Log in

Population and individual firing behaviors in sparsely synchronized rhythms in the hippocampal dentate gyrus

  • Research Article
  • Published:
Cognitive Neurodynamics Aims and scope Submit manuscript

A Correction to this article was published on 29 March 2023

This article has been updated

Abstract

We investigate population and individual firing behaviors in sparsely synchronized rhythms (SSRs) in a spiking neural network of the hippocampal dentate gyrus (DG). The main encoding granule cells (GCs) are grouped into lamellar clusters. In each GC cluster, there is one inhibitory (I) basket cell (BC) along with excitatory (E) GCs, and they form the E-I loop. Winner-take-all competition, leading to sparse activation of the GCs, occurs in each GC cluster. Such sparsity has been thought to enhance pattern separation performed in the DG. During the winner-take-all competition, SSRs are found to appear in each population of the GCs and the BCs through interaction of excitation of the GCs with inhibition of the BCs. Sparsely synchronized spiking stripes appear successively with the population frequency \(f_p~ (= 13.1\) Hz) in the raster plots of spikes. We also note that excitatory hilar mossy cells (MCs) control the firing activity of the GC-BC loop by providing excitation to both the GCs and the BCs. SSR also appears in the population of MCs via interaction with the GCs (i.e., GC-MC loop). Population behaviors in the SSRs are quantitatively characterized in terms of the synchronization measures. In addition, we investigate individual firing activity of GCs, BCs, and MCs in the SSRs. Individual GCs exhibit random spike skip**, leading to a multi-peaked inter-spike-interval histogram, which is well characterized in terms of the random phase-locking degree. In this case, population-averaged mean-firing-rate (MFR) \(<\!f_i^{(\text {GC})}\!>\) is less than the population frequency \(f_p\). On the other hand, both BCs and MCs show “intrastripe” burstings within stripes, together with random spike skip**. Thus, the population-averaged MFR \(\langle f_i^{(X)} \rangle\) (\(X=\) MC and BC) is larger than \(f_p\), in contrast to the case of the GCs. MC loss may occur during epileptogenesis. With decreasing the fraction of the MCs, changes in the population and individual firings in the SSRs are also studied. Finally, quantitative association between the population/individual firing behaviors in the SSRs and the winner-take-all competition is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Change history

References

  • Almeida LD, Idiart M, Lisman JE (2009) A second function of gamma frequency oscillations: An E%-max winner-take-all mechanism selects which cells fire. J Neurosci 29:7497–7503

    Article  PubMed  PubMed Central  Google Scholar 

  • Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571–591

    Article  CAS  PubMed  Google Scholar 

  • Amaral DG, Ishizuka N, Claiborne B (1990) Neurons, numbers and the hippocampal network. Prog Brain Res 83:1–11

    Article  CAS  PubMed  Google Scholar 

  • Amaral DG, Scharfman HE, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3–22

    Article  PubMed  PubMed Central  Google Scholar 

  • Andersen P, Bliss TVP, Skrede KK (1971) Lamellar organization of hippocampal excitatory pathways. Exp Brain Res 13:222–238

    Article  CAS  PubMed  Google Scholar 

  • Andersen P, Soleng AF, Raastad M (2000) The hippocampal lamella hypothesis revisited. Brain Res 886:165–171

    Article  CAS  PubMed  Google Scholar 

  • Bakker A, Kirwan CB, Miller M, Stark CEL (2008) Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319:1640–1642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barranca VJ, Huang H, Kawakita G (2019) Network structure and input integration in competing firing rate models for decision-making. J Comput Neurosci 46:145–168

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck H, Goussakov IV, Lie A, Helmstaedter C, Elger CE (2000) Synaptic plasticity in the human dentate gyrus. J Neurosci 20:7080–7086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bielczyk NZ, Piskała K, Płomecka M, Radziński P, Todorova L, Foryś U, (2019) Time-delay model of perceptual decision making in cortical networks. PLoS One 14:e0211885

  • Brunel N, Hakim V (2008) Sparsely synchronized neuronal oscillations. Chaos 18:015113

    Article  PubMed  Google Scholar 

  • Brunel N, Wang XJ (2003) What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J Neurophysiol 90:415–430

    Article  PubMed  Google Scholar 

  • 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 19:9519–9529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 366:271–292

    Article  CAS  PubMed  Google Scholar 

  • Buckmaster PS, Yamawaki R, Zhang GF (2002) Axon arbors and synaptic connections of a vulnerable population of interneurons in the dentate gyrus in vivo. J Comp Neurol 445:360–373

    Article  PubMed  Google Scholar 

  • Chavlis S, Petrantonakis PC, Poirazi P (2017) Dendrites of dentate gyrus granule cells contribute to pattern separation by controlling sparsity. Hippocampus 27:89–110

    Article  PubMed  Google Scholar 

  • Chiang PH, Wu PY, Kuo TW, Liu YC, Chan CF, Chien TC, Cheng JK, Huang YY, Chiu CD, Lien CC (2012) GABA is depolarizing in hippocampal dentate granule cells of the adolescent and adult rats. J Neurosci 32:62–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coultrip R, Granger R, Lynch G (1992) A cortical model of winner-take-all competition via lateral inhibition. Neural Netw 5:47–54

    Article  Google Scholar 

  • Csicsvari J, Hirase H, Czurko A, Mamiya A, Buzsáki G (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Csicsvari J, Jamieson B, Wise K, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311–322

    Article  CAS  PubMed  Google Scholar 

  • Destexhe A, Paré D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81:1531–1547

    Article  CAS  PubMed  Google Scholar 

  • Dijk van MT, Fenton AA (2018) On how the dentate gyrus contributes to memory discrimination. Neuron 98:832–845

    Article  PubMed  PubMed Central  Google Scholar 

  • Dudek SM, Alexander GM, Farris S (2016) Rediscovering area CA2: unique properties and functions. Nat Rev Nurosci 17:89–102

    Article  CAS  Google Scholar 

  • Espinoza C, Guzman SJ, Zhang X, Jonas P (2018) Parvalbumin+ interneurons obey unique connectivity rules and establish a powerful lateral inhibition microcircuit in dentate gyrus. Nat Commun 9:4605

    Article  PubMed  PubMed Central  Google Scholar 

  • Ewell LA, Jones MV (2010) Frequency-tuned distribution of inhibition in the dentate gyrus. J Neurosci 30:12597–12607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fellous J, Sejnowski TJ (2000) Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5-2 Hz), theta (5–12 Hz) and gamma (35–70 Hz) bands. Hippocampus 10:187–197

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Ruiz A, Oliva A, Soula M, Rocha-Almeida F, Nagy GA, Martin-Vazquez G, Buzsáki G (2021) Gamma rhythm communication between entorhinal cortex and dentate gyrus neuronal assemblies. Science 372:eabf3119

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Geisler C, Brunel N, Wang XJ (2005) Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges. J Neurophysiol 94:4344–4361

    Article  PubMed  Google Scholar 

  • Gerstner W, Kistler W (2002) Spiking Neuron Models. Cambridge University Press, New York

    Book  Google Scholar 

  • Gluck MA, Myers CE (2001) Gateway to memory: an introduction to neural network modeling of the hippocampus in learning and memory. MIT Press, Cambridge

    Google Scholar 

  • Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806

    Article  CAS  PubMed  Google Scholar 

  • Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick D (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423–435

    Article  CAS  PubMed  Google Scholar 

  • Hosp JA, Strüber M, Yanagawa Y, Obata K, Vida I, Jonas P, Bartos M (2014) Morpho-physiological criteria divide dentate gyrus interneurons into classes. Hippocampus 24:189–203

    Article  CAS  PubMed  Google Scholar 

  • Houghton C (2017) Dentate gyrus and hilar region revisited. Behav Brain Sci 39:28–29

    Google Scholar 

  • Hsiao YT, Zheng C, Colgin LL (2016) Slow gamma rhythms in CA3 are entrained by slow gamma activity in the dentate gyrus. J Neurophysiol 116:2594–2603

    Article  PubMed  PubMed Central  Google Scholar 

  • Jahr CE, Stevens CF (1990) Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. J Neurosci 10:3178–3182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • **de 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • **de S, Zsiros V, Nakazawa K (2013) Hilar mossy cell circuitry controlling dentate granule cell excitability. Front Neural Circuit 7:14

    Article  Google Scholar 

  • Kassab R, Alexandre F (2018) Pattern separation in the hippocampus: distinct circuits under different conditions. Brain Struct Funct 223:2785–2808

    Article  PubMed  Google Scholar 

  • Kim SY, Lim W (2014) Realistic thermodynamic and statistical-mechanical measures for neural synchronization. J Neurosci Meth 226:161–170

    Article  Google Scholar 

  • Kim SY, Lim W (2018) Effect of inhibitory spike-timing-dependent plasticity on fast sparsely synchronized rhythms in a small-world neuronal network. Neural Netw 106:50–66

    Article  PubMed  Google Scholar 

  • Kim SY, Lim W (2021) Effect of diverse recoding of granule cells on optokinetic response in a cerebellar ring network with synaptic plasticity. Neural Netw 134:173–204

    Article  PubMed  Google Scholar 

  • Kim SY, Lim W (2021) Influence of various temporal recoding on Pavlovian eyeblink conditioning in the cerebellum. Cogn Neurodyn. https://doi.org/10.1007/s11571-021-09673-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim SY, Lim W (2021) Equalization effect in interpopulation spike-timing-dependent plasticity in two inhibitory and excitatory populations. In: Lintas A, Enrico P, Pan X, Wang R, Villa A (eds) Advances in cognitive neurodynamics (VII). Springer, Singapore, p 8

    Google Scholar 

  • Kim SY, Lim W (2021d) Dynamical origin for winner-take-all competition in a biological network of the hippocampal dentate gyrus. bioRxiv, https://doi.org/10.1101/2021.5.12.443925

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Knierim JJ, Neunuebel JP (2016) Tracking the flow of hippocampal computation: Pattern separation, pattern completion, and attractor dynamics. Neurobiol Learn Mem 129:38–49

    Article  CAS  PubMed  Google Scholar 

  • Krueppel R, Remy S, Beck H (2011) Dendritic integration in hippocampal dentate granule cells. Neuron 71:512–528

    Article  CAS  PubMed  Google Scholar 

  • Larimer P, Strowbridge BW (2008) Nonrandom local circuits in the dentate gyrus. J Neurosci 28:12212–12223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961–966

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Marr D (1971) Simple memory: a theory for archicortex. Phil Trans R Soc Lond B 262:23–81

    Article  CAS  Google Scholar 

  • McNaughton B, Morris R (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415

    Article  Google Scholar 

  • 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 (ed) Kindling and synaptic plasticity: the legacy of Graham Goddar. Springer-Verlag, Boston, pp 110–123

    Google Scholar 

  • Morgan RJ, Santhakumar V, Soletsz I (2007) Modeling the dentate gyrus. Prog Brain Res 163:639–658

    Article  PubMed  Google Scholar 

  • Myers CE, Scharfman HE (2009) A role for hilar cells in pattern separation in the dentate gyrus: A computational approach. Hippocampus 19:321–337

    Article  PubMed  PubMed Central  Google Scholar 

  • Myers CE, Scharfman HE (2011) Pattern separation in the dentate gyrus: A role for the CA3 backprojection. Hippocampus 21:1190–1215

    Article  PubMed  Google Scholar 

  • Myers CE, Bermudez-Hernandez K, Scharfman HE (2013) The influence of ectopic migration of granule cells into the hilus on dentate gyrus-CA3 function. PLoS ONE 8:e68208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nitz D, McNaughton B (2004) Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. J Neurophysiol 91:863–872

    Article  PubMed  Google Scholar 

  • Nomura T, Fukuda T, Aika Y, Heizmann CW, Emson PC, Kobayashi T, Kosaka T (1997) Distribution of nonprincipal neurons in the rat hippocampus, with special reference to their dorsoventral difference. Brain Res 751:64–80

    Article  CAS  PubMed  Google Scholar 

  • Nomura T, Fukuda T, Aika Y, Heizmann CW, Emson PC, Kobayashi T, Kosaka T (1997) Laminar distribution of non-principal neurons in the rat hippocampus, with special reference to their compositional difference among layers. Brain Res 764:197–204

    Article  CAS  PubMed  Google Scholar 

  • O’Reilly RC, McClelland JC (1994) Hippocampal conjunctive encoding, storage, and recall: Avoiding a tradeoff. Hippocampus 4:661–682

  • Pearson K (1895) Notes on regression and inheritance in the case of two parents. Proc R Soc Lond 58:240–242

    Article  Google Scholar 

  • Petrantonakis PC, Poirazi P (2014) A compressed sensing perspective of hippocampal function. Front Syst Neurosci 8:141

    Article  PubMed  PubMed Central  Google Scholar 

  • Petrantonakis PC, Poirazi P (2015) Dentate gyrus circuitry features improve performance of sparse approximation algorithms. PLoS One 10:e0117023

    Article  PubMed  PubMed Central  Google Scholar 

  • Press WH, teukolsky SA, Vetterling WT, Flannery BP, (1992) Nemerical receipes in C: the art of scientific computing, 2nd edn. Cambridge University Press, New York

  • Rangel LM, Chiba AA, Quinn LK (2015) Theta and beta oscillatory dynamics in the dentate gyrus reveal a shift in network processing state during cue encounters. Front Syst Neurosci 9:96

    Article  PubMed  PubMed Central  Google Scholar 

  • Ratzliff AH, Santhakumar V, Howard A, Soltesz I (2002) Mossy cells in epilepsy: rigor mortis or vigor mortis? Trends Neurosci 25:140–144

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rojas-Líbano D, Kay LM (2008) Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system. Cogn Neurodyn 2:179–194

    Article  PubMed  PubMed Central  Google Scholar 

  • Rolls ET (1989) Functions of neuronal networks in the hippocampus and neocortex in memory. In: Byrne JH, Berry WO (eds) Neural models of plasticity: experimental and theoretical approaches. Academic Press, San Diego, pp 240–265

    Chapter  Google Scholar 

  • Rolls ET (1989) The representation and storage of information in neural networks in the primate cerebral cortex and hippocampus. In: Durbin R, Miall C, Mitchison G (eds) Comput Neuron. Addition-Wesley, Wokingham, pp 125–159

    Google Scholar 

  • Rolls ET (1989) Functions of neuronal networks in the hippocampus and cerebral cortex in memory. In: Cotterill R (ed) Models Brain Function. Cambridge University Press, New York, pp 15–33

    Google Scholar 

  • Rolls ET (2016) Pattern separation, completion, and categorization in the hippocampus and neocortex. Neurobiol Learn Mem 129:4–28

    Article  PubMed  Google Scholar 

  • Roux NL, Amar M, Baux G, Fossier P (2006) Homeostatic control of the excitation-inhibition balance in cortical layer 5 pyramidal neurons. Eur J Neurosci 24:3507–3518

    Article  PubMed  Google Scholar 

  • 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 524:117–134

  • 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

    Article  PubMed  Google Scholar 

  • Santoro A (2013) Reassessing pattern separation in the dentate gyrus. Front Behav Neurosci 7:96

    Article  PubMed  PubMed Central  Google Scholar 

  • Savanthrapadian S, Meyer T, Elgueta C, Booker SA, Vida I, Bartos M (2014) Synaptic properties of SOM- and CCK-expressing cells in dentate gyrus interneuron networks. J Neurosci 34:8197–8209

    Article  PubMed  PubMed Central  Google Scholar 

  • Scharfman HE (1991) Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J Neurosci 11:1660–1673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scharfman HE (2018) Advances in understanding hilar mossy cells of the dentate gyrus. Cell Tissue Res 373:643–652

    Article  CAS  PubMed  Google Scholar 

  • Scharfman HE, Myers CE (2013) Hilar mossy cells of the dentate gyrus: A historical perspective. Front Neural Circuit 6:106

    Article  Google Scholar 

  • Scharfman HE, Myers CE (2016) Corruption of the dentate gyrus by “dominant” granule cells: Implications for dentate gyrus function in health and disease. Neurobiol Learn Mem 129:69–82

  • Schmidt B, Marrone DF, Markus EJ (2012) Disambiguating the similar: the dentate gyrus and pattern separation. Behav Brain Res 226:56–65

    Article  PubMed  Google Scholar 

  • Schmidt-Hieber C, Bischofberger J (2010) Fast sodium channel gating supports localized and efficient axonal action potential initiation. J Neurosci 30:10233–10242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimazaki H, Shinomoto S (2010) Kernel bandwidth optimization in spike rate estimation. J Comput Neurosci 29:171–182

    Article  PubMed  Google Scholar 

  • Sloviter RS (1991) Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the “dormant basket cell” hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1:41–66

  • Sloviter RS (1994) The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann Neurol 35:640–654

    Article  CAS  PubMed  Google Scholar 

  • Sloviter RS, Lømo T (2012) Updating the lamellar hypothesis of hippocampal organization. Front Neural Circuit 6:102

    Article  Google Scholar 

  • Solages De C, Szapiro G, Brunel N, Hakim V, Isope P, Buisseret P, Rousseau C, Barbour B, Lna C (2008) High-frequency organization and synchrony of activity in the purkinje cell layer of the cerebellum. Neuron 58:775–788

    Article  PubMed  Google Scholar 

  • Squire L (1987) Memory and Brain. Oxford University Press, New York

    Google Scholar 

  • Su L, Chang CJ, Lynch N (2019) Spike-based winner-take-all computation: Fundamental limits and order-optimal circuits. Neural Comput 31:2523–2561

    Article  PubMed  Google Scholar 

  • Trapp P, Echeveste R, Gros C (2018) E-I balance naturally emerges from continuous Hebbian learning in autonomous neural networks. Sci Rep 8:8939

    Article  PubMed  PubMed Central  Google Scholar 

  • Treves A, Rolls ET (1991) What determines the capacity of autoassociative memories in the brain? Network 2:371–397

    Article  Google Scholar 

  • Treves A, Rolls ET (1992) Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2:189–199

    Article  CAS  PubMed  Google Scholar 

  • Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4:374–391

    Article  CAS  PubMed  Google Scholar 

  • Wang XJ (2010) Neurophysiological and computational principles of fscortical rhythms in cognition. Physiol Rev 90:1195–1268

    Article  PubMed  Google Scholar 

  • Wang Y, Zhang X, **n Q, Hung W, Florman J, Huo J, Xu T, **e Y, Alkema MJ, Zhen M, Wen Q (2020) Flexible motor sequence generation during stereotyped escape responses. eLife 9: e56942

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Willshaw D, Buckingham J (1990) An assessment of Marr’s theory of the hippocampus as a temporary memory store. Phil Trans R Soc Lond B 329:205–215

  • Yassa MA, Stark CEL (2011) Pattern separation in the hippocampus. Trends Neurosci 34:515–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

Funding

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (Grant No. 20162007688).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Woochang Lim.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, SY., Lim, W. Population and individual firing behaviors in sparsely synchronized rhythms in the hippocampal dentate gyrus. Cogn Neurodyn 16, 643–665 (2022). https://doi.org/10.1007/s11571-021-09728-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-021-09728-4

Keywords

Navigation