Maturation of PNN and ErbB4 Signaling in Area CA2 during Adolescence Underlies the Emergence of PV Interneuron Plasticity and Social Memory

被引:53
作者
Dominguez, Soledad [1 ]
Rey, Christophe Clement [2 ]
Therreau, Ludivine [1 ,4 ]
Fanton, Aurelien [1 ]
Massotte, Dominique [3 ]
Verret, Laure [2 ]
Piskorowski, Rebecca Ann [1 ]
Chevaleyre, Vivien [1 ]
机构
[1] Inst Psychiat & Neurosci Paris, INSERM UMR 1266, Team Synapt Plast & Neural Networks, 102-108 Rue Sante, F-75014 Paris, France
[2] Toulouse Univ, Res Ctr Anim Cognit, Ctr Integrat Biol, CNRS,UPS, Toulouse, France
[3] Inst Neurosci Cellulaires & Integrat, CNRS UPR 3212, 5 Rue Blaise Pascal, F-67084 Strasbourg, France
[4] Ctr Rech Sci Vivant, Inovar, 251 Rue St Jacques, F-75005 Paris, France
关键词
DELTA-OPIOID RECEPTORS; PARVALBUMIN-CONTAINING NEURONS; FAST-SPIKING INTERNEURONS; PERINEURONAL NETS; EXTRACELLULAR-MATRIX; EXCITATORY SYNAPSES; SYNAPTIC PLASTICITY; HIPPOCAMPUS; REGION; SCHIZOPHRENIA;
D O I
10.1016/j.celrep.2019.09.044
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Adolescence is a vulnerable period characterized by major cognitive changes. The mechanisms underlying the emergence of new cognitive functions are poorly understood. We find that a long-term depression of inhibitory transmission (iLTD) from parvalbumin-expressing (PV+) interneurons in the hippocampal area Cornu Ammonis 2 (CA2) is absent in young mice but emerges at the end of adolescence. We demonstrate that the maturation of both the perineuronal net (PNN) and signaling through ErbB4 is required for this plasticity. Furthermore, we demonstrate that social recognition memory displays the same age dependence as iLTD and is impaired by targeted degradation of the PNN or iLTD blockade in area CA2. Our data reveal an unusual developmental rule for plasticity at the PV+ interneuron transmission in area CA2 and indicate that this plasticity is involved in the emergence of higher cognitive function, such as social memory formation, in late adolescence.
引用
收藏
页码:1099 / +
页数:18
相关论文
共 53 条
[1]   Ontogeny of neural circuits underlying spatial memory in the rat [J].
Ainge, James A. ;
Langston, Rosamund F. .
FRONTIERS IN NEURAL CIRCUITS, 2012, 6
[2]   Genetic Labeling Reveals Novel Cellular Targets of Schizophrenia Susceptibility Gene: Distribution of GABA and Non-GABA ErbB4-Positive Cells in Adult Mouse Brain [J].
Bean, Jonathan C. ;
Lin, Thiri W. ;
Sathyamurthy, Anupama ;
Liu, Fang ;
Yin, Dong-Min ;
Xiong, Wen-Cheng ;
Mei, Lin .
JOURNAL OF NEUROSCIENCE, 2014, 34 (40) :13549-13566
[3]   Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia [J].
Berretta, Sabina ;
Pantazopoulos, Harry ;
Markota, Matej ;
Brown, Christopher ;
Batzianouli, Eleni T. .
SCHIZOPHRENIA RESEARCH, 2015, 167 (1-3) :18-27
[4]   Perineuronal nets and schizophrenia: The importance of neuronal coatings [J].
Bitanihirwe, Byron K. Y. ;
Woo, Tsung-Ung W. .
NEUROSCIENCE AND BIOBEHAVIORAL REVIEWS, 2014, 45 :85-99
[5]   The social brain in adolescence [J].
Blakemore, Sarah-Jayne .
NATURE REVIEWS NEUROSCIENCE, 2008, 9 (04) :267-277
[6]   Distribution of interneurons in the CA2 region of the rat hippocampus [J].
Botcher, Nicola A. ;
Falck, Joanne E. ;
Thomson, Alex M. ;
Mercer, Audrey .
FRONTIERS IN NEUROANATOMY, 2014, 8
[7]   Proteolytic Remodeling of Perineuronal Nets: Effects on Synaptic Plasticity and Neuronal Population Dynamics [J].
Bozzelli, P. Lorenzo ;
Alaiyed, Seham ;
Kim, Eunyoung ;
Villapol, Sonia ;
Conant, Katherine .
NEURAL PLASTICITY, 2018, 2018
[8]   Region and lamina-specific distribution of extracellular matrix proteoglycans, hyaluronan and tenascin-R in the mouse hippocampal formation [J].
Brückner, G ;
Grosche, J ;
Hartlage-Rübsamen, M ;
Schmidt, S ;
Schachner, M .
JOURNAL OF CHEMICAL NEUROANATOMY, 2003, 26 (01) :37-50
[9]   The neuregulin signaling pathway and schizophrenia: From genes to synapses and neural circuits [J].
Buonanno, Andres .
BRAIN RESEARCH BULLETIN, 2010, 83 (3-4) :122-131
[10]   Perineuronal nets protect fast-spiking interneurons against oxidative stress [J].
Cabungcal, Jan-Harry ;
Steullet, Pascal ;
Morishita, Hirofumi ;
Kraftsik, Rudolf ;
Cuenod, Michel ;
Hensch, Takao K. ;
Do, Kim Q. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2013, 110 (22) :9130-9135