[en] Songbirds learn their vocalizations during developmental sensitive periods of song memorization and sensorimotor learning. Some seasonal songbirds, called open-ended learners, recapitulate transitions from sensorimotor learning and song crystallization on a seasonal basis during adulthood. In adult male canaries, sensorimotor learning occurs each year in autumn and leads to modifications of the syllable repertoire during successive breeding seasons. We previously showed that perineuronal nets (PNN) expression in song control nuclei decreases during this sensorimotor learning period. Here we explored the causal link between PNN expression in adult canaries and song modification by enzymatically degrading PNN in HVC, a key song control system nucleus. Three independent experiments identified limited effects of the PNN degradation in HVC on the song structure of male canaries. They clearly establish that presence of PNN in HVC is not required to maintain general features of crystallized song. Some suggestion was collected that PNN are implicated in the stability of song repertoires but this evidence is too preliminary to draw firm conclusions and additional investigations should consider producing PNN degradations at specified time points of the seasonal cycle. It also remains possible that once song has been crystallized at the beginning of the first breeding season, PNN no longer play a key role in determining song structure; this could be tested by treatments with chondroitinase ABC at key steps in ontogeny. It would in this context be important to develop multiple stereotaxic procedures allowing the simultaneous bilateral degradation of PNN in several song control nuclei for extended periods.
Doupe AJ, Kuhl PK. Birdsong and human speech: Common themes and mechanisms. Annu Rev Neurosci. 1999; 22:567-631. https://doi.org/10.1146/annurev.neuro.22.1.567 PMID: 10202549
Williams H. Birdsong and singing behavior. Ann N Y Acad Sci. 2004; 1016:1-30. https://doi.org/10. 1196/annals.1298.029 PMID: 15313767.
Brainard MS, Doupe AJ. What songbirds teach us about learning. Nature. 2002; 417(6886):351-8. https://doi.org/10.1038/417351a PMID: 12015616.
Nottebohm F, Stokes TM, Leonard CM. Central control of song in the canary, Serinus canarius. J Comp-Neurol. 1976; 165:457-86.
Bottjer SW, Arnold AP. Developmental plasticity in neural circuits for a learned behavior. Annu Rev Neurosci. 1997; 20:459-81. https://doi.org/10.1146/annurev.neuro.20.1.459 PMID: 9056722
Nottebohm F. The neural basis of birdsong. PLoS Biol. 2005; 3(5):e164. https://doi.org/10.1371/journal. pbio.0030164 PMID: 15884976.
Brainard MS. The anterior forebrain pathway and vocal plasticity. In: Ziegler HP, Marler P, editors. Neuroscience of birdsong. Cambridge MA: Cambridge University Press; 2008. p. 240-55.
Brenowitz EA, Beecher MD. Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci. 2005; 28(3):127-32. Epub 2005/03/08. https://doi.org/10.1016/j.tins.2005.01. 004 PMID: 15749165.
Brenowitz EA. Plasticity of the song control system in adult birds. In: Zeigler HP, Marler P, editors. Neuroscience of birdsong. Cambridge: Cambridge University Press; 2008. p. 332-49.
Ball GF, Bohner J, Chaiken M, Marler P. Seasonal effects on birdsong production and acquisition I: song learning in starlings. Society for Neuroscience Meeting. 1989; 0:AB 247.10-0.
Böhner J, Chaiken M, Ball GF, Marler P. Song acquisition in photosensitive and photorefractory male European starlings. Horm Behav. 1990; 24:582-94. https://doi.org/10.1016/0018-506x(90)90043-w PMID: 2286369
Chaiken M, Bohner J, Marler P. Repertoire turnover and the timing of song acquisition in European starlings. Behaviour. 1994; 128:25-39.
Leitner S, Voigt C, Gahr M. Seasonal changes in the song pattern of the non-domesticated canary (Serinus canaria), a field study. Behaviour. 2001; 138:885-904.
Leitner S, Voigt C, Garcia-Segura LM, Van't Hof T, Gahr M. Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas. Hormones and behavior. 2001; 40(2):160-8. Epub 2001/09/06. https://doi.org/10.1006/hbeh. 2001.1700 PMID: 11534977.
Voigt C, Leitner S. Seasonality in song behaviour revisited: seasonal and annual variants and invariants in the song of the domesticated canary (Serinus canaria). Hormones and behavior. 2008; 54(3):373-8. https://doi.org/10.1016/j.yhbeh.2008.05.001 PMID: 18571653.
Nottebohm F, Nottebohm M.E., Crane L. Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. Behav Neural Biol. 1986; 46:445-71. https://doi.org/10.1016/s0163-1047(86)90485-1 PMID: 3814048
Dawson A, King VM, Bentley GE, Ball GF. Photoperiodic control of seasonality in birds. Journal of biological rhythms. 2001; 16(4):365-80. https://doi.org/10.1177/074873001129002079 PMID: 11506381.
Hurley LL, Wallace AM, Sartor JJ, Ball GF. Photoperiodic induced changes in reproductive state of border canaries (Serinus canaria) are associated with marked variation in hypothalamic gonadotropinreleasing hormone immunoreactivity and the volume of song control regions. General and comparative endocrinology. 2008; 158(1):10-9. Epub 2008/07/04. https://doi.org/10.1016/j.ygcen.2008.05.011 PMID: 18597755
Dawson A, Sharp PJ. Photorefractoriness in birds-photoperiodic and non-photoperiodic control. General and comparative endocrinology. 2007; 153(1-3):378-84. https://doi.org/10.1016/j.ygcen.2007.01. 043 PMID: 17367789.
Nicholls TJ, Storey CR. The effect of duration of the daily photoperiod on recovery of photosensitivity in photorefractory canaries (Serinus canarius). General and comparative endocrinology. 1977; 31(1):72-4. https://doi.org/10.1016/0016-6480(77)90192-7 PMID: 832820
Nottebohm F, Nottebohm ME, Crane LA, Wingfield JC. Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. Behav Neural Biol. 1987; 47:197-211.
Cornez G, Collignon C, Müller W, Ball GF, Cornil CA, Balthazart J. Seasonal changes of perineuronal nets and song learning in adult canaries (Serinus canaria). Behav Brain Res. 2020; 380:112437. https://doi.org/10.1016/j.bbr.2019.112437 PMID: 31857148
Nottebohm F. A brain for all seasons: Cyclical anatomical changes in song-control nuclei of the canary brain. Science. 1981; 214:1368-70. https://doi.org/10.1126/science.7313697 PMID: 7313697
Alvarez-Buylla A, Kirn JR, Nottebohm F. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science. 1990; 249:1444-6. https://doi.org/10.1126/science.1698312 PMID: 1698312
Alvarez-Buylla A, Kirn JR. Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. JNeurobiol. 1997; 33:585-601.
Kirn JR, Alvarez-Buylla A, Nottebohm F. Production and survival of projection neurons in a forebrain vocal center of adult male canaries. The Journal of neuroscience: the official journal of the Society for Neuroscience. 1991; 11(6):1756-62. Epub 1991/06/01. https://doi.org/10.1523/JNEUROSCI.11-06-01756.1991 PMID: 2045885.
Smith GT, Brenowitz EA, Beecher MD, Wingfield JC. Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. JNeurosci. 1997; 17:6001-10.
DeVoogd TJ, Nixdorf B, Nottebohm F. Synaptogenesis and changes in synaptic morphology related to acquisition of a new behavior. Brain Res. 1985; 329:304-8. https://doi.org/10.1016/0006-8993(85) 90539-6 PMID: 3978452
Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L. Perineuronal nets: past and present. Trends Neurosci. 1998; 21(12):510-5. Epub 1999/01/09. https://doi.org/10.1016/s0166-2236(98)01298-3 PMID: 9881847.
Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science. 2002; 298(5596):1248-51. https://doi.org/10.1126/science. 1072699 PMID: 12424383.
Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L. Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci U S A. 2006; 103(22):8517-22. Epub 2006/05/20. https://doi.org/10.1073/pnas.0602657103 PMID: 16709670
Karetko M, Skangiel-Kramska J. Diverse functions of perineuronal nets. Acta neurobiologiae experimentalis. 2009; 69(4):564-77. Epub 2010/01/06. PMID: 20048772.
Gogolla N, Caroni P, Luthi A, Herry C. Perineuronal nets protect fear memories from erasure. Science. 2009; 325(5945):1258-61. Epub 2009/09/05. https://doi.org/10.1126/science.1174146 PMID: 19729657.
Hylin MJ, Orsi SA, Moore AN, Dash PK. Disruption of the perineuronal net in the hippocampus or medial prefrontal cortex impairs fear conditioning. Learn Mem. 2013; 20(5):267-73. Epub 2013/04/18. https://doi.org/10.1101/lm.030197.112 PMID: 23592037
Thompson EH, Lensjo KK, Wigestrand MB, Malthe-Sorenssen A, Hafting T, Fyhn M. Removal of perineuronal nets disrupts recall of a remote fear memory. Proc Natl Acad Sci U S A. 2018; 115(3):607-12. Epub 2017/12/28. https://doi.org/10.1073/pnas.1713530115 PMID: 29279411
Happel MF, Niekisch H, Castiblanco Rivera LL, Ohl FW, Deliano M, Frischknecht R. Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex. Proc Natl Acad Sci U S A. 2014; 111(7):2800-5. https://doi.org/10.1073/pnas.1310272111 PMID: 24550310
Balmer TS, Carels VM, Frisch JL, Nick TA. Modulation of perineuronal nets and parvalbumin with developmental song learning. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009; 29(41):12878-85. Epub 2009/10/16. https://doi.org/10.1523/JNEUROSCI.2974-09.2009 PMID: 19828802
Cornez G, Jonckers E, Ter Haar SM, Van der Linden A, Cornil CA, Balthazart J. Timing of perineuronal net development in the zebra finch song control system correlates with developmental song learning. Proceedings Biological sciences. 2018; 285(1883): https://doi.org/10.1098/rspb.2018.0849 PMID: 30051835
Meyer CA, Boroda E, Nick TA. Sexually dimorphic perineuronal net expression in the songbird. Basal Ganglia. 2014; 3:229-37.
Cornez G, ter Haar SM, Cornil CA, Balthazart J. Anatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets. PloS one. 2015; 10(4):e0123199. https://doi.org/10. 1371/journal.pone.0123199 PMID: 25848776
Cornez G, Collignon C, Muller W, Cornil CA, Ball GF, Balthazart J. Development of Perineuronal Nets during Ontogeny Correlates with Sensorimotor Vocal Learning in Canaries. eNeuro. 2020; 7(2). Epub 2020/03/15. https://doi.org/10.1523/ENEURO.0361-19.2020 PMID: 32169884
Cornez G, Shevchouk OT, Ghorbanpoor S, Ball GF, Cornil CA, Balthazart J. Testosterone stimulates perineuronal nets development around parvalbumin cells in the adult canary brain in parallel with song crystallization. Hormones and behavior. 2020; 119:104643. https://doi.org/10.1016/j.yhbeh.2019. 104643 PMID: 31785283
Best BJ, Day NF, Larson GT, Carels VM, Nick TA. Vocal effects of perineuronal net destruction in adult zebra finches. Abst Soc Neurosc Meeting Washington DC. 2011:Abst.303.18.
Darkwa LO, Nerurka V, Semu D, Gardner TJ, Otchy TM. Dissociation in behavioral effects of perineuronal net degradation in premotor nuclei of adult songbirds. Abst Soc Neurosc Meeting San Diego CA Abst 57420. 2018.
Griffiths R, Double MC, Orr K, Dawson RJ. A DNA test to sex most birds. Mol Ecol. 1998; 7(8):1071-5. Epub 1998/08/26. https://doi.org/10.1046/j.1365-294x.1998.00389.x PMID: 9711866.
Shevchouk OT, Ghorbanpoor S, Smith E, Liere P, Schumacher M, Ball GF, et al. Behavioral evidence for sex steroids hypersensitivity in castrated male canaries. Hormones and behavior. 2018; 103:80-96. https://doi.org/10.1016/j.yhbeh.2018.06.004 PMID: 29909262.
Halle F, Gahr M, Kreutzer M. Impaired recovery of syllable repertoires after unilateral lesions of the HVC of male domesticated canaries. Anim Biol 2003; 53:113-28.
Deregnaucourt S, Poirier C, Kant AV, Linden AV, Gahr M. Comparisons of different methods to train a young zebra finch (Taeniopygia guttata) to learn a song. J Physiol Paris. 2013; 107(3):210-8. Epub 2012/09/18. https://doi.org/10.1016/j.jphysparis.2012.08.003 PMID: 22982543.
Chen Y, Matheson LE, Sakata JT. Mechanisms underlying the social enhancement of vocal learning in songbirds. Proc Natl Acad Sci U S A. 2016; 113(24):6641-6. Epub 2016/06/02. https://doi.org/10.1073/pnas.1522306113 PMID: 27247385
Marler P, Waser MS. Role of auditory feedback in canary song development. J Comp Physiol Psychol. 1977; 91(1):8-16. Epub 1977/02/01. https://doi.org/10.1037/h0077303 PMID: 838918.
Romberg C, Yang S, Melani R, Andrews MR, Horner AE, Spillantini MG, et al. Depletion of perineuronal nets enhances recognition memory and long-term depression in the perirhinal cortex. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2013; 33(16):7057-65. Epub 2013/04/19. https://doi.org/10.1523/JNEUROSCI.6267-11.2013 PMID: 23595763
Brenowitz EA, Lent K. Afferent input is necessary for seasonal growth and maintenance of adult avian song control circuits. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2001; 21(7):2320-9.
Wissman AM, Brenowitz EA. The role of neurotrophins in the seasonal-like growth of the avian song control system. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009; 29(20):6461-71. Epub 2009/05/22. https://doi.org/10.1523/JNEUROSCI.0638-09.2009 PMID: 19458217.
Miller KE, Wood WE, Brenowitz EA, Perkel DJ. Brain-Derived Neurotrophic Factor Has a Transsynaptic Trophic Effect on Neural Activity in an Adult Forebrain Circuit. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2020; 40(6):1226-31. Epub 2019/12/21. https://doi.org/10. 1523/JNEUROSCI.2375-19.2019 PMID: 31857358
Alvarez-Borda B, Nottebohm F. Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2002; 22(19):8684-90. https://doi.org/10.1523/JNEUROSCI.22-19-08684.2002 PMID: 12351743
Li XC, Jarvis ED, Alvarez-Borda B, Lim DA, Nottebohm F. A relationship between behavior, neurotrophin expression, and new neuron survival. PNAS. 2000; 97:8584-9. https://doi.org/10.1073/pnas. 140222497 PMID: 10890902
Sartor JJ, Ball GF. Social suppression of song is associated with a reduction in volume of a song-control nucleus in European starlings (Sturnus vulgaris). Behav Neurosci. 2005; 119(1):233-44. https://doi.org/10.1037/0735-7044.119.1.233 PMID: 15727528.
Wild JM. Descending projections of the songbird nucleus robustus archistriatalis. J Comp Neurol. 1993; 338:225-41. https://doi.org/10.1002/cne.903380207 PMID: 8308169
Alward BA, Balthazart J, Ball GF. Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate. Proc Natl Acad Sci U S A. 2013; 110(48):19573-8. Epub 2013/11/13. https://doi.org/10.1073/pnas.1311371110 PMID: 24218603
Alward BA, Madison FN, Parker SE, Balthazart J. Pleiotropic Control by Testosterone of a Learned Vocal Behavior and Its Underlying Neuroplasticity(1,2,3). 2016; 3(1). https://doi.org/10.1523/eneuro. 0145-15.2016 PMID: 26835510.
Alward BA, Balthazart J, Ball GF. Dissociable Effects on Birdsong of Androgen Signaling in Cortex-Like Brain Regions of Canaries. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2017; 37(36):8612-24. https://doi.org/10.1523/JNEUROSCI.3371-16.2017 PMID: 28821656
Mundinger PC. Behaviour-genetic analysis of canary song: inter-strain differences in sensory learning, and epigenetic rules. Anim Behav. 1995; 49:357-66.
Hough GE, 2nd, Nelson DA, Volman SF. Re-expression of songs deleted during vocal development in white-crowned sparrows, Zonotrichia leucophrys. Animal behaviour. 2000; 60(3):279-87. Epub 2000/09/29. https://doi.org/10.1006/anbe.2000.1498 PMID: 11007636.
Beurdeley M, Spatazza J, Lee HH, Sugiyama S, Bernard C, Di Nardo AA, et al. Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2012; 32(27):9429-37. Epub 2012/07/06. https://doi. org/10.1523/JNEUROSCI.0394-12.2012 PMID: 22764251
Vo T, Carulli D, Ehlert EM, Kwok JC, Dick G, Mecollari V, et al. The chemorepulsive axon guidance protein semaphorin3A is a constituent of perineuronal nets in the adult rodent brain. Mol Cell Neurosci. 2013; 56:186-200. Epub 2013/05/15. https://doi.org/10.1016/j.mcn.2013.04.009 PMID: 23665579.
Wild JM, Williams MN, Howie GJ, Mooney R. Calcium-binding proteins define Interneurons in HVC of the zebra finch (Taeniopygia guttata). J Comp Neurol. 2005; 483(1):76-90. https://doi.org/10.1002/cne. 20403 PMID: 15672397
Kosche G, Vallentin D, Long MA. Interplay of inhibition and excitation shapes a premotor neural sequence. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2015; 35 (3):1217-27. Epub 2015/01/23. https://doi.org/10.1523/JNEUROSCI.4346-14.2015 PMID: 25609636
Fee MS, Kozhevnikov AA, Hahnloser RH. Neural mechanisms of vocal sequence generation in the songbird. Ann N Y Acad Sci. 2004; 1016:153-70. Epub 2004/08/18. https://doi.org/10.1196/annals. 1298.022 PMID: 15313774.
Brainard MS. Contributions of the anterior forebrain pathway to vocal plasticity. Ann N Y Acad Sci. 2004; 1016:377-94. https://doi.org/10.1196/annals.1298.042 PMID: 15313786.
Zhao RR, Muir EM, Alves JN, Rickman H, Allan AY, Kwok JC, et al. Lentiviral vectors express chondroitinase ABC in cortical projections and promote sprouting of injured corticospinal axons. J Neurosci Methods. 2011; 201(1):228-38. Epub 2011/08/23. https://doi.org/10.1016/j.jneumeth.2011.08.003 PMID: 21855577
Alves JN, Muir EM, Andrews MR, Ward A, Michelmore N, Dasgupta D, et al. AAV vector-mediated secretion of chondroitinase provides a sensitive tracer for axonal arborisations. J Neurosci Methods. 2014; 227:107-20. https://doi.org/10.1016/j.jneumeth.2014.02.010 PMID: 24583077.