دورية أكاديمية

Toroidal topology of population activity in grid cells.

التفاصيل البيبلوغرافية
العنوان: Toroidal topology of population activity in grid cells.
المؤلفون: Gardner RJ; Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Trondheim, Norway. richard.gardner@ntnu.no., Hermansen E; Department of Mathematical Sciences, Norwegian University of Science and Technology, Trondheim, Norway., Pachitariu M; HHMI Janelia Research Campus, Ashburn, VA, USA., Burak Y; Edmond and Lily Safra Center for Brain Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel.; Racah Institute of Physics, The Hebrew University of Jerusalem, Jerusalem, Israel., Baas NA; Department of Mathematical Sciences, Norwegian University of Science and Technology, Trondheim, Norway. nils.baas@ntnu.no., Dunn BA; Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Trondheim, Norway. benjamin.dunn@ntnu.no.; Department of Mathematical Sciences, Norwegian University of Science and Technology, Trondheim, Norway. benjamin.dunn@ntnu.no., Moser MB; Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Trondheim, Norway., Moser EI; Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Trondheim, Norway. edvard.moser@ntnu.no.
المصدر: Nature [Nature] 2022 Feb; Vol. 602 (7895), pp. 123-128. Date of Electronic Publication: 2022 Jan 12.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE
أسماء مطبوعة: Publication: Basingstoke : Nature Publishing Group
Original Publication: London, Macmillan Journals ltd.
مواضيع طبية MeSH: Models, Neurological*, Grid Cells/*physiology, Action Potentials ; Animals ; Entorhinal Cortex/anatomy & histology ; Entorhinal Cortex/cytology ; Entorhinal Cortex/physiology ; Grid Cells/classification ; Male ; Rats ; Rats, Long-Evans ; Sleep/physiology ; Space Perception/physiology ; Wakefulness/physiology
مستخلص: The medial entorhinal cortex is part of a neural system for mapping the position of an individual within a physical environment 1 . Grid cells, a key component of this system, fire in a characteristic hexagonal pattern of locations 2 , and are organized in modules 3 that collectively form a population code for the animal's allocentric position 1 . The invariance of the correlation structure of this population code across environments 4,5 and behavioural states 6,7 , independent of specific sensory inputs, has pointed to intrinsic, recurrently connected continuous attractor networks (CANs) as a possible substrate of the grid pattern 1,8-11 . However, whether grid cell networks show continuous attractor dynamics, and how they interface with inputs from the environment, has remained unclear owing to the small samples of cells obtained so far. Here, using simultaneous recordings from many hundreds of grid cells and subsequent topological data analysis, we show that the joint activity of grid cells from an individual module resides on a toroidal manifold, as expected in a two-dimensional CAN. Positions on the torus correspond to positions of the moving animal in the environment. Individual cells are preferentially active at singular positions on the torus. Their positions are maintained between environments and from wakefulness to sleep, as predicted by CAN models for grid cells but not by alternative feedforward models 12 . This demonstration of network dynamics on a toroidal manifold provides a population-level visualization of CAN dynamics in grid cells.
(© 2022. The Author(s).)
References: Science. 2010 Jun 18;328(5985):1576-80. (PMID: 20558721)
Nat Neurosci. 2015 Apr;18(4):569-75. (PMID: 25730672)
Science. 2006 May 5;312(5774):758-62. (PMID: 16675704)
Nature. 2015 Jan 8;517(7533):159-64. (PMID: 25470055)
Cell Rep. 2022 Apr 5;39(1):110612. (PMID: 35385721)
Biol Cybern. 2012 Oct;106(8-9):483-506. (PMID: 22892761)
Nature. 2017 Jun 1;546(7656):101-106. (PMID: 28538731)
J Neurosci Methods. 1995 Dec;63(1-2):43-54. (PMID: 8788047)
Nature. 2021 Aug;596(7872):404-409. (PMID: 34381211)
Neuron. 2023 Jan 4;111(1):121-137.e13. (PMID: 36306779)
Cell Rep. 2021 May 25;35(8):109175. (PMID: 34038726)
Phys Rev Lett. 2017 Jul 21;119(3):038101. (PMID: 28777606)
Nature. 2012 Dec 6;492(7427):72-8. (PMID: 23222610)
Nat Rev Neurosci. 2006 Aug;7(8):663-78. (PMID: 16858394)
Phys Rev E. 2018 Mar;97(3-1):032313. (PMID: 29776117)
J Neurosci. 1997 Aug 1;17(15):5900-20. (PMID: 9221787)
Nat Neurosci. 2019 Sep;22(9):1512-1520. (PMID: 31406365)
Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13339-44. (PMID: 8917592)
Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3844-8. (PMID: 7731993)
Neuron. 2002 Dec 19;36(6):1183-94. (PMID: 12495631)
Biol Cybern. 1977 Aug 3;27(2):77-87. (PMID: 911931)
J Neurosci. 2006 Jan 11;26(2):622-31. (PMID: 16407560)
Elife. 2017 Sep 07;6:. (PMID: 28879851)
J Neurosci. 2015 Aug 05;35(31):10963-76. (PMID: 26245960)
Adv Neural Inf Process Syst. 1995;7:173-80. (PMID: 11539168)
PLoS Comput Biol. 2012;8(8):e1002581. (PMID: 22912564)
Front Comput Neurosci. 2021 Apr 08;15:616748. (PMID: 33897395)
Nature. 2015 Feb 12;518(7538):232-235. (PMID: 25673417)
Neural Comput. 2019 Jan;31(1):68-93. (PMID: 30462582)
Nat Neurosci. 2013 Mar;16(3):318-24. (PMID: 23334580)
J Neurosci. 2006 Apr 19;26(16):4266-76. (PMID: 16624947)
Nature. 2005 Aug 11;436(7052):801-6. (PMID: 15965463)
Nature. 2015 Feb 12;518(7538):207-12. (PMID: 25673414)
Nat Neurosci. 2007 Apr;10(4):494-504. (PMID: 17369822)
Nature. 2017 Nov 8;551(7679):232-236. (PMID: 29120427)
Neural Comput. 2013 Mar;25(3):626-49. (PMID: 23272922)
Science. 2019 Mar 29;363(6434):1447-1452. (PMID: 30923222)
Nat Neurosci. 2014 Mar;17(3):431-9. (PMID: 24487232)
Nat Neurosci. 2017 Nov;20(11):1643-1653. (PMID: 28967910)
Nat Neurosci. 2007 Jun;10(6):682-4. (PMID: 17486102)
J Neurosci. 2008 Jun 25;28(26):6731-41. (PMID: 18579747)
J Neurosci. 1990 Feb;10(2):420-35. (PMID: 2303851)
Hippocampus. 2008;18(12):1256-69. (PMID: 19021261)
PLoS Comput Biol. 2017 Oct 2;13(10):e1005782. (PMID: 28968386)
Proc Natl Acad Sci U S A. 2015 Nov 3;112(44):13455-60. (PMID: 26487684)
Science. 2010 Jun 18;328(5985):1573-6. (PMID: 20558720)
Nat Neurosci. 2013 Aug;16(8):1077-84. (PMID: 23852111)
Nature. 2015 May 14;521(7551):186-91. (PMID: 25971509)
Science. 2017 Mar 17;355(6330):. (PMID: 28154241)
Nat Neurosci. 2019 Apr;22(4):598-608. (PMID: 30911185)
Nat Biotechnol. 2021 Feb;39(2):156-157. (PMID: 33526945)
Elife. 2016 Mar 08;5:e10094. (PMID: 26952211)
Elife. 2018 Feb 21;7:. (PMID: 29465399)
Int J Neural Syst. 2007 Aug;17(4):231-40. (PMID: 17696288)
Science. 2021 Apr 16;372(6539):. (PMID: 33859006)
Biol Cybern. 1993;69(5-6):517-24. (PMID: 8274549)
J Vis. 2008 Jun 30;8(8):11.1-18. (PMID: 18831634)
Front Syst Neurosci. 2014 Oct 14;8:193. (PMID: 25352787)
Cereb Cortex. 2000 Sep;10(9):910-23. (PMID: 10982751)
PLoS Comput Biol. 2009 Feb;5(2):e1000291. (PMID: 19229307)
J Neurosci. 2020 Jun 3;40(23):4512-4524. (PMID: 32332120)
J Neurosci. 1996 Mar 15;16(6):2112-26. (PMID: 8604055)
Science. 2017 May 26;356(6340):849-853. (PMID: 28473639)
Nat Commun. 2019 Oct 18;10(1):4745. (PMID: 31628322)
Nat Neurosci. 2019 Apr;22(4):609-617. (PMID: 30911183)
Science. 2019 Mar 29;363(6434):1443-1447. (PMID: 30923221)
J Exp Biol. 1996 Jan;199(Pt 1):173-85. (PMID: 8576689)
Neuron. 2017 Apr 19;94(2):375-387.e7. (PMID: 28392071)
Science. 2005 Feb 18;307(5712):1121-4. (PMID: 15718474)
Nature. 2007 Mar 8;446(7132):190-4. (PMID: 17322902)
PLoS Comput Biol. 2010 Aug 05;6(8):. (PMID: 20700490)
Neuron. 2008 Oct 23;60(2):215-34. (PMID: 18957215)
معلومات مُعتمدة: International ERC_ European Research Council
تواريخ الأحداث: Date Created: 20220113 Date Completed: 20220309 Latest Revision: 20240822
رمز التحديث: 20240822
مُعرف محوري في PubMed: PMC8810387
DOI: 10.1038/s41586-021-04268-7
PMID: 35022611
قاعدة البيانات: MEDLINE