Synapsin I Controls Synaptic Maturation of Long-Range Projections in the Lateral Amygdala in a Targeted Selective Fashion.

amygdala cortical projections interneurons synapse maturation synapsin thalamic projections

Journal

Frontiers in cellular neuroscience
ISSN: 1662-5102
Titre abrégé: Front Cell Neurosci
Pays: Switzerland
ID NLM: 101477935

Informations de publication

Date de publication:
2019
Historique:
received: 09 12 2018
accepted: 01 05 2019
entrez: 6 6 2019
pubmed: 6 6 2019
medline: 6 6 2019
Statut: epublish

Résumé

The amygdala, and more precisely its lateral nucleus, is thought to attribute emotional valence to external stimuli by generating long-term plasticity changes at long-range projections to principal cells. Aversive experience has also been shown to modify pre- and post-synaptic markers in the amygdala, suggesting their possible role in the structural organization of adult amygdala networks. Here, we focused on how the maturation of cortical and thalamic long-range projections occurs on principal neurons and interneurons in the lateral amygdala (LA). We performed dual electrophysiological recordings of identified cells in juvenile and adult GAD67-GFP mice after independent stimulation of cortical and thalamic afferent systems. The results demonstrate that synaptic strengthening occurs during development at synapses projecting to LA principal neurons, but not interneurons. As synaptic strengthening underlies fear conditioning which depends, in turn, on presence and increasing expression of synapsin I, we tested if synapsin I contributes to synaptic strengthening during development. Interestingly, the physiological synaptic strengthening of cortical and thalamic synapses projecting to LA principal neurons was virtually abolished in synapsin I knockout mice, but not differences were observed in the excitatory projections to interneurons. Immunohistochemistry analysis showed that the presence of synapsin I is restricted to excitatory contacts projecting to principal neurons in LA of adult mice. These results indicate that synapsin I is a key regulator of the maturation of synaptic connectivity in this brain region and that is expression is dependent on postsynaptic identity.

Identifiants

pubmed: 31164805
doi: 10.3389/fncel.2019.00220
pmc: PMC6536628
doi:

Types de publication

Journal Article

Langues

eng

Pagination

220

Références

Annu Rev Neurosci. 2000;23:155-84
pubmed: 10845062
J Neurophysiol. 2001 Feb;85(2):714-23
pubmed: 11160506
Annu Rev Neurosci. 2001;24:897-931
pubmed: 11520922
Learn Mem. 2001 Sep-Oct;8(5):229-42
pubmed: 11584069
Neuron. 2002 Apr 11;34(2):289-300
pubmed: 11970870
J Comp Neurol. 2002 Aug 26;450(3):241-55
pubmed: 12209853
Cell Mol Neurobiol. 2003 Oct;23(4-5):727-38
pubmed: 14514027
J Comp Neurol. 2003 Dec 1;467(1):60-79
pubmed: 14574680
Nature. 2003 Dec 18;426(6968):841-5
pubmed: 14685239
J Med Genet. 2004 Mar;41(3):183-6
pubmed: 14985377
Neuron. 2005 Jan 6;45(1):119-31
pubmed: 15629707
Science. 2005 Apr 1;308(5718):83-8
pubmed: 15746389
Neuron. 2005 Oct 20;48(2):175-87
pubmed: 16242399
Science. 2007 Apr 20;316(5823):457-60
pubmed: 17446403
J Neurosci. 2007 Oct 10;27(41):10947-56
pubmed: 17928436
Neuroscience. 2009 Jan 12;158(1):231-41
pubmed: 18606212
J Cell Sci. 2008 Sep 15;121(Pt 18):3042-51
pubmed: 18713831
Cereb Cortex. 2009 Jun;19(6):1422-39
pubmed: 19020204
Science. 2009 Mar 13;323(5920):1492-6
pubmed: 19286560
Neuron. 2009 Jun 25;62(6):757-71
pubmed: 19555645
Cell Mol Life Sci. 2010 May;67(9):1383-96
pubmed: 20035364
Genes Brain Behav. 2010 Apr;9(3):257-68
pubmed: 20050925
Prog Neurobiol. 2010 Aug;91(4):313-48
pubmed: 20438797
PLoS One. 2010 Jun 21;5(6):e11236
pubmed: 20574537
PLoS One. 2010 Jul 02;5(7):e11399
pubmed: 20625482
Hum Mol Genet. 2011 Jun 15;20(12):2297-307
pubmed: 21441247
J Cell Sci. 2011 Nov 1;124(Pt 21):3643-53
pubmed: 22045728
Front Behav Neurosci. 2012 Apr 10;6:16
pubmed: 22514524
PLoS One. 2012;7(4):e35320
pubmed: 22563382
Proc Natl Acad Sci U S A. 2012 Oct 2;109(40):16318-23
pubmed: 22988092
Hum Mol Genet. 2013 Jun 1;22(11):2186-99
pubmed: 23406870
Nat Commun. 2013;4:1512
pubmed: 23443540
J Neurophysiol. 2013 Aug;110(4):926-41
pubmed: 23719209
J Neurosci. 2013 Aug 21;33(34):13805-19
pubmed: 23966701
PLoS Biol. 2014 Mar 25;12(3):e1001820
pubmed: 24667537
Nature. 2014 May 22;509(7501):453-8
pubmed: 24814341
Nature. 2014 Jul 31;511(7511):596-600
pubmed: 25043046
Brain Struct Funct. 2016 Mar;221(2):839-54
pubmed: 25381464
Nature. 2015 Jan 15;517(7534):284-92
pubmed: 25592533
Curr Mol Med. 2015;15(2):146-67
pubmed: 25732149
Epilepsia. 2015 Jul;56(7):1098-108
pubmed: 26096837
J Physiol. 2015 Oct 1;593(19):4387-409
pubmed: 26227545
Mol Brain. 2016 Jan 28;9:11
pubmed: 26822304
Nat Commun. 2016 May 24;7:11475
pubmed: 27215672
Epilepsia. 2018 Nov;59(11):2162-2163
pubmed: 30390306
J Comp Neurol. 1982 Dec 10;212(3):293-312
pubmed: 6185547
Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9230-4
pubmed: 7568107
Neuron. 1997 Sep;19(3):613-24
pubmed: 9331352
Int J Dev Neurosci. 1997 Oct;15(6):755-65
pubmed: 9402226
Prog Neurobiol. 1998 Jun;55(3):257-332
pubmed: 9643556

Auteurs

Eleonora Lugarà (E)

Department of Experimental Medicine, Section of Human Physiology, University of Genova, Genoa, Italy.
Center for Synaptic Neuroscience and Technology, Istituto Italiano di Tecnologia, Genoa, Italy.

Antonio De Fusco (A)

Department of Experimental Medicine, Section of Human Physiology, University of Genova, Genoa, Italy.
Center for Synaptic Neuroscience and Technology, Istituto Italiano di Tecnologia, Genoa, Italy.

Gabriele Lignani (G)

Center for Synaptic Neuroscience and Technology, Istituto Italiano di Tecnologia, Genoa, Italy.

Fabio Benfenati (F)

Center for Synaptic Neuroscience and Technology, Istituto Italiano di Tecnologia, Genoa, Italy.
IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Yann Humeau (Y)

Team Synapse in Cognition, Institut Interdisciplinaire de Neuroscience, Centre National de la Recherche Scientifique CNRS UMR5297, Université de Bordeaux, Bordeaux, France.

Classifications MeSH