Perineuronal nets; European starling; Zebra finch; canary; song control nuclei; parvalbumin; Song plasticity
Abstract :
[en] Perineuronal nets (PNN) are aggregations of chondroitin sulfate proteoglycans surrounding the soma and proximal processes of neurons, mostly GABAergic interneurons expressing parvalbumin. They limit the plasticity of their afferent synaptic connections. In zebra finches PNN develop in an experience-dependent manner in the song control nuclei HVC and RA (nucleus robustus arcopallialis) when young birds crystallize their song. Because songbird species that are open-ended learners tend to recapitulate each year the different phases of song learning until their song crystallizes at the beginning of the breeding season, we tested whether seasonal changes in PNN expression would be found in the song control nuclei of a seasonally breeding species such as the European starling. Only minimal changes in PNN densities and total number of cells surrounded by PNN were detected. However, comparison of the density of PNN and of PNN surrounding parvalbumin-positive cells revealed that these structures are far less numerous in starlings that show extensive adult vocal plasticity, including learning of new songs throughout the year, than in the closed-ended learner zebra finches. Canaries that also display some vocal plasticity across season but were never formally shown to learn new songs in adulthood were intermediate in this respect. Together these data suggest that establishment of PNN around parvalbumin-positive neurons in song control nuclei has diverged during evolution to control the different learning capacities observed in songbird species. This differential expression of PNN in different songbird species could represent a key cellular mechanism mediating species variation between closed-ended and open-ended learning strategies.
Research center :
Giga-Neurosciences - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Cornez, Gilles ; Université de Liège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Madison, F.N.
Van der Linden, A.
Cornil, Charlotte ; Université de Liège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Yoder, K.M.
Ball, G.F.
Balthazart, Jacques ; Université de Liège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Language :
English
Title :
Perineuronal nets and vocal plasticity in songbirds: a proposed mechanism to explain the difference between closed-ended and open-ended learning
Publication date :
07 February 2017
Journal title :
Developmental Neurobiology
ISSN :
1932-8451
eISSN :
1932-846X
Publisher :
John Wiley & Sons, Hoboken, United States - New Jersey
Volume :
77
Issue :
8
Pages :
975-994
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
BELSPO - SPP Politique scientifique - Service Public Fédéral de Programmation Politique scientifique
Alvarez-Borda B, Nottebohm F. 2002. Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain. J Neurosci 22:8684–8690.
Alvarez-Buylla A, Kirn JR. 1997. Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurobiol 33:585–601.
Alward BA, Balthazart J, Ball GF. 2013. Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate. Proc Natl Acad Sci U S A 110:19573–19578.
Alward BA, Madison FN, Parker SE, Balthazart J, Ball GF. 2016. Pleiotropic control by testosterone of a learned vocal behavior and its underlying neuroplasticity(1,2,3). eNeuro 3:15.
Baig S, Wilcock GK, Love S. 2005. Loss of perineuronal net N-acetylgalactosamine in Alzheimer's disease. Acta Neuropathol 110:393–401.
Balmer TS, Carels VM, Frisch JL, Nick TA. 2009. Modulation of perineuronal nets and parvalbumin with developmental song learning. J Neurosci 29:12878–12885.
Balthazart J, Ball GF. 2016. Endocrine and social regulation of adult neurogenesis in songbirds. Front Neuroendocrinol 41:3–22.
Balthazart J, Boseret G, Konkle ATM, Hurley LL, Ball GF. 2008. Doublecortin as a marker of adult neuroplasticity in the canary song control nucleus HVC. Eur J Neurosci 27:801–817.
Beecher MD, Brenowitz EA. 2005. Functional aspects of song learning in songbirds. Trends Ecol Evol 20:143–149.
Bernard DJ, Ball GF. 1995. Two histological markers reveal a similar photoperiodic difference in the volume of the high vocal center in male European starlings. J Comp Neurol 360:726–734.
Bernard DJ, Eens M, Ball GF. 1996. Age- and behavior-related variation in volumes of song control nuclei in male European starlings. J Neurobiol 30:329–339.
Best BJ, Day NF, Larson GT, Carels VM, Nick TA. 2012. Vocal effects of perineuronal net destruction in adult zebra finc. Abst. Soc for Neurosc Nbr 303.18.
Bidmon HJ, Jancsik V, Schleicher A, Hagemann G, Witte OW, Woodhams P, Zilles K. 1998. Structural alterations and changes in cytoskeletal proteins and proteoglycans after focal cortical ischemia. Neuroscience 82:397–420.
Böhner J. 1990. Early acquisition of song in the zebra finch, Taeniopygia guttata. Anim Behav 39:369–374.
Böhner J, Chaiken M, Ball GF, Marler P. 1990. Song acquisition in photosensitive and photorefractory male European starlings. Horm Behav 24:582–594.
Boseret G, Carere C, Ball GF, Balthazart J. 2006. Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria). J Neurobiol 66:1044–1060.
Bottjer SW, Miesner EA, Arnold AP. 1984. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224:901–903.
Brainard MS, Doupe AJ. 2002. What songbirds teach us about learning. Nat: Insight Rev 417:351–358.
Brenowitz EA. 2004. Plasticity of the adult avian song control system. Ann N Y Acad Sci 1016:560–585.
Brenowitz EA. 2008. Plasticity of the song control system in adult birds. In: Zeigler HP, Marler P, editors. Neuroscience of Birdsong. Cambridge: Cambridge University Press, pp 332–349.
Brenowitz EA, Beecher MD. 2005. Song learning in birds: Diversity and plasticity, opportunities and challenges. Trends Neurosci 28:127–132.
Brenowitz EA, Larson TA. 2015. Neurogenesis in the adult avian song-control system. Cold Spring Harbor Perspect Biol 7:e019000.
Bruckner G, Hausen D, Hartig W, Drlicek M, Arendt T, Brauer K. 1999. Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer's disease. Neuroscience 92:791–805.
Chaiken M, Bohner J, Marler P. 1994. Repertoire turnover and the timing of song acquisition in European starlings. Behaviour 128:25–39.
Cornez G, ter Haar SM, Cornil CA, Balthazart J. 2015. Anatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets. PloS One 10:e0123199.
Cornez G, Shevchouk O, Madison FN, Ball GF, Van Der Linden A, Cornil CA, Balthazart J. 2016. Seasonal changes and steroid control of perineuronal nets in the song control system. Abstract of the International Symposium on Avian Endocirnology, Niagara Falls Canada, October 2016.
Dawson A, King VM, Bentley GE, Ball GF. 2001. Photoperiodic control of seasonality in birds. J Biol Rhythms 16:365–380.
De Groof G, Verhoye M, Van Meir V, Balthazart J, Van Der Linden A. 2008. Seasonal rewiring of the songbird brain: An in vivo MRI study. Eur J Neurosci 28:2475–2485.
Deepa SS, Carulli D, Galtrey C, Rhodes K, Fukuda J, Mikami T, Sugahara K, et al. 2006. Composition of perineuronal net extracellular matrix in rat brain: A different disaccharide composition for the net-associated proteoglycans. J Biol Chem 281:17789–17800.
Eens M. 1997. Understanding the complex song of the European starling: An integrated ethological approach. Adv Study Anim Behav 26:355–434.
Eens M, Pinxten R, Verheyen RF. 1992. No overlap in song repertoire size between yearling and older starlings Sturnus vulgaris. Ibis 134:72–76.
Feare CJ. 1984. The Starling. Oxford: Oxford Press.
Galtrey CM, Fawcett JW. 2007. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 54:1–18.
Geberzahn N, Hultsch H. 2003. Long-time storage of song types in birds: Evidence from interactive playbacks. Proc Biol Sci R Soc 270:1085–1090.
Gill KE, Madison FN, Akins CK. 2015. Cocaine-induced sensitization correlates with testosterone in male Japanese quail but not with estradiol in female Japanese quail. Horm Behav 67:21–27.
Gogolla N, Caroni P, Luthi A, Herry C. 2009. Perineuronal nets protect fear memories from erasure. Science 325:1258–1261.
Hara E, Rivas MV, Ward JM, Okanoya K, Jarvis ED. 2012. Convergent differential regulation of parvalbumin in the brains of vocal learners. PloS One 7:e29457.
Hartig W, Bruckner G, Brauer K, Schmidt C, Bigl V. 1995. Allocation of perineuronal nets and parvalbumin-, calbindin-D28k- and glutamic acid decarboxylase-immunoreactivity in the amygdala of the rhesus monkey. Brain Res 698:265–269.
Hartig W, Derouiche A, Welt K, Brauer K, Grosche J, Mader M, Reichenbach A, et al. 1999. Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res 842:15–29.
Hensch TK. 2005a. Critical period mechanisms in developing visual cortex. Curr Top Dev Biol 69:215–237.
Hensch TK. 2005b. Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6:877–888.
Hough GE, 2nd, Nelson DA, Volman SF. 2000. Re-expression of songs deleted during vocal development in white-crowned sparrows, Zonotrichia leucophrys. Anim Behav 60:279–287.
Hurley LL, Wallace AM, Sartor JJ, Ball GF. 2008. Photoperiodic induced changes in reproductive state of border canaries (Serinus canaria) are associated with marked variation in hypothalamic gonadotropin-releasing hormone immunoreactivity and the volume of song control regions. Gen Comp Endocrinol 158:10–19.
Jarvis ED. 2004. Learned birdsong and the neurobiology of human language. Ann N Y Acad Sci 1016:749–777.
Kao MH, Doupe AJ, Brainard MS. 2005. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433:638–643.
Karetko M, Skangiel-Kramska J. 2009. Diverse functions of perineuronal nets. Acta Neurobiol Exp 69:564–577.
Kirn JR, Nottebohm F. 1993. Direct evidence for loss and replacement of projection neurons in adult canary brain. J Neurosci 13:1654–1663.
Leitner S, Voigt C, Gahr M. 2001a. Seasonal changes in the song pattern of the non-domesticated canary (Serinus canaria), a field study. Behaviour 138:885–904.
Leitner S, Voigt C, Garcia-Segura LM, Van't Hof T, Gahr M. 2001b. Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas. Horm Behav 40:160–168.
Li XC, Jarvis ED, Alvarez-Borda B, Lim DA, Nottebohm F. 2000. A relationship between behavior, neurotrophin expression, and new neuron survival. Pnas 97:8584–8589.
London SE, Clayton DF. 2008. Functional identification of sensory mechanisms required for developmental song learning. Nat Neurosci 11:579–586.
Madison FN, Rouse ML, Jr, Balthazart J, Ball GF. 2015. Reversing song behavior phenotype: Testosterone driven induction of singing and measures of song quality in adult male and female canaries (Serinus canaria). Gen Comp Endocrinol 215:61–75.
Marler P. 1987. Sensitive period and the role of specific and general sensory stimulation in birdsong learning. In: Rauschecker JP, Marler P, editors. Imprinting and Cortical Plasticity. New York: John Wiley & Sons, pp 99–135.
Marler P. 1990. Song learning: The interface between behaviour and neuroethology. Philos Trans R Soc Lond Ser B, Biol Sci 329:109–114.
Meyer CA, Boroda E, Nick TA. 2014. Sexually dimorphic perineuronal net expression in the songbird. Basal Ganglia 3:229–237.
Morris NP, Henderson Z. 2000. Perineuronal nets ensheath fast spiking, parvalbumin-immunoreactive neurons in the medial septum/diagonal band complex. Eur J Neurosci 12:828–838.
Nottebohm F. 1981. A brain for all seasons: Cyclical anatomical changes in song-control nuclei of the canary brain. Science 214:1368–1370.
Nottebohm F. 2004. The road we travelled: Discovery, choreography, and significance of brain replaceable neurons. Ann N Y Acad Sci 1016:628–658.
Nottebohm F. 2005. The neural basis of birdsong. PLoS Biol 3:e164.
Nottebohm F, Stokes TM, Leonard CM. 1976. Central control of song in the canary, Serinus canarius. J Comp Neurol 165:457–486.
Nottebohm F, Nottebohm ME, Crane L. 1986. Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. Behav Neural Biol 46:445–471.
Nottebohm F, Nottebohm ME, Crane LA, Wingfield JC. 1987. Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. Behav Neural Biol 47:197–211.
Olveczky BP, Andalman AS, Fee MS. 2005. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol 3:e153.
Phillmore LS, Hoshooley JS, Sherry DF, MacDougall-Shackleton SA. 2006. Annual cycle of the black-capped chickadee: Seasonality of singing rates and vocal-control brain regions. J Neurobiol 66:1002–1010.
Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L. 2002. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248–1251.
Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L. 2006. Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci U S A 103:8517–8522.
Riters LV, Eens M, Pinxten R, Duffy DL, Balthazart J, Ball GF. 2000. Seasonal changes in courtship song and the medial preoptic area in male European starlngs (Sturnus vulgaris). Horm Behav 38:250–261.
Riters LV, Eens M, Pinxten R, Ball GF. 2002. Seasonal changes in the densities of alpha2-noradrenergic receptors are inversely related to changes in testosterone and the volumes of song control nuclei in male European starlings. J Comp Neurol 444:63–74.
Sartor JJ, Balthazart J, Ball GF. 2005. Coordinated and dissociated effects of testosterone on singing behavior and song control nuclei in canaries (Serinus canaria). Horm Behav 47:467–476.
Scharff C, Nottebohm F. 1991. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: Implications for vocal learning. J Neurosci 11:2896–2913.
Slaker M, Churchill L, Todd RP, Blacktop JM, Zuloaga DG, Raber J, Darling RA, et al. 2015. Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory. J Neurosci 35:4190–4202.
Tramontin AD, Brenowitz EA. 2000. Seasonal plasticity in the adult brain. tins 23:251–258.
Van Hout AJM, Eens M, Balthazart J, Pinxten R. 2009. Complex modulation of singing behavior by testosterone in an open-ended learner, the European Starling. Horm Behav 56:564–573.
Van Hout AJ, Pinxten R, Darras VM, Eens M. 2012. Testosterone increases repertoire size in an open-ended learner: An experimental study using adult male European starlings (Sturnus vulgaris). Horm Behav 62:563–568.
Voigt C, Leitner S. 2008. Seasonality in song behaviour revisited: Seasonal and annual variants and invariants in the song of the domesticated canary (Serinus canaria). Horm Behav 54:373–378.
Wang D, Fawcett J. 2012. The perineuronal net and the control of CNS plasticity. Cell Tissue Res 349:147–160.
Wild JM, Williams MN, Suthers RA. 2001. Parvalbumin-positive projection neurons characterise the vocal premotor pathway in male, but not female, zebra finches. Brain Res 917:235–252.
Wild JM, Williams MN, Howie GJ, Mooney R. 2005. Calcium-binding proteins define Interneurons in HVC of the zebra finch (Taeniopygia guttata). J Comp Neurol 483:76–90.
Williams H. 2004. Birdsong and singing behavior. Ann N Y Acad Sci 1016:1–30.
Xu JC, Xiao MF, Jakovcevski I, Sivukhina E, Hargus G, Cui YF, Irintchev A, et al. 2014. The extracellular matrix glycoprotein tenascin-R regulates neurogenesis during development and in the adult dentate gyrus of mice. J Cell Sci 127:641–652.
