Comparing perineuronal nets and parvalbumin development between black bird species with differences in early developmental song exposure

Cornez, Gilles; Langro, Justin; Cornil, Charlotte; Balthazart, Jacques; Lynch, Kathleen

doi:10.1242/jeb.212910

Article (Scientific journals)

Comparing perineuronal nets and parvalbumin development between black bird species with differences in early developmental song exposure

Cornez, Gilles; Langro, Justin; Cornil, Charlotte et al.

2020 • In Journal of Experimental Biology, 223 (Pt1), p. 212910

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/244226

DOI
10.1242/jeb.212910

PubMed
31767738

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Keywords :

Brain plasticity; Song learning; Red-winged blackbirds; PNN; Icteridae; Brown-headed cowbirds; Brood parasitism

Abstract :

[en] Brood parasitic songbirds are a natural system in which developing birds are isolated from species-typical song and therefore present a unique opportunity to compare neural plasticity in song learners raised with and without conspecific tutors. We compared perineuronal nets (PNN) and parvalbumin (PV) in song control nuclei in juveniles and adults of two closely related icterid species (i.e. blackbirds): brown-headed cowbirds (Molothrus ater; brood parasite) and red-winged blackbirds (Agelaius phoeniceus; non-parasite). The number of PV cells per nucleus was significantly higher in adults compared with juveniles in the nucleus HVC and the robust nucleus of the arcopallium (RA), whereas no significant species difference appeared in any region of interest. The number of PNN per nuclei was significantly higher in adults compared with juveniles in HVC, RA and Area X, but only RA exhibited a significant difference between species. PV cells surrounded by PNN (PV+PNN) also exhibited age-related differences in HVC, RA and Area X, but RA was the only region in which PV+PNN exhibited significant species differences. Furthermore, a significant interaction existed in RA between age and species with respect to PNN and PV+PNN, revealing RA as a region displaying differing plasticity patterns across age and species. Additional comparisons of PNN and PV between adult male and female cowbirds revealed that males have greater numbers of all three measures in RA compared with females. Species-, sex- and age-related differences in RA suggest that species differences in neural plasticity are related to differences in song production rather than sensitivity to song learning, despite a stark contrast in early exposure to conspecific male tutors.

Disciplines :

Neurosciences & behavior

Author, co-author :

Cornez, Gilles ; Université de Liège - ULiège > GIGA

Langro, Justin

Cornil, Charlotte ; Université de Liège - ULiège > Neurosciences-Neuroendocrinology

Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques

Lynch, Kathleen

Language :

English

Title :

Comparing perineuronal nets and parvalbumin development between black bird species with differences in early developmental song exposure

Publication date :

2020

Journal title :

Journal of Experimental Biology

ISSN :

0022-0949

eISSN :

1477-9145

Publisher :

The Company of Biologists, United Kingdom

Volume :

223

Issue :

Pt1

Pages :

jeb.212910

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

NIH - National Institutes of Health
F.R.S.-FNRS - Fonds de la Recherche Scientifique

Available on ORBi :

since 29 January 2020

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Bibliography

Alward, B. A., Rouse, M. L., Balthazart, J. and Ball, G. F. (2017). Testosterone regulates birdsong in an anatomically specific manner. Anim. Behav. 124, 291-298. doi:10.1016/j.anbehav.2016.09.013
Balmer, T. S. (2016). Perineuronal nets enhance the excitability of fast-spiking neurons. eNeuro 3, 1-13. doi:10.1523/ENEURO.0112-16.2016
Balmer, T. S., Carels, V. M., Frisch, J. L. and Nick, T. A. (2009). Modulation of perineuronal nets and parvalbumin with developmental song learning. J. Neurosci. 29, 12878-12885. doi:10.1523/JNEUROSCI.2974-09.2009
Beurdeley, M., Spatazza, J., Lee, H. H. C., Sugiyama, S., Bernard, C., Di Nardo, A. A., Hensch, T. K. and Prochiantz, A. (2012). Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J. Neurosci. 32, 9429-9437. doi:10.1523/JNEUROSCI.0394-12.2012
Böhner, J. (1990). Early acquisition in the zebra finch, Taeniopygia guttata. Anim. Behav. 39, 369-374. doi:10.1016/S0003-3472(05)80883-8
Boseret, G., Carere, C., Ball, G. F. and Balthazart, J. (2006). Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria). J. Neurobio 66, 1044-1060. doi:10.1002/neu.20268
Brainard, M. S. and Doupe, A. J. (2002). What songbirds teach us about learning. Nature 417, 351-358. doi:10.1038/417351a
Brenowitz, E. A. and Beecher, M. D. (2005). Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci. 28, 127-132. doi:10. 1016/j.tins.2005.01.004
Cornez, G., ter Haar, S. M., Cornil, C. A. and Balthazart, J. (2015). Anatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets. PLoS ONE 10, e0123199. doi:10.1371/journal.pone.0123199
Cornez, G., Jonckers, E., Ter Haar, S., Shevchouk, O. Ghorbanpoor, S., Ball, G., Van der Linden, A., Cornil, C. and Balthazart, J. (2017a). Perineuronal nets development correlates with developmental and adult neuroplasticity related to song learning in the songbird brain. Conference Abstract: 12th National Congress of the Belgian Society for Neuroscience. Front. Neurosci. doi:10.3389/conf.fnins. 2017.94.00099
Cornez, G., Madison, F. N., Van der Linden, A., Cornil, C., Yoder, K. M., Ball, G. F. and Balthazart, J. (2017b). Perineuronal nets and vocal plasticity in songbirds: a proposed mechanism to explain the difference between closed-ended and open-ended learning. Dev. Neurobiol. 77, 975-994. doi:10.1002/dneu. 22485
Cornez, G., Collignon, C., Müller, W., Ball, G. F., Cornil, C. A. and Balthazart, J. (2018a). Correlation between song learning and perineuronal nets development in song control system nuclei of juvenile canaries. Program no. 406.03. 2018 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience.
Cornez, G., Jonckers, E., ter Haar, S. M., Van der Linden, A., Cornil, C. A. and Balthazart, J. (2018b). Timing of perineuronal net development in the zebra finch song control system correlates with developmental song learning. Proc. R. Soc. B Biol. Sci. 285, 20180849. doi:10.1098/rspb.2018.0849
Dityatev, A., Brückner, G., Dityateva, G., Grosche, J., Kleene, R. and Schachner, M. (2007). Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev. Neurobiol. 67, 570-588. doi:10.1002/ dneu.20361
Doupe, A. J. and Kuhl, P. K. (1999). Birdsong and human speech: common themes and mechanisms. Annu.Rev.Neurosci. 22, 567-631. doi:10.1146/annurev.neuro. 22.1.567
Eales, L. A. (1985). Song learning in zebra finches: some effects of song model availability on what is learnt and when. Anim. Behav. 33, 1293-1300. doi:10.1016/ S0003-3472(85)80189-5
Eales, L. A. (1987). Song Learning in female-raised zebra finches: another look at the sensitive phase. Anim. Behav. 35, 1356-1365. doi:10.1016/S0003-3472(87)80008-8
Friedmann, H. (1929). The Cowbirds, a Study in the Biology of Social Parasitism. Springfield, IL: C. C. Thomas.
Friedmann, H. and Kiff, L. F. (1985). The parasitic cowbirds and their hosts. Proc. West. Fund. Vertebr. Zool. 2, 225-304.
Gogolla, N., Caroni, P., Luthi, A. and Herry, C. (2009). Perineuronal nets protect fear memories from erasure. Science 325, 1258-1261. doi:10.1126/science. 1174146
Guigueno, M. F., Sherry, D. F. and MacDougall-Shackleton, S. A. (2016). Sex and seasonal differences in neurogenesis and volume of the song-control system are associated with song in brood-parasitic and non-brood-parasitic icterid songbirds. Dev. Neurobiol. 76, 1226-1240. doi:10.1002/dneu.22385
Happel, M. F. K., Niekisch, H., Castiblanco Rivera, L. L., Ohl, F. W., Deliano, M. and Frischknecht, R. (2014). Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex. Proc. Natl. Acad. Sci. USA 111, 2800-2805. doi:10.1073/pnas.1310272111
Hara, E., Rivas, M. V., Ward, J. M., Okanoya, K. and Jarvis, E. D. (2012). Convergent differential regulation of parvalbumin in the brains of vocal learners. PLoS ONE 7, e29457. doi:10.1371/journal.pone.0029457
Hauber, M. E., Sherman, P. W. and Paprika, D. (2000). Self-referent phenotype matching in a brood parasite: the armpit effect in brown-headed cowbirds (Molothrus ater). Anim. Cogn. 3, 113-117. doi:10.1007/s100710000071
Hauber, M. E., Russo, S. A. and Sherman, P. W. (2001). A password for species recognition in a brood-parasitic bird. Proc. R. Soc. B Biol. Sci. 268, 1041-1048. doi:10.1098/rspb.2001.1617
Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888. doi:10.1038/nrn1787
Karetko, M. and Skangiel-Kramska, J. (2009). Diverse functions of perineuronal nets. Acta Neurobiol. Exp. 69, 564-577.
King, A. P. and West, M. J. (1977). Species identification in the North American cowbird: appropriate responses to abnormal song. Science 195, 1002-1004. doi:10.1126/science.841321
King, A. P. and West, M. J. (1988). Searching for the functional origins of song in eastern brown-headed cowbirds, Molothrus ater ater. Anim. Behav. 36, 1575-1588. doi:10.1016/S0003-3472(88)80100-3
Konishi, M. (1965). The role of auditory feedback in the control of vocalization in the white crowned sparrow. Zeitschrift Tierpsychologie 22, 770-783.
Lynch, K. S., Gaglio, A., Tyler, E., Coculo, J., Louder, M. I. and Hauber, M. E. (2017). A neural basis for password-based species recognition in an avian brood parasite. J. Exp. Biol. 220, 2345-2353. doi:10.1242/jeb.158600
Marler, P. and Peters, S. (1982). Subsong and plastic song: their role in the vocal learning process. In Acoustic Communication in Birds, Vol. 2 (ed. D. E. Kroodsma, E. H. Miller and H. Ouellet), pp. 1-19. New York: Academic Press.
Marler, P. and Peters, S. (1987). A sensitive period for song acquisition in the song sparrow, Melospiza melodia: a case of age-limited learning. Ethology 76, 89-100. doi:10.1111/j.1439-0310.1987.tb00675.x
Marler, B. Y. P., Mundinger, P., Waser, M. S. U. E. and Lutjen, A. N. N. (1972). Song development in red-winged blackbirds (Agelaius phoeniceus). Anim. Behav. 20, 586-606. doi:10.1016/S0003-3472(72)80024-1
Miller-Sims, V. C. and Bottjer, S. W. (2012). Auditory experience refines corticobasal ganglia inputs to motor cortex via remapping of single axons during vocal learning in zebra finches. J. Neurophysiol. 107, 1142-1156. doi:10.1152/jn.00614. 2011
Morikawa, S., Ikegaya, Y., Narita, M. and Tamura, H. (2017). Activation of perineuronal net-expressing excitatory neurons during associative memory encoding and retrieval. Sci. Rep. 7, 46024. doi:10.1038/srep46024
Nixdorf-Bergweiler, B. E. (1996). Divergent and parallel development in volume sizes of telencephalic song nuclei in male and female zebra finches. J. Comp. Neurol. 375, 445-456. doi:10.1002/(SICI)1096-9861(19961118)375:3<445::AIDCNE7>3.0.CO;2-2
Nordeen, K. W., Marler, P. and Nordeen, E. J. (1989). Addition of song-related neurons in swamp sparrows coincides with memorization, not production, of learned songs. J. Neurobiol. 20, 651-661. doi:10.1002/neu.480200705
Nottebohm, F. (1999). The anatomy and timing of vocal learning in birds. In The Design of Animal Communication (ed. M. D. Hauser and M. Konishi), pp. 63-110. MIT Press.
Nottebohm, F. (2005). The neural basis of birdsong. PLoS Biol. 3, e164. doi:10. 1371/journal.pbio.0030164
O’Loghlen, A. L. and Rothstein, S. I. (1993). An extreme example of delayed vocal development: song learning in a population of wild brown-headed cowbirds. Anim. Behav. 46, 293-304. doi:10.1006/anbe.1993.1190
O’Loghlen, A. L. and Rothstein, S. I. (2002). Ecological effects on song learning: delayed development is widespread in wild populations of brown-headed cowbirds. Anim. Behav. 63, 475-486. doi:10.1006/anbe.2001.1951
O’Loghlen, A. L. and Rothstein, S. I. (2010). Delayed sensory learning and development of dialect songs in brown-headed cowbirds, Molothrus ater. Anim. Behav. 79, 299-311. doi:10.1016/j.anbehav.2009.10.029
Ortega, C. P., Ortega, J. C., Backensto, S. A. and Rapp, C. A. (1996). Improved methods for aging second-year and after-second-year male brown-headed cowbirds. J. Field Ornithol. 67, 542-548.
Payne, R. B. (1977). The ecology of brood parasitism in birds. Annu. Rev. Ecol. Evol. Syst. 8, 1-28. doi:10.1146/annurev.es.08.110177.000245
Pfenning, A. R., Hara, E., Whitney, O., Rivas, M. V., Wang, R., Roulhac, P. L., Howard, J. T., Wirthlin, M., Lovell, P. V., Ganapathy, G. et al. (2014). Convergent transcriptional specializations in the brains of humans and song-learning birds. Science 346, 1256846-1256846. doi:10.1126/science. 1256846
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W. and Maffei, L. (2002). Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251. doi:10.1126/science.1072699
Pizzorusso, T., Medini, P., Landi, S., Baldini, S., Berardi, N. and Maffei, L. (2006). Structural and functional recovery from early monocular deprivation in adult rats. Proc. Natl. Acad. Sci. USA 103, 8517-8522. doi:10.1073/pnas. 0602657103
Rothstein, S. I., Verner, J. and Stevens, E. (1980). Range expansion and diurnal changes in dispersion of the brown-headed cowbird in the sierra nevada. The Auk 97, 253-267.
Scharff, C. and 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. doi:10.1523/ JNEUROSCI.11-09-02896.1991
Sherman, P. W. (1999). Birds of a feather lek together. Nature 401, 119-120. doi:10. 1038/43574
Slagsvold, T. and Hansen, B. T. (2001). Sexual imprinting and the origin of obligate brood parasitism in birds. Am. Nat. 158, 354-367. doi:10.1086/321994
van ‘t Spijker, H. M. and Kwok, J. C. F. (2017). A sweet talk: the molecular systems of perineuronal nets in controlling neuronal communication. Front. Integr. Neurosci. 11, 1-10. doi:10.3389/fnint.2017.00033
White, D. J., King, A. P. and West, M. J. (2002a). Facultative development of courtship and communication in juvenile male cowbirds (Molothrus ater). Behav. Ecol. 13, 487-496. doi:10.1093/beheco/13.4.487
White, D. J., King, A. P., Cole, A. and West, M. J. (2002b). Opening the social gateway: early vocal and social sensitivities in brown-headed cowbirds (Molothrus ater). Ethology 108, 23-37. doi:10.1046/j.1439-0310.2002.00755.x
Wild, J. M. (2004). Functional neuroanatomy of the sensorimotor control of singing. Ann. N.Y. Acad. Sci. 1016, 438-462. doi:10.1196/annals.1298.016
Williams, H. (2004). Birdsong and singing behavior. Ann. N.Y. Acad. Sci. 1016, 1-30. doi:10.1196/annals.1298.029
Winfree, R. (1999). Cuckoos, cowbirds and the persistence of brood parasitism. Trends Ecol. Evol. 14, 338-343. doi:10.1016/S0169-5347(99)01643-2
Yasukawa, K., Blank, J. L. and Patterson, C. B. (1980). Song repertoires and sexual selection in the Red-winged Blackbird. Behav. Ecol. Sociobiol. 7, 233-238. doi:10.1007/BF00299369