Precise Long-Range Microcircuit-to-Microcircuit Communication Connects the Frontal and Sensory Cortices in the Mammalian Brain.
columnar microcircuit
cortical circuit
excitatory neuron clone
in utero retroviral labeling
long-range circuit
quadruple whole-cell recording
rabies virus tracing
top-down modulation
Journal
Neuron
ISSN: 1097-4199
Titre abrégé: Neuron
Pays: United States
ID NLM: 8809320
Informations de publication
Date de publication:
23 10 2019
23 10 2019
Historique:
received:
31
12
2018
revised:
06
05
2019
accepted:
27
06
2019
pubmed:
3
8
2019
medline:
9
4
2020
entrez:
3
8
2019
Statut:
ppublish
Résumé
The frontal area of the cerebral cortex provides long-range inputs to sensory areas to modulate neuronal activity and information processing. These long-range circuits are crucial for accurate sensory perception and complex behavioral control; however, little is known about their precise circuit organization. Here we specifically identified the presynaptic input neurons to individual excitatory neuron clones as a unit that constitutes functional microcircuits in the mouse sensory cortex. Interestingly, the long-range input neurons in the frontal but not contralateral sensory area are spatially organized into discrete vertical clusters and preferentially form synapses with each other over nearby non-input neurons. Moreover, the assembly of distant presynaptic microcircuits in the frontal area depends on the selective synaptic communication of excitatory neuron clones in the sensory area that provide inputs to the frontal area. These findings suggest that highly precise long-range reciprocal microcircuit-to-microcircuit communication mediates frontal-sensory area interactions in the mammalian cortex.
Identifiants
pubmed: 31371111
pii: S0896-6273(19)30598-7
doi: 10.1016/j.neuron.2019.06.028
pmc: PMC6813886
mid: NIHMS1535278
pii:
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
385-401.e3Subventions
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA024681
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH101382
Pays : United States
Informations de copyright
Copyright © 2019 Elsevier Inc. All rights reserved.
Références
Science. 2015 Nov 27;350(6264):aac9462
pubmed: 26612957
Neuron. 2013 Jan 23;77(2):346-60
pubmed: 23352170
Neuron. 2016 Dec 21;92(6):1368-1382
pubmed: 28009277
Neuron. 1988 Oct;1(8):635-47
pubmed: 3272182
Cereb Cortex. 2014 Aug;24(8):2237-48
pubmed: 23547136
J Comp Neurol. 2003 Sep 8;464(1):98-103
pubmed: 12866130
Nature. 2001 Feb 8;409(6821):714-20
pubmed: 11217860
Neuron. 2009 Jan 29;61(2):301-16
pubmed: 19186171
Nature. 2012 Jun 06;486(7401):41-2
pubmed: 22678277
Nature. 2009 Mar 26;458(7237):501-4
pubmed: 19204731
Nat Rev Neurosci. 2002 Mar;3(3):201-15
pubmed: 11994752
Nature. 1999 Oct 14;401(6754):699-703
pubmed: 10537108
Cereb Cortex. 1991 Jan-Feb;1(1):1-47
pubmed: 1822724
Neuron. 2008 Oct 9;60(1):84-96
pubmed: 18940590
Adv Virus Res. 2011;79:165-202
pubmed: 21601048
Nature. 2012 Dec 13;492(7428):247-51
pubmed: 23143335
Science. 2007 Mar 30;315(5820):1860-2
pubmed: 17395832
Nat Rev Neurosci. 2005 Nov;6(11):877-88
pubmed: 16261181
Ann N Y Acad Sci. 2013 Aug;1296:88-107
pubmed: 23909769
Elife. 2018 Sep 26;7:
pubmed: 30256194
Neuron. 2012 Jul 12;75(1):65-72
pubmed: 22794261
Neuron. 2007 Jun 7;54(5):677-96
pubmed: 17553419
Science. 1988 Jul 8;241(4862):170-6
pubmed: 3291116
Science. 2014 Aug 8;345(6197):660-5
pubmed: 25104383
Annu Rev Neurosci. 2004;27:649-77
pubmed: 15217346
Neuron. 2012 Jul 12;75(1):4-5
pubmed: 22794254
Annu Rev Neurosci. 1995;18:193-222
pubmed: 7605061
J Comp Neurol. 1972 May;145(1):61-83
pubmed: 4624784
Neuron. 2015 Jun 3;86(5):1304-16
pubmed: 26004915
J Neurophysiol. 1957 Jul;20(4):408-34
pubmed: 13439410
Science. 1988 Sep 9;241(4871):1342-5
pubmed: 3137660
Cell. 2014 Nov 6;159(4):775-88
pubmed: 25417155
Science. 2012 Feb 24;335(6071):989-93
pubmed: 22363012
Nat Neurosci. 2015 Nov;18(11):1687-1697
pubmed: 26457553
Nature. 2012 May 02;486(7401):118-21
pubmed: 22678292
Nat Rev Neurosci. 2013 Nov;14(11):755-69
pubmed: 24105342
Nature. 2012 May 02;486(7401):113-7
pubmed: 22678291
Nat Neurosci. 2013 Nov;16(11):1662-70
pubmed: 24097044
Genes Dev. 1998 Dec 1;12(23):3675-85
pubmed: 9851974
Nat Neurosci. 2011 Jan;14(1):100-7
pubmed: 21076426
Proc Natl Acad Sci U S A. 2013 Mar 19;110(12):E1152-61
pubmed: 23487772
Annu Rev Neurosci. 2009;32:149-84
pubmed: 19555289
Eur J Neurosci. 2010 Jun;31(12):2221-33
pubmed: 20550566
Science. 1996 Nov 15;274(5290):1133-8
pubmed: 8895456
Science. 2013 Mar 15;339(6125):1290-5
pubmed: 23493706
Nature. 2014 Sep 11;513(7517):189-94
pubmed: 25162524
J Neurosci Methods. 2010 Dec 15;194(1):2-20
pubmed: 20004688
J Neurosci. 2015 Jun 17;35(24):8979-85
pubmed: 26085623
J Neurosci. 2013 Sep 4;33(36):14342-53
pubmed: 24005287
Nat Neurosci. 2016 Dec;19(12):1658-1664
pubmed: 27618309
Curr Opin Neurobiol. 2008 Dec;18(6):617-23
pubmed: 19349161
Cell. 2014 Feb 27;156(5):1096-111
pubmed: 24581503
Neuron. 2011 Oct 6;72(1):111-23
pubmed: 21982373
Nat Neurosci. 2016 Dec;19(12):1733-1742
pubmed: 27749828
Annu Rev Neurosci. 2001;24:167-202
pubmed: 11283309
Nature. 2004 Oct 14;431(7010):775-81
pubmed: 15483598
Brain. 1997 Apr;120 ( Pt 4):701-22
pubmed: 9153131
Philos Trans R Soc Lond B Biol Sci. 2014 Nov 5;369(1655):null
pubmed: 25267814
Neuropsychol Rev. 2005 Jun;15(2):59-71
pubmed: 16211466
Science. 2016 Jun 10;352(6291):1315-8
pubmed: 27229145
Nat Rev Neurosci. 2013 May;14(5):350-63
pubmed: 23595013
J Physiol. 1963 Mar;165:559-68
pubmed: 13955384
Nat Rev Neurosci. 2008 Apr;9(4):255-66
pubmed: 18354398
Neuron. 2007 Mar 1;53(5):639-47
pubmed: 17329205
J Neurosci. 1996 Nov 15;16(22):7376-89
pubmed: 8929444
Nat Neurosci. 2015 Mar;18(3):393-401
pubmed: 25664912
Neuron. 2015 Jun 3;86(5):1159-66
pubmed: 26050035
Proc R Soc Lond B Biol Sci. 1977 Jul 28;198(1130):1-59
pubmed: 20635