Excitation-inhibition imbalance disrupts visual familiarity in amyloid and non-pathology conditions.
Alzheimer's disease
CP: Neuroscience
amyloid
excitation-inhibition balance
familiarity representation
hyperactivity
in vivo synapse imaging
memory interference
neural ensemble
visual cortex
visual recognition memory
Journal
Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691
Informations de publication
Date de publication:
31 01 2023
31 01 2023
Historique:
received:
16
05
2022
revised:
14
09
2022
accepted:
15
12
2022
pubmed:
15
1
2023
medline:
7
2
2023
entrez:
14
1
2023
Statut:
ppublish
Résumé
Neuronal hyperactivity induces memory deficits in Alzheimer's disease. However, how hyperactivity disrupts memory is unclear. Using in vivo synaptic imaging in the mouse visual cortex, we show that structural excitatory-inhibitory synapse imbalance in the apical dendrites favors hyperactivity in early amyloidosis. Consistent with this, natural images elicit neuronal hyperactivity in these mice. Compensatory changes that maintain activity homeostasis disrupt functional connectivity and increase population sparseness such that a small fraction of neurons dominates population activity. These properties reduce the selectivity of neural response to natural images and render visual recognition memory vulnerable to interference. Deprivation of non-specific visual experiences improves the neural representation and behavioral expression of visual familiarity. In contrast, in non-pathological conditions, deprivation of non-specific visual experiences induces disinhibition, increases excitability, and disrupts visual familiarity. We show that disrupted familiarity occurs when the fraction of high-responsive neurons and the persistence of neural representation of a memory-associated stimulus are not constrained.
Identifiants
pubmed: 36640331
pii: S2211-1247(22)01847-2
doi: 10.1016/j.celrep.2022.111946
pmc: PMC9939293
mid: NIHMS1870512
pii:
doi:
Substances chimiques
Amyloidogenic Proteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
111946Subventions
Organisme : NIA NIH HHS
ID : R01 AG064067
Pays : United States
Informations de copyright
Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests The authors declare no competing interests.
Références
Am J Pathol. 2016 Sep;186(9):2279-91
pubmed: 27423698
J Alzheimers Dis Rep. 2021 Feb 27;5(1):153-160
pubmed: 33981952
Nat Rev Neurosci. 2004 Feb;5(2):97-107
pubmed: 14735113
J Neurosci. 2008 Dec 31;28(53):14537-45
pubmed: 19118188
J Neurosci. 2015 Dec 2;35(48):15916-20
pubmed: 26631472
J Neurosci. 2000 Jun 1;20(11):4050-8
pubmed: 10818140
Neuron. 2018 Apr 4;98(1):75-89.e5
pubmed: 29551491
Ann Neurol. 1991 Oct;30(4):572-80
pubmed: 1789684
Cell. 2017 Oct 5;171(2):456-469.e22
pubmed: 28985566
J Neurosci. 2011 Jan 12;31(2):700-11
pubmed: 21228179
Nat Neurosci. 2015 Aug;18(8):1116-22
pubmed: 26167904
Cell Rep. 2018 Dec 11;25(11):3158-3168.e3
pubmed: 30540947
J Neurosci. 2013 Apr 24;33(17):7245-52
pubmed: 23616533
Science. 2019 Aug 9;365(6453):559-565
pubmed: 31395777
Science. 2002 Oct 25;298(5594):789-91
pubmed: 12399581
Bioinformatics. 2013 Jul 15;29(14):1840-1
pubmed: 23681123
Nat Neurosci. 2018 Jun;21(6):843-850
pubmed: 29760525
Neurotherapeutics. 2017 Jul;14(3):662-676
pubmed: 28560709
Nat Commun. 2020 Jul 16;11(1):3565
pubmed: 32678087
Front Aging Neurosci. 2016 Feb 23;8:31
pubmed: 26941642
Sci Rep. 2019 Oct 16;9(1):14837
pubmed: 31619689
Nat Commun. 2012 Apr 10;3:774
pubmed: 22491322
Neurology. 2010 Oct 12;75(15):1381-7
pubmed: 20938031
Front Cell Neurosci. 2020 Dec 17;14:592607
pubmed: 33408613
Neuron. 2020 May 20;106(4):566-578.e8
pubmed: 32169170
Neuron. 2014 Dec 3;84(5):1023-33
pubmed: 25456500
Neuropsychol Rev. 2014 Sep;24(3):313-31
pubmed: 25115809
J Neurosci. 2017 Mar 29;37(13):3532-3543
pubmed: 28258167
Nat Neurosci. 2020 Jan;23(1):138-151
pubmed: 31844315
J Neurosci. 2015 Aug 12;35(32):11346-57
pubmed: 26269641
Nat Commun. 2021 May 10;12(1):2603
pubmed: 33972518
J Neurosci. 2015 Jun 17;35(24):9205-10
pubmed: 26085642
Annu Rev Vis Sci. 2016 Oct 14;2:85-107
pubmed: 28532362
Cell Rep. 2021 Apr 20;35(3):109008
pubmed: 33882308
Proc Natl Acad Sci U S A. 2012 Oct 16;109(42):E2895-903
pubmed: 22869752
Science. 2008 Sep 19;321(5896):1686-9
pubmed: 18802001
J Alzheimers Dis. 2008 Jul;14(3):313-21
pubmed: 18599957
Front Neurosci. 2018 Feb 02;12:46
pubmed: 29456491
Brain Res. 2019 Mar 15;1707:216-226
pubmed: 30503351
Science. 2016 May 6;352(6286):712-716
pubmed: 27033548
Philos Trans R Soc Lond B Biol Sci. 2016 Aug 5;371(1700):
pubmed: 27377723
PLoS One. 2019 Jan 15;14(1):e0209228
pubmed: 30645585
Neuron. 2003 May 22;38(4):529-45
pubmed: 12765606
Eur J Neurosci. 2018 Feb;47(4):346-357
pubmed: 29357122
Neuron. 2007 Sep 6;55(5):697-711
pubmed: 17785178
J Neurosci. 2017 Dec 6;37(49):11947-11966
pubmed: 29101243
iScience. 2020 Jul 24;23(7):101271
pubmed: 32593000
Nat Neurosci. 2015 Feb;18(2):262-71
pubmed: 25599221
Curr Opin Neurobiol. 2004 Aug;14(4):481-7
pubmed: 15321069
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Biol Cybern. 1998 Jan;78(1):45-56
pubmed: 9518026
Nat Commun. 2018 Jul 24;9(1):2893
pubmed: 30042473
Cell Rep. 2019 Aug 6;28(6):1584-1595.e5
pubmed: 31390571
Nat Neurosci. 2020 Aug;23(8):952-958
pubmed: 32514139
Elife. 2021 Jul 30;10:
pubmed: 34328414
Neuron. 2016 Oct 5;92(1):114-125
pubmed: 27641495
J Neurosci. 2010 Jan 6;30(1):372-81
pubmed: 20053918
Nat Commun. 2019 Nov 26;10(1):5372
pubmed: 31772192
J Neurocytol. 2004 May;33(3):377-87
pubmed: 15475691
Nat Neurosci. 2018 Apr;21(4):463-473
pubmed: 29403035
Nat Commun. 2016 Oct 27;7:13239
pubmed: 27807345
Nat Commun. 2017 Nov 13;8(1):1464
pubmed: 29133888
Cell Rep. 2020 Sep 22;32(12):108169
pubmed: 32966798
Sci Rep. 2021 Mar 23;11(1):6649
pubmed: 33758244
Nat Rev Neurosci. 2016 Dec;17(12):777-792
pubmed: 27829687
Proc Natl Acad Sci U S A. 2018 Feb 6;115(6):E1279-E1288
pubmed: 29358403
Annu Rev Neurosci. 2018 Jul 8;41:277-297
pubmed: 29986165
J Neurosci. 2015 Apr 15;35(15):6221-30
pubmed: 25878292
Front Cell Neurosci. 2020 Jan 14;13:555
pubmed: 32009901
Cell. 2012 Apr 27;149(3):708-21
pubmed: 22541439
Ageing Res Rev. 2021 Aug;69:101372
pubmed: 34029743
Mol Neurodegener. 2020 Sep 14;15(1):53
pubmed: 32921309
Mol Psychiatry. 2020 Dec;25(12):3380-3398
pubmed: 31431685
Commun Biol. 2022 Jan 20;5(1):77
pubmed: 35058544
Curr Opin Neurobiol. 2015 Dec;35:57-65
pubmed: 26151761
Alzheimer Dis Assoc Disord. 2021 Oct-Dec 01;35(4):321-326
pubmed: 34310441
Nat Neurosci. 2012 Oct;15(10):1422-9
pubmed: 22922786
Trends Neurosci. 2012 Jun;35(6):345-55
pubmed: 22579264
Neuron. 2006 Aug 3;51(3):339-49
pubmed: 16880128
Front Neuroanat. 2015 Apr 07;9:36
pubmed: 25904849
Curr Biol. 2016 Apr 4;26(7):956-64
pubmed: 27020746
Cell Rep. 2022 Apr 26;39(4):110751
pubmed: 35476991
Nat Neurosci. 2014 Nov;17(11):1500-9
pubmed: 25151264
Nature. 2012 Aug 16;488(7411):379-83
pubmed: 22878719
Lancet Neurol. 2012 Feb;11(2):170-8
pubmed: 22265212
Neuron. 2016 Jul 20;91(2):356-69
pubmed: 27373832
Neuron. 2012 Apr 26;74(2):361-73
pubmed: 22542188
Brain Res. 2006 Jul 12;1099(1):189-98
pubmed: 16781686
Neuron. 2018 Jan 3;97(1):32-58
pubmed: 29301104
J Microsc. 2006 Dec;224(Pt 3):213-32
pubmed: 17210054
Cell Rep. 2017 Jul 11;20(2):344-355
pubmed: 28700937
J Alzheimers Dis. 2020;78(3):951-964
pubmed: 33074225
Neuron. 2016 Feb 17;89(4):756-69
pubmed: 26853302
Int J Mol Sci. 2021 Sep 17;22(18):
pubmed: 34576197
Eur J Neurol. 2022 May;29(5):1311-1323
pubmed: 34331352
Commun Biol. 2022 Dec 2;5(1):1323
pubmed: 36460716
Neurobiol Dis. 2021 Jul;154:105344
pubmed: 33766652