Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus.
disambiguation
hippocampus
navigation
neural differentiation
overlapping
place cells
Journal
Frontiers in systems neuroscience
ISSN: 1662-5137
Titre abrégé: Front Syst Neurosci
Pays: Switzerland
ID NLM: 101477946
Informations de publication
Date de publication:
2019
2019
Historique:
received:
06
06
2019
accepted:
29
08
2019
entrez:
2
10
2019
pubmed:
2
10
2019
medline:
2
10
2019
Statut:
epublish
Résumé
Disambiguation of overlapping events is thought to be the hallmark of episodic memory. Recent rodent studies have reported that when navigating overlapping path segments in the different routes place cell activity in the same overlapping path segments were remapped according to different goal locations in different routes. However, it is unknown how hippocampal neurons disambiguate reward delivery in overlapping path segments in different routes. In the present study, we recorded monkey hippocampal neurons during performance of three virtual navigation (VN) tasks in which a monkey alternately navigated two different routes that included overlapping path segments (common central hallway) and acquired rewards in the same locations in overlapping path segments by manipulating a joystick. The results indicated that out of 106 hippocampal neurons, 57 displayed place-related activity (place-related neurons), and 18 neurons showed route-dependent activity in the overlapping path segments, consistent with a hippocampal role in the disambiguation of overlapping path segments. Moreover, 75 neurons showed neural correlates to reward delivery (reward-related neurons), whereas 56 of these 75 reward-related neurons showed route-dependent reward-related activity in the overlapping path segments. The ensemble activity of reward-related neurons represented reward delivery, locations, and routes in the overlapping path segments. In addition, ensemble activity patterns of hippocampal neurons more distinctly represented overlapping path segments than non-overlapping path segments. The present results provide neurophysiological evidence of disambiguation in the monkey hippocampus, consistent with a hippocampal role in episodic memory, and support a recent computational model of "neural differentiation," in which overlapping items are better represented by repeated retrieval with competitive learning.
Identifiants
pubmed: 31572133
doi: 10.3389/fnsys.2019.00048
pmc: PMC6751269
doi:
Types de publication
Journal Article
Langues
eng
Pagination
48Informations de copyright
Copyright © 2019 Bretas, Matsumoto, Nishimaru, Takamura, Hori, Ono and Nishijo.
Références
Science. 1991 Sep 20;253(5026):1380-6
pubmed: 1896849
Nat Neurosci. 2016 Jul;19(7):959-64
pubmed: 27182818
J Neurophysiol. 2007 Oct;98(4):1997-2007
pubmed: 17671106
Neuroscience. 2003;117(4):1025-35
pubmed: 12654354
Neurosci Lett. 2019 May 14;701:32-37
pubmed: 30738872
Front Pharmacol. 2017 Aug 15;8:536
pubmed: 28860992
Neuron. 2016 Oct 5;92(1):93-99
pubmed: 27710793
Nat Rev Neurosci. 2009 Mar;10(3):173-85
pubmed: 19229240
Neuron. 2005 Jun 2;46(5):703-13
pubmed: 15924857
Science. 2017 Jan 13;355(6321):176-180
pubmed: 28082589
Hippocampus. 2014 Jan;24(1):113-30
pubmed: 24123569
Neuroscience. 2008 Nov 11;157(1):254-70
pubmed: 18824217
J Neurosci. 2007 Jan 17;27(3):472-82
pubmed: 17234580
J Neurophysiol. 2000 Jul;84(1):401-14
pubmed: 10899214
Hippocampus. 2012 Jun;22(6):1325-37
pubmed: 21830249
J Neurophysiol. 1998 Feb;79(2):1017-44
pubmed: 9463459
Neuron. 2018 Jul 11;99(1):179-193.e7
pubmed: 30008297
Front Syst Neurosci. 2019 Sep 12;13:48
pubmed: 31572133
Nature. 2009 Oct 15;461(7266):941-6
pubmed: 19829374
Elife. 2016 Jun 10;5:
pubmed: 27282386
J Neurosci. 2008 Jul 2;28(27):6950-9
pubmed: 18596169
Proc Natl Acad Sci U S A. 2005 Mar 22;102(12):4602-7
pubmed: 15761059
PLoS Biol. 2013 Oct;11(10):e1001684
pubmed: 24167442
Nature. 1996 May 30;381(6581):425-8
pubmed: 8632799
Neurosci Lett. 1997 Apr 18;226(1):57-60
pubmed: 9153641
Science. 2013 Nov 29;342(6162):1111-4
pubmed: 24288336
J Neurophysiol. 1997 Aug;78(2):597-613
pubmed: 9307098
Hippocampus. 2006;16(7):586-95
pubmed: 16685707
Hippocampus. 2017 Jul;27(7):743-758
pubmed: 28241404
Hippocampus. 1998;8(3):198-204
pubmed: 9662134
J Neurosci. 1990 Nov;10(11):3531-42
pubmed: 2230943
J Neurophysiol. 1993 Oct;70(4):1516-29
pubmed: 8283212
Proc Natl Acad Sci U S A. 2009 Jun 30;106(26):10805-10
pubmed: 19528659
Neuron. 2002 Aug 15;35(4):625-41
pubmed: 12194864
Hippocampus. 2012 Mar;22(3):534-43
pubmed: 21365712
J Neurosci. 1987 Jul;7(7):1935-50
pubmed: 3612225
Hippocampus. 2007;17(10):988-1002
pubmed: 17554771
Hippocampus. 2004;14(7):808-18
pubmed: 15382251
Neuron. 2000 Jul;27(1):169-78
pubmed: 10939340
Front Behav Neurosci. 2013 Dec 03;7:177
pubmed: 24348352
J Neurosci. 2005 Feb 9;25(6):1313-23
pubmed: 15703385
Hippocampus. 2008;18(2):193-209
pubmed: 17979198
Nat Neurosci. 2010 Aug;13(8):995-1002
pubmed: 20639874
J Neurosci. 2010 May 26;30(21):7414-22
pubmed: 20505108
Brain Res. 1971 Nov;34(1):171-5
pubmed: 5124915
J Neurosci. 2005 Jun 29;25(26):6167-74
pubmed: 15987946
PLoS Biol. 2017 Feb 27;15(2):e2001045
pubmed: 28241007
Hippocampus. 2012 Feb;22(2):299-308
pubmed: 21080411
Cell Rep. 2017 Jun 6;19(10):2143-2156
pubmed: 28591584
J Neurosci Methods. 2006 Sep 15;155(2):207-16
pubmed: 16580733
Neuron. 2003 Dec 18;40(6):1227-39
pubmed: 14687555
Hippocampus. 1996;6(6):749-62
pubmed: 9034860
Behav Brain Res. 2003 Jun 16;142(1-2):181-91
pubmed: 12798280
J Neurosci. 2012 Oct 24;32(43):15053-65
pubmed: 23100426
Curr Biol. 2017 Aug 7;27(15):2307-2317.e5
pubmed: 28736170
Neuron. 2000 Sep;27(3):623-33
pubmed: 11055443
Hippocampus. 2000;10(6):717-28
pubmed: 11153717
Exp Brain Res. 1983;52(1):41-9
pubmed: 6628596
Nat Neurosci. 2016 Apr;19(4):564-7
pubmed: 26900924
Nature. 2003 Sep 11;425(6954):184-8
pubmed: 12968182
Front Behav Neurosci. 2013 May 23;7:54
pubmed: 23734111
Hippocampus. 2011 May;21(5):502-19
pubmed: 20087892
J Neurol Neurosurg Psychiatry. 1957 Feb;20(1):11-21
pubmed: 13406589
Cell Rep. 2017 Jan 24;18(4):905-917
pubmed: 28122241
J Neurosci. 1999 Mar 15;19(6):2381-93
pubmed: 10066288
Hippocampus. 2005;15(8):991-6
pubmed: 16108028
Brain Res. 2004 Jul 16;1014(1-2):97-109
pubmed: 15212996
J Neurosci. 1987 Jul;7(7):1951-68
pubmed: 3612226
Curr Opin Neurobiol. 2007 Dec;17(6):692-7
pubmed: 18313289
Nat Neurosci. 2010 Apr;13(4):501-6
pubmed: 20190745
J Neurosci. 2017 Feb 22;37(8):2022-2031
pubmed: 28115478
J Neurosci. 2001 Mar 1;21(5):1635-44
pubmed: 11222654
Science. 2019 Mar 29;363(6434):1443-1447
pubmed: 30923221
J Neurosci. 2014 Sep 24;34(39):13163-9
pubmed: 25253861
J Neurosci. 2007 Nov 7;27(45):12176-89
pubmed: 17989284
Cereb Cortex. 2015 Oct;25(10):3994-4008
pubmed: 25477369
J Neurophysiol. 2017 Apr 1;117(4):1785-1796
pubmed: 28148640
Nat Neurosci. 2012 Mar 25;15(5):769-75
pubmed: 22446878
Science. 2015 May 1;348(6234):560-3
pubmed: 25931556