google Scholar
  51. Hjorth-Simonsen A, Jeune B (1972) Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J Comp Neurol 144:215–232PubMedCrossRefGoogle Scholar
  52. Ishizuka N, Weber J, Amaral DG (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol. 295:580–623PubMedCrossRefGoogle Scholar
  53. Jaffe DB, Ross WN, Lisman JE, Lasser-Ross N, Miyakawa H, Johnston D (1994) A model for dendritic Ca2+ accumulation in hippocampal pyramidal neurons based on fluorescence imaging measurements. J Neurosci 71:1065–1077Google Scholar
  54. Krueppel R, Remy S, Beck H (2011) Dendritic integration in hippocampal dentate granule cells. Neuron 71:512–528PubMedCrossRefGoogle Scholar
  55. Krupic J, Burgess N, O’Keefe J (2012) Neural representations of location composed of spatially periodic bands. Science 337:853–857PubMedPubMedCentralCrossRefGoogle Scholar
  56. Levy WB (1989) A computational approach to hippocampal function. In: Psychology of learning and motivation. Elsevier, pp 243–305Google Scholar
  57. Lorente de Nó R (1934) Studies on the structure of the cerebral cortex II: continuation of the study of the ammonic system. J Psychol Neurol 46:113–177Google Scholar
  58. MacKenzie S, Frank AJ, Kinsky NR, Porter B, Riviére PD, Eichenbaum H (2014) Hippocampal representation of related and opposing memories develop within distinct, hierarchically organized neural schemas. Neuron 83:202–215CrossRefGoogle Scholar
  59. McClelland JL, McNaughton BL, O’Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102:419–457. CrossRefPubMedGoogle Scholar
  60. McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415. CrossRefGoogle Scholar
  61. Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond 262:23–81CrossRefGoogle Scholar
  62. Morgan RJ, Soltesz I (2010) Microcircuit model of the dentate gyrus in epilepsy. In: Cutsuridis V, Graham BP, Cobb S, Vida I (eds) Hippocampal microcircuits. Springer, New York, pp 495–525CrossRefGoogle Scholar
  63. Mulders WHAM, West MJ, Slomianka L (1997) Neuron numbers in the presubiculum, parasubiculum, and entorhinal area of the rat. J Comp Neurol 385:83–94PubMedCrossRefGoogle Scholar
  64. Myers CE, Scharfman HE (2011) Pattern separation in the dentate gyrus: a role for the CA3 backprojection. Hippocampus 21:1190–1215PubMedPubMedCentralCrossRefGoogle Scholar
  65. Nadel L, Moscovitch M (1997) Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 7:217–227PubMedCrossRefGoogle Scholar
  66. O’Keefe J, Nadel L (1978) The Hippocampus as a cognitive map. Oxford University Press, LondonGoogle Scholar
  67. Oliphant TE (2007) Python for scientific computing. Comput Sci Eng 9:10–20CrossRefGoogle Scholar
  68. Patton PE, McNaughton BL (1995) Connection matrix of the hippocampal formation: I. The dentate gyrus. Hippocampus 5:245–286PubMedCrossRefGoogle Scholar
  69. Ribak CE, Seress L (1983) Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study. J Neurocytol 12:577–597PubMedCrossRefGoogle Scholar
  70. Ribak CE, Shapiro LA (2007) Ultrastructure and synaptic connectivity of cell types in the adult rat dentate gyrus. Prog Brain Res 163:155–166PubMedCrossRefGoogle Scholar
  71. Ribak CE, Nitsch R, Seress L (1990) Proportion of parvalbumin-positive basket cells in the GABAergic innervation of pyramidal and granule cells of the rat hippocampal formation. J Comp Neurol 300:449–461PubMedCrossRefGoogle Scholar
  72. Rihn LL, Claiborne BJ (1990) Dendritic growth and regression in rat dentate granule cells during late postnatal development. Dev Brain Res 54:115–124CrossRefGoogle Scholar
  73. Santhakumar V, Bender R, Frotscher M, Ross ST, Hollrigel GS, Toth Z, Soltesz I (2000) Granule cell hyperexcitability in the early post-traumatic rat dentate gyrus: the ‘irritable mossy cell’ hypothesis. J Physiol 524(Pt 1):117–134PubMedPubMedCentralCrossRefGoogle Scholar
  74. 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 93:437–453CrossRefGoogle Scholar
  75. Scharfman HE (1995) Electrophysiological evidence that dentate hilar mossy cells are excitatory and innervate both granule cells and interneurons. J Neurophysiol 74:179–194PubMedCrossRefGoogle Scholar
  76. Scharfman HE, Kunkel DD, Schwartkroin PA (1990) Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience 37:693–707PubMedCrossRefGoogle Scholar
  77. Scorcioni R, Polavaram S, Ascoli GA (2008) L-measure: a web-accessible tool for the analysis, comparison and search of digital reconstructions of neuronal morphologies. Nat Protoc 3:866–876PubMedPubMedCentralCrossRefGoogle Scholar
  78. Seress L, Pokorny J (1978) Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J Anat 133:181–195Google Scholar
  79. Seress L, Pokorny J (1981) Structure of the granular layer of the rat dentate gyrus: a light microscopic and Golgi study. J Anat 133:181–195PubMedPubMedCentralGoogle Scholar
  80. Seress L, Ribak CE (1983) GABAergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp Brain Res 50:173–182PubMedGoogle Scholar
  81. Sík A, Penttonen M, Buzsáki G (1997) Interneurons in the hippocampal dentate gyrus: an in vivo intracellular study. Eur J Neurosci 9:573–588CrossRefGoogle Scholar
  82. Sloviter RS, Zappone CA, Harvey BD, Bumanglag AV, Bender RA, Frotscher M (2003) ‘Dormant basket cell’ hypothesis revisited: relative vulnerabilities of dentate gyrus mossy cells and inhibitory interneurons after hippocampal status epilepticus in the rat. J Comp Neurol 459:44–76CrossRefGoogle Scholar
  83. Solstad T, Moser EI, Einevoll GT (2006) From grid cells to place cells: a mathematical model. Hippocampus 16:1026–1031. CrossRefPubMedGoogle Scholar
  84. Soriano E, Frotscher M (1989) A GABAergic axo-axonic cell in the fascia dentata controls the main excitatory hippocampal pathway. Brain Res 503:170–174PubMedCrossRefGoogle Scholar
  85. Soriano E, Frotscher M (1994) Mossy cells of the rat fascia dentate are glutamate-immunoreactive. Hippocampus 4:65–69PubMedCrossRefGoogle Scholar
  86. Spruston N, Johnston D (1992) Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J Neurophysiol 67:508–529. CrossRefGoogle Scholar
  87. Squire LR (1986) Mechanisms of memory. Science 232:1612–1619PubMedCrossRefGoogle Scholar
  88. Swanson LW, Wyss JM, Cowan WM (1978) An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181:681–716PubMedCrossRefGoogle Scholar
  89. Tamamaki N, Nojyo Y (1993) Projection of the entorhinal layer II neurons in the rat as revealed by intracellular pressure-injection of neurobiotin. Hippocampus 3:471–480PubMedCrossRefGoogle Scholar
  90. Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374–391PubMedCrossRefGoogle Scholar
  91. Vida I (2010) Morphology of hippocampal neurons. In: Cutsuridis V, Graham BP, Cobb S, Vida I (eds) Hippocampal microcircuits. Springer, New York, pp 27–67CrossRefGoogle Scholar
  92. Warman EN, Durand DM, Yuen GLF (1994) Reconstruction of hippocampal CA1 pyramidal cell electrophysiology by computer simulation. J Neurosci 71:2033–2045Google Scholar
  93. Wenzel HJ, Buckmaster PS, Anderson NL, Wenzel ME, Schwartzkroin PA (1997) Ultrastructural localization of neurotransmitter immunoreactivity in mossy cell axons and their synaptic targets in the rat dentate gyrus. Hippocampus 7:559–570PubMedCrossRefGoogle Scholar
  94. Witter MP (2007) The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog Brain Res 163:43–61PubMedCrossRefGoogle Scholar
  95. Yeckel MF, Berger TW (1990) Feedforward excitation of the hippocampus by entorhinal afferents: redefinition of the role of the trisynaptic pathway. Proc Natl Acad Sci USA 87:5832–5836PubMedCrossRefGoogle Scholar
  96. Yeckel MF, Berger TW (1995) Monosynaptic excitation of CA1 hippocampal pyramidal neurons by afferents from the entorhinal cortex. Hippocampus 5:108–114PubMedCrossRefGoogle Scholar
  97. Yu GJ, Song D, Berger TW (2014) Implementation of the excitatory entorhinal-dentate-CA3 topography in a large-scale computational model of the rat hippocampus. In: EMBC, 2014: 36th annual international conference of the IEEE Engineering in Medicine and Biology Society, Chicago. IEEE, pp 6581–6584Google Scholar
  98. Yu GJ, Hendrickson PJ, Song D, Berger TW (2015) Topography-dependent spatio-temporal correlations in the entorhinal-dentate-CA3 circuit in a large-scale computational model of the rat hippocampus. In: EMBC, 2015: 37th annual international conference of the IEEE Engineering in Medicine and Biology Society, Milan. IEEE, pp 3965–3968Google Scholar
  99. Yu GJ, Song D, Berger TW (2016). Place field detection using grid-based clustering in a large-scale computational model of the rat dentate gyrus. In: EMBC, 2016: 38th annual international conference of the IEEE Engineering in Medicine and Biology Society, Orlando. IEEE, pp 1405–1408Google Scholar
  100. Yuen GLF, Durand DM (1991) Reconstruction of hippocampal granule cell electrophysiology by computer simulation. Neuroscience 41:411–423CrossRefGoogle Scholar
  101. Zimmer J (1971) Ipsilateral afferents to the commissural zone of the fascia dentata, demonstrated in decommissurated rats by silver impregnation. J Comp Neurol 142:393–416PubMedCrossRefGoogle Scholar
  102. Zipp F, Nitsch R, Soriano E, Frotscher M (1989) Entorhinal fibers form synaptic contacts on parvalbumin-immunoreactive neurons in the rat fascia dentata. Brain Res 495:161–166PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Gene J. Yu
    • 1
    Email author
  • Phillip J. Hendrickson
    • 1
  • Dong Song
    • 1
  • Theodore W. Berger
    • 1
  1. 1.Department of Biomedical Engineering, Center for Neural Engineering, Viterbi School of EngineeringUniversity of Southern CaliforniaLos AngelesUSA

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