Artigo Acesso aberto Revisado por pares

Coordinated Emergence of Hippocampal Replay and Theta Sequences during Post-natal Development

2019; Elsevier BV; Volume: 29; Issue: 5 Linguagem: Inglês

10.1016/j.cub.2019.01.005

ISSN

1879-0445

Autores

Laurenz Muessig, Michal Lasek, Isabella Varsavsky, Francesca Cacucci, Thomas J. Wills,

Tópico(s)

Sleep and Wakefulness Research

Resumo

Hippocampal place cells encode an animal's current position in space during exploration [1O'Keefe J. Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat.Brain Res. 1971; 34: 171-175Crossref PubMed Scopus (3810) Google Scholar]. During sleep, hippocampal network activity recapitulates patterns observed during recent experience: place cells with overlapping spatial fields show a greater tendency to co-fire ("reactivation") [2Wilson M.A. McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep.Science. 1994; 265: 676-679Crossref PubMed Scopus (2061) Google Scholar], and temporally ordered and compressed sequences of place cell firing observed during wakefulness are reinstated ("replay") [3Skaggs W.E. McNaughton B.L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience.Science. 1996; 271: 1870-1873Crossref PubMed Scopus (749) Google Scholar, 4Nádasdy Z. Hirase H. 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Hippocampal offline reactivation consolidates recently formed cell assembly patterns during sharp wave-ripples.Neuron. 2016; 92: 968-974Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar, 9Girardeau G. Benchenane K. Wiener S.I. Buzsáki G. Zugaro M.B. Selective suppression of hippocampal ripples impairs spatial memory.Nat. Neurosci. 2009; 12: 1222-1223Crossref PubMed Scopus (853) Google Scholar, 10Ego-Stengel V. Wilson M.A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat.Hippocampus. 2010; 20: 1-10PubMed Google Scholar]. Compressed sequences of place cell firing also occur during exploration: during each cycle of the theta oscillation, the set of active place cells shifts from those signaling positions behind to those signaling positions ahead of an animal's current location [11Dragoi G. Buzsáki G. Temporal encoding of place sequences by hippocampal cell assemblies.Neuron. 2006; 50: 145-157Abstract Full Text Full Text PDF PubMed Scopus (452) Google Scholar, 12Foster D.J. Wilson M.A. Hippocampal theta sequences.Hippocampus. 2007; 17: 1093-1099Crossref PubMed Scopus (193) Google Scholar]. These "theta sequences" have been linked to spatial planning [13Wikenheiser A.M. Redish A.D. Hippocampal theta sequences reflect current goals.Nat. Neurosci. 2015; 18: 289-294Crossref PubMed Scopus (167) Google Scholar]. Here, we demonstrate that, before weaning (post-natal day [P]21), offline place cell activity associated with sharp-wave ripples (SWRs) reflects predominantly stationary locations in recently visited environments. By contrast, sequential place cell firing, describing extended trajectories through space during exploration (theta sequences) and subsequent rest (replay), emerge gradually after weaning in a coordinated fashion, possibly due to a progressive decrease in the threshold for experience-driven plasticity. Hippocampus-dependent learning and memory emerge late in altricial mammals [14Dumas T.C. Late postnatal maturation of excitatory synaptic transmission permits adult-like expression of hippocampal-dependent behaviors.Hippocampus. 2005; 15: 562-578Crossref PubMed Scopus (70) Google Scholar, 15Wills T.J. Muessig L. Cacucci F. The development of spatial behaviour and the hippocampal neural representation of space.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013; 369: 20130409Crossref PubMed Scopus (41) Google Scholar, 16Alberini C.M. Travaglia A. Infantile amnesia: a critical period of learning to learn and remember.J. 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Development of the hippocampal cognitive map in preweanling rats.Science. 2010; 328: 1573-1576Crossref PubMed Scopus (390) Google Scholar, 19Langston R.F. Ainge J.A. Couey J.J. Canto C.B. Bjerknes T.L. Witter M.P. Moser E.I. Moser M.B. Development of the spatial representation system in the rat.Science. 2010; 328: 1576-1580Crossref PubMed Scopus (416) Google Scholar, 20Muessig L. Hauser J. Wills T.J. Cacucci F. A developmental switch in place cell accuracy coincides with grid cell maturation.Neuron. 2015; 86: 1167-1173Abstract Full Text Full Text PDF PubMed Scopus (59) Google Scholar, 21Scott R.C. Richard G.R. Holmes G.L. Lenck-Santini P.P. Maturational dynamics of hippocampal place cells in immature rats.Hippocampus. 2011; 21: 347-353Crossref PubMed Scopus (28) Google Scholar]. By examining the development of hippocampal reactivation, replay, and theta sequences, we show that the coordinated maturation of offline consolidation and online sequence generation parallels the late emergence of hippocampal memory in the rat.

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