Skip to main content
SpringerLink
Log in

Effect of adult-born immature granule cells on pattern separation in the hippocampal dentate gyrus

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

Abstract

Young immature granule cells (imGCs) appear via adult neurogenesis in the hippocampal dentate gyrus (DG). In comparison to mature GCs (mGCs) (born during development), the imGCs exhibit two competing distinct properties such as high excitability (increasing activation degree) and low excitatory innervation (reducing activation degree). We develop a spiking neural network for the DG, incorporating both the mGCs and the imGCs. The mGCs are well known to perform “pattern separation” (i.e., a process of transforming similar input patterns into less similar output patterns) to facilitate pattern storage in the hippocampal CA3. In this paper, we investigate the effect of the young imGCs on pattern separation of the mGCs. The pattern separation efficacy (PSE) of the mGCs is found to vary through competition between high excitability and low excitatory innervation of the imGCs. Their PSE becomes enhanced (worsened) when the effect of high excitability is higher (lower) than the effect of low excitatory innervation. In contrast to the mGCs, the imGCs are found to perform “pattern integration” (i.e., making association between dissimilar patterns). Finally, we speculate that memory resolution in the hippocampal CA3 might be optimally maximized via mixed cooperative encoding through pattern separation and pattern integration.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Aimone JB, Wiles J, Gage FH (2009) Computational influence of adult neurogenesis on memory encoding. Neuron 61:187–202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aimone JB, Deng W, Gage FH (2010) Adult neurogenesis: integrating theories and separating functions. Trends Cogn Sci 14:325–337

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Altman J (1962) Are new neurons formed in the brains of adult mammals? Science 135:1127–1128

    Article  CAS  PubMed  Google Scholar 

  • Altman J (1963) Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 145:573–591

    Article  CAS  PubMed  Google Scholar 

  • Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335

    Article  CAS  PubMed  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 

  • Bayer SA (2016) Joseph Altman (1925–2016): a life in neurodevelopment. J Comp Neurol 524:2933–2944

    Article  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

    Article  CAS  PubMed  PubMed Central  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 

  • Cameron HA, Mckay RDG (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406–417

    Article  CAS  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 

  • Christian KM, Ming GI, Song H (2020) Adult neurogenesis and the dentate gyrus: predicting function from form. Behav Brain Res 379:112346

    Article  PubMed  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 

  • Dieni CV, Panichi R, Aimone JB, Kuo CT, Wadiche JI, Overstreet-Wadiche L (2016) Low excitatory innervation balances high intrinsic excitability of immature dentate neurons. Nat Commun 7:11313

    Article  CAS  PubMed  PubMed Central  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 

  • 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 

  • Finnegan R, Becker S (2015) Neurogenesis paradoxically decreases both pattern separation and memory interference. Front Syst Neurosci 9:136

    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 

  • 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 

  • Gu Y, Arruda-Carvalho M, Wang J, Janoschka S, Josselyn S, Frankland P, Ge S (2012) Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 15:1700–1706

    Article  CAS  PubMed  PubMed Central  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 

  • Heigele S, Sultan S, Toni N, Bischofberger J (2016) Bidirectional GABAergic control of action potential firing in newborn hippocampal granule cells. Nat Neurosci 19:263–270

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153–1161

    Article  CAS  PubMed  Google Scholar 

  • Jahn HM, Bergami M (2018) Critical periods regulating the circuit integration of adult-born hippocampal neurons. Cell Tissue Res 371:23–32

    Article  PubMed  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 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    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 (2022a) Dynamical origin for winner-take-all competition in a biological network of the hippocampal dentate gyrus. Phys Rev E 105:014418

    Article  CAS  PubMed  Google Scholar 

  • Kim SY, Lim W (2022b) Population and individual firing behaviors in sparsely synchronixed rhythms in the hippocampal dentata gyrus. Cogn Neurodyn 16:643–665

    Article  PubMed  Google Scholar 

  • Kim SY, Lim W (2022c) Disynaptic effect of hilar cells on pattern separation in a spiking neural network of hippocampal dentate gyrus. Cogn Neurodyn 16:1427–1447

    Article  PubMed  Google Scholar 

  • 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 

  • Laplagne DA, Espósito MS, Piatti VC, Morgenstern NA, Zhao C, van Praag H, Gage FH, Schinder AF (2006) Functional convergence of neurons generated in the developing and adult hippocampus. PLOS Biol 4:e409

    Article  PubMed  PubMed Central  Google Scholar 

  • Laplagne DA, Kamienkowski JE, Esposito MS, Piatti VC, Zhao C, Gage FH, Schinder AF (2007) Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur J Neurosci 25:2973–2981

    Article  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

  • Ming GI, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Murray KD, Liu XB, King AN, Luu JD, Cheng HJ (2020) Age-related changes in synaptic plasticity associated with mossy fiber terminal integration during adult neurogenesis. eNeuro 7:1–16

    Article  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 

  • 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

    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 (1997a) 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 (1997b) 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

    Article  PubMed  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 

  • 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 

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

    Google Scholar 

  • Rolls ET (1989c) Functions of neuronal networks in the hippocampus and cerebral cortex in memory. In: Cotterill R (ed) Models of 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 

  • Sahay A, Wilson DA, Hen R (2011a) Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70:582–588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sahay A, Scobie KN, Hill AS, O’Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R (2011b) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 Circ 6:106

    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

    Article  PubMed  Google Scholar 

  • 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 

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

    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 

  • Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH (2007) Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10:727–734

    Article  CAS  PubMed  Google Scholar 

  • Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF (2008) Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11:901–907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treves A, Rolls ET (1991) What determines the capacity of auto associative 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 

  • van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030–1034

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

Acknowledgements

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

  1. Institute for Computational Neuroscience and Department of Science Education, Daegu National University of Education, Daegu, 42411, Korea

    Sang-Yoon Kim & Woochang Lim

Authors
  1. Sang-Yoon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Woochang Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

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. Effect of adult-born immature granule cells on pattern separation in the hippocampal dentate gyrus. Cogn Neurodyn (2023). https://doi.org/10.1007/s11571-023-09985-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11571-023-09985-5

Keywords

Search

Navigation