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Coherence among Head Direction Cells before Eye Opening in Rat Pups

2014; Elsevier BV; Volume: 25; Issue: 1 Linguagem: Inglês

10.1016/j.cub.2014.11.009

1879-0445

Tale L. Bjerknes, Rosamund F. Langston, Ingvild Ulsaker Kruge, Edvard I Moser, May‐Britt Moser,

Sleep and Wakefulness Research

Mammalian navigation is thought to depend on an internal map of space consisting of functionally specialized cells in the hippocampus and the surrounding parahippocampal cortices [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, 2Ranck J.B. Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats.in: Buzsáki G. Vanderwolf C.H. Electrical Activity of the Archicortex. Akademiai Kiado, Budapest1985: 217-220Google Scholar, 3Taube J.S. Muller R.U. Ranck Jr., J.B. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis.J. Neurosci. 1990; 10: 420-435PubMed Google Scholar, 4Hafting T. Fyhn M. Molden S. Moser M.B. Moser E.I. Microstructure of a spatial map in the entorhinal cortex.Nature. 2005; 436: 801-806Crossref PubMed Scopus (2432) Google Scholar, 5Solstad T. Boccara C.N. Kropff E. Moser M.B. Moser E.I. Representation of geometric borders in the entorhinal cortex.Science. 2008; 322: 1865-1868Crossref PubMed Scopus (693) Google Scholar, 6Lever C. Burton S. Jeewajee A. O'Keefe J. Burgess N. Boundary vector cells in the subiculum of the hippocampal formation.J. Neurosci. 2009; 29: 9771-9777Crossref PubMed Scopus (438) Google Scholar, 7Moser E.I. Roudi Y. Witter M.P. Kentros C. Bonhoeffer T. Moser M.B. Grid cells and cortical representation.Nat. Rev. Neurosci. 2014; 15: 466-481Crossref PubMed Scopus (198) Google Scholar]. Basic properties of this map are present when rat pups explore the world outside of their nest for the first time, around postnatal day 16–18 (P16–P18) [8Langston 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, 9Wills T.J. Cacucci F. Burgess N. O'Keefe J. Development of the hippocampal cognitive map in preweanling rats.Science. 2010; 328: 1573-1576Crossref PubMed Scopus (390) Google Scholar, 10Bjerknes T.L. Moser E.I. Moser M.B. Representation of geometric borders in the developing rat.Neuron. 2014; 82: 71-78Abstract Full Text Full Text PDF PubMed Scopus (77) Google Scholar]. One of the first functions to be expressed in navigating animals is the directional tuning of the head direction cells [8Langston 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, 9Wills T.J. Cacucci F. Burgess N. O'Keefe J. Development of the hippocampal cognitive map in preweanling rats.Science. 2010; 328: 1573-1576Crossref PubMed Scopus (390) Google Scholar]. To determine whether head direction tuning is expressed at even earlier ages, before the start of exploration, and to establish whether vision is necessary for the development of directional tuning, we recorded neural activity in pre- and parasubiculum, or medial entorhinal cortex, from P11 onward, 3–4 days before the eyelids unseal. Head direction cells were present from the first day of recording. Firing rates were lower than in adults, and preferred firing directions were less stable, drifting within trials and changing completely between trials. Yet the cells drifted coherently, i.e., relative firing directions were maintained from one trial to the next. Directional tuning stabilized shortly after eye opening. The data point to a hardwired attractor network for representation of head direction in which directional tuning develops before vision and visual input serves primarily to anchor firing direction to the external world.