title: Anatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets.
abstract: Large morphological sex differences in the vertebrate brain were initially identified in song control nuclei of oscines. Besides gross differences between volumes of nuclei in males and females, sex differences also concern the size and dendritic arborization of neurons and various neurochemical markers, such as the calcium-binding protein parvalbumin (PV). Perineuronal nets (PNN) of the extracellular matrix are aggregates of different compounds, mainly chondroitin sulfate proteoglycans, that surround subsets of neurons, often expressing PV. PNN develop in zebra finches song control nuclei around the end of the sensitive period for song learning and tutor deprivation, known to delay the end of the song learning sensitive period, decreases the numbers of PNN in HVC. We demonstrate here the existence in zebra finches of a major sex difference (males > females) affecting the number of PNN (especially those surrounding PV-positive cells) in HVC and to a smaller extent the robust nucleus of the arcopallium, RA, the two main nuclei controlling song production. These differences were not present in Area X and LMAN, the lateral magnocellular nucleus of the anterior nidopallium. A dense expression of material immunoreactive for chondroitin sulfate was also detected in several nuclei of the auditory and visual pathways. This material was often organized in perineuronal rings but quantification of these PNN did not reveal any sex difference with the exception that the percentage of PNN surrounding PV-ir cells in the dorsal lateral mesencephalic nucleus, MLd, was larger in females than in males, a sex difference in the opposite direction compared to what is seen in HVC and RA. These data confirm and extend previous studies demonstrating the sex difference affecting PNN in HVC-RA by showing that this sex difference is anatomically specific and does not concern visual or auditory pathways.
authors.affiliation: GIGA Neurosciences, Research group in Behavioral Neuroendocrinology, University of Liège, Liège, Belgium.
authors.forename: Gilles
authors.initials: G
authors.lastname: Cornez
authors.affiliation: GIGA Neurosciences, Research group in Behavioral Neuroendocrinology, University of Liège, Liège, Belgium.
authors.forename: Sita M
authors.initials: SM
authors.lastname: ter Haar
authors.affiliation: GIGA Neurosciences, Research group in Behavioral Neuroendocrinology, University of Liège, Liège, Belgium.
authors.forename: Charlotte A
authors.initials: CA
authors.lastname: Cornil
authors.affiliation: GIGA Neurosciences, Research group in Behavioral Neuroendocrinology, University of Liège, Liège, Belgium.
authors.forename: Jacques
authors.initials: J
authors.lastname: Balthazart
mesh_terms: D000818:Animals; D030161:Avian Proteins / Q000378:metabolism; D001921:Brain / Q000166:cytology / Q000378:metabolism; D005260:Female; D046369:Finches / Q000033:anatomy & histology*; D008297:Male; D009415:Nerve Net / Q000166:cytology / Q000378:metabolism*; D009473:Neuronal Plasticity; D010320:Parvalbumins / Q000378:metabolism; D012727:Sex Characteristics; D014828:Vocalization, Animal
chemical_list: D030161:Avian Proteins; D010320:Parvalbumins
references.citation: Brain Res. 1983 Dec;313(1):7-18
references.pmid: 6661666
references.citation: PLoS One. 2012;7(1):e29457
references.pmid: 22238614
references.citation: Neuroscience. 1991;40(3):853-69
references.pmid: 2062443
references.citation: Psychoneuroendocrinology. 1991;16(1-3):105-9
references.pmid: 1961834
references.citation: J Neurosci. 1993 Apr;13(4):1654-63
references.pmid: 8385206
references.citation: J Neurobiol. 1997 Nov;33(5):602-18
references.pmid: 9369462
references.citation: Neuroreport. 1998 Sep 14;9(13):3047-52
references.pmid: 9804314
references.citation: Behav Brain Res. 1998 Nov;96(1-2):135-50
references.pmid: 9821550
references.citation: Behav Brain Res. 1998 Nov;96(1-2):151-9
references.pmid: 9821551
references.citation: Trends Neurosci. 1998 Dec;21(12):510-5
references.pmid: 9881847
references.citation: J Neuroendocrinol. 1999 Feb;11(2):77-84
references.pmid: 10048462
references.citation: Microsc Res Tech. 2001 Sep 15;54(6):327-34
references.pmid: 11668646
references.citation: Nature. 2002 Apr 11;416(6881):636-40
references.pmid: 11948352
references.citation: Nature. 2002 May 16;417(6886):351-8
references.pmid: 12015616
references.citation: Science. 2002 Nov 8;298(5596):1248-51
references.pmid: 12424383
references.citation: Ment Retard Dev Disabil Res Rev. 2003;9(3):135-48
references.pmid: 12953292
references.citation: J Neurobiol. 2004 May;59(2):247-58
references.pmid: 15085541
references.citation: J Comp Neurol. 2004 May 24;473(2):194-212
references.pmid: 15101089
references.citation: J Comp Neurol. 2004 May 31;473(3):377-414
references.pmid: 15116397
references.citation: Neuron. 2004 Sep 30;44(1):5-21
references.pmid: 15450156
references.citation: Science. 1981 Dec 18;214(4527):1368-70
references.pmid: 7313697
references.citation: J Comp Neurol. 1982 Jun 1;207(4):344-57
references.pmid: 7119147
references.citation: Science. 1976 Oct 8;194(4261):211-3
references.pmid: 959852
references.citation: Brain Res. 1979 Dec 7;178(1):143-60
references.pmid: 497857
references.citation: Brain Res. 1979 Dec 7;178(1):201-6
references.pmid: 91415
references.citation: Brain Res. 1980 May 12;189(2):429-36
references.pmid: 7370785
references.citation: Trends Neurosci. 2005 Jul;28(7):353-63
references.pmid: 15935486
references.citation: Proc Biol Sci. 2005 Oct 7;272(1576):2089-96
references.pmid: 16191621
references.citation: J Comp Neurol. 2006 Feb 10;494(5):784-91
references.pmid: 16374807
references.citation: Proc Natl Acad Sci U S A. 2006 Jan 24;103(4):1088-93
references.pmid: 16418265
references.citation: Proc Natl Acad Sci U S A. 2006 May 30;103(22):8517-22
references.pmid: 16709670
references.citation: Nat Rev Neurosci. 2006 May;7(5):347-57
references.pmid: 16760915
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2007 Feb;193(2):201-15
references.pmid: 17066303
references.citation: Dev Neurobiol. 2007 Apr;67(5):570-88
references.pmid: 17443809
references.citation: Brain Res Rev. 2007 Apr;54(1):1-18
references.pmid: 17222456
references.citation: J Neurosci. 2007 May 16;27(20):5405-13
references.pmid: 17507562
references.citation: Eur J Neurosci. 2008 Dec;28(12):2475-85; discussion 2474
references.pmid: 19032586
references.citation: Hear Res. 2009 Jun;252(1-2):49-55
references.pmid: 19397967
references.citation: J Neurosci. 2009 Oct 14;29(41):12878-85
references.pmid: 19828802
references.citation: Learn Mem. 2009 Nov;16(11):655-69
references.pmid: 19850665
references.citation: J Neurosci. 2009 Oct 28;29(43):13557-65
references.pmid: 19864568
references.citation: Acta Neurobiol Exp (Wars). 2009;69(4):564-77
references.pmid: 20048772
references.citation: Curr Opin Neurobiol. 2009 Dec;19(6):654-60
references.pmid: 19892546
references.citation: Eur J Neurosci. 2009 Dec 3;30(11):2053-63
references.pmid: 20128844
references.citation: Neurosci Res. 2010 Sep;68(1):22-34
references.pmid: 20566402
references.citation: J Chem Neuroanat. 2010 Nov;40(3):243-7
references.pmid: 20621181
references.citation: Science. 2011 Nov 4;334(6056):666-70
references.pmid: 22053048
references.citation: J Neurophysiol. 2012 Feb;107(4):1142-56
references.pmid: 22157116
references.citation: Cell Tissue Res. 2012 Jul;349(1):147-60
references.pmid: 22437874
references.citation: PLoS One. 2013;8(5):e63239
references.pmid: 23650558
references.citation: Curr Eye Res. 2015 Feb;40(2):110-27
references.pmid: 25153712
references.citation: Gen Comp Endocrinol. 2015 May 1;215:61-75
references.pmid: 25260250
references.citation: J Exp Zool. 1975 Mar;191(3):309-26
references.pmid: 1092802
references.citation: J Comp Neurol. 1989 Jun 15;284(3):337-49
references.pmid: 2474004
references.citation: Nature. 2005 Feb 10;433(7026):638-43
references.pmid: 15703748
references.citation: Neuroimage. 2005 May 1;25(4):1242-55
references.pmid: 15850742
references.citation: J Neurobiol. 2000 Jan;42(1):1-13
references.pmid: 10623896
references.citation: Nat Neurosci. 2001 Feb;4(2):170-5
references.pmid: 11175878
references.citation: Brain Res. 2001 Nov 2;917(2):235-52
references.pmid: 11640910
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2012 Jan;198(1):61-8
references.pmid: 21987264
references.citation: J Comp Neurol. 1976 Feb 15;165(4):457-86
references.pmid: 1262540