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Adult neurogenesis in the hippocampal dentate gyrus affects sparsely synchronized rhythms, associated with pattern separation and integration

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Abstract

We are concerned about sparsely synchronized rhythms (SSRs), associated with diverse cognitive functions, in the hippocampal dentate gyrus. Distinctly, adult-born immature GCs (imGCs) emerge through neurogenesis, in addition to the mature granule cells (mGCs) (emerged in the developmental stage). In prior work, these mGCs and imGCs were found to exhibit their distinct roles in pattern separation and integration for encoding cortical inputs, respectively. But, the underlying dynamical mechanismremains unclear. In this paper, we first study influence of the young adult-born imGCs on emergence of SSRs in the populations of the mGCs and the imGCs; population and individual firing behaviors in the SSRs are intensively studied. We then examine how the SSRs play a role in the underlying mechanism for pattern separation and integration. Particularly, quantitative relationship between SSRs of the mGCs and the imGCs and their pattern separation and integration is investigated.

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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 (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 

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

    Article  CAS  PubMed  ADS  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 

  • 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  ADS  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 

  • Boldrini M, Fulmore CA, Tartt AN, Simeon LR, Pavlova I, Poposka V, Rosoklija GB, Stankov A, Arango V, Dwork AJ, Hen R, Mann JJ (2018) Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell 22:589-599.e5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  MathSciNet  PubMed  ADS  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 

  • Buzsáki G (2006) Rhythms of the brain. Oxford University Press, New York

    Book  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 

  • 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 

  • Csicsvari J, Hirase H, Czurko A, Buzsáki G (1998) Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 21:179–189

    Article  CAS  PubMed  Google Scholar 

  • Destexhe A, Sejnowski TJ (2003) Interactions between membrane conductances underlying thalamocortical slow-wave oscillations. Physiol Rev 83:1401–1453

    Article  CAS  PubMed  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  ADS  PubMed Central  Google Scholar 

  • Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186–189

    Article  CAS  PubMed  ADS  Google Scholar 

  • Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560–1563

    Article  CAS  PubMed  ADS  Google Scholar 

  • Gage FH (2019) Adult neurogenesis in mammals. Science 364:827–828

    Article  CAS  PubMed  ADS  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 

  • 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 

  • 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 (2013) Sparsely-synchronized brain rhythm in a small-world neural network. J Korean Phys Soc 63:104–113

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kim SY, Lim W (2015a) Effect of small-world connectivity on fast sparsely synchronized cortical rhythms. Physica A 421:109–123

    Article  Google Scholar 

  • Kim SY, Lim W (2015b) Fast sparsely synchronized brain rhythms in a scale-free neural network. Phys Rev E 92:022717

    Article  MathSciNet  ADS  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) 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, Ch, p 8

    Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  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 

  • 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  ADS  Google Scholar 

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

    Article  CAS  ADS  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 

  • 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 

  • 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  ADS  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 

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

    Article  PubMed  Google Scholar 

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

    Article  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  ADS  PubMed Central  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, 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 

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

    Article  MathSciNet  PubMed  Google Scholar 

  • Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Boström E, Westerlund I, Vial C, Buchholz BA, Possnert G, Mash DC, Druid H, Frisén J (2013) Dynamics of hippocampal neurogenesis in adult humans. Cell 153:1219–1227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Steriade M, McCormick D, Sejnowski T (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679–685

    Article  CAS  PubMed  ADS  Google Scholar 

  • Traub RD, Whittington MA (2010) Cortical oscillations in health and diseases. Oxford University Press, New York

    Book  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 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang XJ (2003) Neural oscillations. In: Nadel L (ed) Encyclopedia of cognitive science. MacMillan, London, pp 272–280

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wang X, Liu H, Morstein J, Novak AJE, Trauner D, Xiong Q, Yu Y, Ge S (2020) Metabolic tuning of inhibition regulates hippocampal neurogenesis in the adult brain. Proc Natl Acad Sci USA 117:25818–25829

    Article  CAS  PubMed  ADS  PubMed Central  Google Scholar 

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

    Article  CAS  ADS  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 

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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).

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Kim, SY., Lim, W. Adult neurogenesis in the hippocampal dentate gyrus affects sparsely synchronized rhythms, associated with pattern separation and integration. Cogn Neurodyn (2024). https://doi.org/10.1007/s11571-024-10089-x

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