Differential regulation of parvalbumin and calretinin interneurons in the prefrontal cortex during adolescence

被引:129
作者
Caballero, Adriana [1 ]
Flores-Barrera, Eden [1 ]
Cass, Daryn K. [1 ]
Tseng, Kuei Y. [1 ]
机构
[1] Rosalind Franklin Univ Med & Sci, Chicago Med Sch, Dept Cellular & Mol Pharmacol, N Chicago, IL 60064 USA
基金
美国国家卫生研究院;
关键词
Interneurons; Calcium-binding proteins; Prefrontal cortex; Fast spiking; Non-fast spiking; CALCIUM-BINDING PROTEINS; LOCAL-CIRCUIT NEURONS; VENTRAL HIPPOCAMPAL LESION; GABAERGIC INTERNEURONS; GABA NEURONS; IMMUNOREACTIVE NEURONS; AFFERENT CONNECTIONS; BRAIN-DEVELOPMENT; GENE-EXPRESSION; CEREBRAL-CORTEX;
D O I
10.1007/s00429-013-0508-8
中图分类号
R602 [外科病理学、解剖学]; R32 [人体形态学];
学科分类号
100101 ;
摘要
Determining the normal developmental trajectory of individual GABAergic components in the prefrontal cortex (PFC) during the adolescent transition period is critical because local GABAergic interneurons are thought to play an important role in the functional maturation of cognitive control that occurs in this developmental window. Based on the expression of calcium-binding proteins, three distinctive subtypes of interneurons have been identified in the PFC: parvalbumin (PV)-, calretinin (CR)-, and calbindin (CB)-positive cells. Using biochemical and histochemical measures, we found that the protein level of PV is lowest in juveniles [postnatal days (PD) 25-35] and increases during adolescence (PD 45-55) to levels similar to those observed in adulthood (PD 65-75). In contrast, the protein expression of CR is reduced in adults compared to juvenile and adolescent animals, whereas CB levels remain mostly unchanged across the developmental window studied here. Semi-quantitative immunostaining analyses revealed that the periadolescent upregulation of PV and the loss of the CR signal appear to be attributable to changes in PV- and CR-positive innervation, which are dissociable from the trajectory of PV- and CR-positive cell number. At the synaptic level, our electrophysiological data revealed that a developmental facilitation of spontaneous glutamatergic synaptic inputs onto PV-positive/fast-spiking interneurons parallels the increase in prefrontal PV signal during the periadolescent transition. In contrast, no age-dependent changes in glutamatergic transmission were observed in PV-negative/non fast-spiking interneurons. Together, these findings emphasize that GABAergic inhibitory interneurons in the PFC undergo a dynamic, cell type-specific remodeling during adolescence and provide a developmental framework for understanding alterations in GABAergic circuits that occur in psychiatric disorders.
引用
收藏
页码:395 / 406
页数:12
相关论文
共 63 条
[1]  
ALCANTARA S, 1993, ANAT EMBRYOL, V188, P63
[2]   Trajectories of brain development: point of vulnerability or window of opportunity? [J].
Andersen, SL .
NEUROSCIENCE AND BIOBEHAVIORAL REVIEWS, 2003, 27 (1-2) :3-18
[3]   CALCIUM-BINDING PROTEINS - SELECTIVE MARKERS OF NERVE-CELLS [J].
ANDRESSEN, C ;
BLUMCKE, I ;
CELIO, MR .
CELL AND TISSUE RESEARCH, 1993, 271 (02) :181-208
[4]   Petilla terminology:: nomenclature of features of GABAergic interneurons of the cerebral cortex [J].
Ascoli, Giorgio A. ;
Alonso-Nanclares, Lidia ;
Anderson, Stewart A. ;
Barrionuevo, German ;
Benavides-Piccione, Ruth ;
Burkhalter, Andreas ;
Buzsaki, Gyoergy ;
Cauli, Bruno ;
DeFelipe, Javier ;
Fairen, Alfonso ;
Feldmeyer, Dirk ;
Fishell, Gord ;
Fregnac, Yves ;
Freund, Tamas F. ;
Gardner, Daniel ;
Gardner, Esther P. ;
Goldberg, Jesse H. ;
Helmstaedter, Moritz ;
Hestrin, Shaul ;
Karube, Fuyuki ;
Kisvarday, Zoltan F. ;
Lambolez, Bertrand ;
Lewis, David A. ;
Marin, Oscar ;
Markram, Henry ;
Munoz, Alberto ;
Packer, Adam ;
Petersen, Carl C. H. ;
Rockland, Kathleen S. ;
Rossier, Jean ;
Rudy, Bernardo ;
Somogyi, Peter ;
Staiger, Jochen F. ;
Tamas, Gabor ;
Thomson, Alex M. ;
Toledo-Rodriguez, Maria ;
Wang, Yun ;
West, David C. ;
Yuste, Rafael .
NATURE REVIEWS NEUROSCIENCE, 2008, 9 (07) :557-568
[5]   Functional characteristics of parvalbumin- and cholecystokinin-expressing basket cells [J].
Bartos, Marlene ;
Elgueta, Claudio .
JOURNAL OF PHYSIOLOGY-LONDON, 2012, 590 (04) :669-681
[6]   Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase [J].
Behrens, M. Margarita ;
Ali, Sameh S. ;
Dao, Diep N. ;
Lucero, Jacinta ;
Shekhtman, Grigoriy ;
Quick, Kevin L. ;
Dugan, Laura L. .
SCIENCE, 2007, 318 (5856) :1645-1647
[7]  
Benes FM, 1996, SYNAPSE, V23, P237, DOI 10.1002/(SICI)1098-2396(199608)23:4<237::AID-SYN1>3.0.CO
[8]  
2-8
[9]   GABAergic interneurons: Implications for understanding schizophrenia and bipolar disorder [J].
Benes, FM ;
Berretta, S .
NEUROPSYCHOPHARMACOLOGY, 2001, 25 (01) :1-27
[10]   A Developmental Perspective on Executive Function [J].
Best, John R. ;
Miller, Patricia H. .
CHILD DEVELOPMENT, 2010, 81 (06) :1641-1660