Anatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Cornez, Gilles ^a   Ter Haar, Sita M ^a   Cornil, Charlotte A ^a   Balthazart, Jacques ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN; PERINEURONAL NET; PROTEOCHONDROITIN SULFATE; UNCLASSIFIED DRUG; AVIAN PROTEIN;

ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; CELL POPULATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; IMMUNOFLUORESCENCE TEST; MAGNOCELLULAR NUCLEUS; MALE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEX DIFFERENCE; TAENIOPYGIA GUTTATA; VISUAL SYSTEM; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN; CYTOLOGY; FINCH; METABOLISM; NERVE CELL NETWORK; SEXUAL DEVELOPMENT; VOCALIZATION;

PASSERI; TAENIOPYGIA GUTTATA; VERTEBRATA;

ANIMALS; AVIAN PROTEINS; BRAIN; FEMALE; FINCHES; MALE; NERVE NET; NEURONAL PLASTICITY; PARVALBUMINS; SEX CHARACTERISTICS; VOCALIZATION, ANIMAL;

EID: 84927658658     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123199     Document Type: Article

References (68)

1. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 2004; 44: 5-21. PMID: 15450156
2. Nottebohm F. A brain for all seasons: Cyclical anatomical changes in song-control nuclei of the canary brain. Science 1981; 214: 1368-1370. PMID: 7313697
3. Brainard MS, Doupe AJ. What songbirds teach us about learning. Nature: Insight reviews 2002; 417: 351-358. PMID: 12015616
4. Wilbrecht L, Nottebohm F. Vocal learning in birds and humans. Ment Retard Dev Disabil Res Rev 2003; 9: 135-148. PMID: 12953292
5. Mooney R. Neural mechanisms for learned birdsong. Learn Mem 2009; 16: 655-669. doi: 10.1101/lm.1065209 PMID: 19850665
6. Mooney R. Neurobiology of song learning. Curr Opin Neurobiol 2009; 19: 654-660. doi: 10.1016/j.conb.2009.10.004 PMID: 19892546
7. Phan ML, Pytte CL, Vicario DS. Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. Proc Natl Acad Sci U S A 2006; 103: 1088-1093. PMID: 16418265
8. Balmer TS, Carels VM, Frisch JL, Nick TA. Modulation of perineuronal nets and parvalbumin with developmental song learning. J Neurosci 2009; 29: 12878-12885. doi: 10.1523/JNEUROSCI.2974-09.2009 PMID: 19828802
9. Arnold AP. The effects of castration and androgen replacement on song courtship, and aggression in zebra finches (Poephila guttata). J Exp Zool 1975; 191: 309-326. PMID: 1092802
10. Pröve E. Der Einfluss von Kastration und Testosteronsubstitution auf das Verhalten manlicher Zebrafinken. J Ornithol 1974; 115: 338-347.
11. Nottebohm F, Arnold AP. Sexual dimorphism in the vocal control areas in the song bird brain. Science 1976; 194: 211-213. PMID: 959852
12. Reiner AD, Perkel J, Bruce L, Butler A, Csillag A, Kuenzel W, et al. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 2004; 473: 377-414. PMID: 15116397
13. Nottebohm F, Stokes TM, Leonard CM. Central control of song in the canary, Serinus canarius. J Comp Neurol 1976; 165: 457-486. PMID: 1262540
14. Nottebohm F, Kelley DB, Paton JA. Connections of vocal control nuclei in the canary telencephalon. J Comp Neurol 1982; 207: 344-357. PMID: 7119147
15. Bottjer SW, Johnson F. Circuits, hormones, and learning: Vocal behavior in songbirds. J Neurobiol 1997; 33: 602-618. PMID: 9369462
16. Doupe AJ, Perkel DJ, Reiner A, Stern EA. Birdbrains could teach basal ganglia research a new song. Trends Neurosci 2005; 28: 353-363. PMID: 15935486
17. Benton S, Nelson DA, Marler P, DeVoogd TJ. Anterior forebrain pathway is needed for stable song expression in adult male white-crowned sparrows (Zonotrichia leucophrys). Behav Brain Res 1998; 96: 135-150. PMID: 9821550
18. Miller-Sims VC, Bottjer SW. Auditory experience refines cortico-basal ganglia inputs to motor cortex via remapping of single axons during vocal learning in zebra finches. J Neurophysiol 2012; 107: 1142-1156. doi: 10.1152/jn.00614.2011 PMID: 22157116
19. Kao MH, Doupe AJ, Brainard MS. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 2005; 433: 638-643. PMID: 15703748
20. Nixdorf BE, Davis SS, DeVoogd TJ. Morphology of Golgi-impregnated neurons in hyperstriatum ventralis, pars caudalis in adult male and female canaries. J Comp Neurol 1989; 284: 337-349. PMID: 2474004
21. Ball GF, MacDougall-Shackleton SA. Sex differences in songbirds 25 years later: What have we learned and where do we go? Microsc Res Tech 2001; 54: 327-334. PMID: 11668646
22. Holloway CC, Clayton DE. Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat Neurosci 2001; 4: 170-175. PMID: 11175878
23. Kirn JR, Nottebohm F. Direct evidence for loss and replacement of projection neurons in adult canary brain. J Neurosci 1993; 13: 1654-1663. PMID: 8385206
24. De Groof G, Verhoye M, Van Meir V, Balthazart J, Van der Linden A. Seasonal rewiring of the songbird brain: an in vivo MRI study. Eur J Neurosci 2008; 28: 2475-2485. doi: 10.1111/j.1460-9568.2008.06545.x PMID: 19032586
25. De Groof G, Verhoye M, Poirier C, Leemans A, Eens M, Darras VM, et al. Structural changes between seasons in the songbird auditory forebrain. J Neurosci 2009; 29: 13557-13565. doi: 10.1523/JNEUROSCI.1788-09.2009 PMID: 19864568
26. Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L. Perineuronal nets: past and present. Trends Neurosci 1998; 21: 510-515. PMID: 9881847
27. Karetko M, Skangiel-Kramska J. Diverse functions of perineuronal nets. Acta Neurobiol Exp (Wars) 2009; 69: 564-577. PMID: 20048772
28. Wang D, Fawcett J. The perineuronal net and the control of CNS plasticity. Cell Tissue Res 2012; 349: 147-160. doi: 10.1007/s00441-012-1375-y PMID: 22437874
29. Galtrey CM, Fawcett JW. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 2007; 54: 1-18. PMID: 17222456
30. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002; 416: 636-640. PMID: 11948352
31. Dityatev A, Bruckner G, Dityateva G, Grosche J, Kleene R, Schachner M. Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev Neurobiol 2007; 67: 570-588. PMID: 17443809
32. Braun K, Scheich H, Heizmann CW, Hunziker W. Parvalbumin and calbindin-D28K immunoreactivity as developmental markers of auditory and vocal motor nuclei of the zebra finch. Neuroscience 1991; 40: 853-869. PMID: 2062443
33. Hara E, Rivas MV, Ward JM, Okanoya K, Jarvis ED. Convergent differential regulation of parvalbumin in the brains of vocal learners. PLoS One 2012; 7: e29457. doi: 10.1371/journal.pone.0029457 PMID: 22238614
34. Nowicka D, Soulsby S, Skangiel-Kramska J, Glazewski S. Parvalbumin-containing neurons, perineuronal nets and experience-dependent plasticity in murine barrel cortex. Eur J Neurosci 2009; 30: 2053-2063. doi: 10.1111/j.1460-9568.2009.06996.x PMID: 20128844
35. Best BJ, Day NF, Larson GT, Carels VM, Nick TA. Vocal effects of perineuronal net destruction in adult zebra finc. Abst Soc for Neurosc nbr 30318 2012.
36. Del Negro C, Gahr M, Leboucher G, Kreutzer M. The selectivity of sexual responses to song displays: effects of partial chemical lesion of the HVC in female canaries. Behav Brain Res 1998; 96: 151-159. PMID: 9821551
37. Burt JM, Lent KL, Beecher MD, Brenowitz EA. Lesions of the anterior forebrain song control pathway in female canaries affect song perception in an operant task. J Neurobiol 2000; 42: 1-13. PMID: 10623896
38. Maguire SE, Schmidt MF, White DJ. Social brains in context: lesions targeted to the song control system in female cowbirds affect their social network. PLoS One 2013; 8: e63239. doi: 10.1371/journal.pone.0063239 PMID: 23650558
39. MacDougall-Schackleton SA, Hulse SH, Ball GF. Neural bases of song preferences in female zebra finches (Taeniopygia guttata). Neuroreport 1998; 9: 3047-3052. PMID: 9804314
40. Hernandez AM, MacDougall-Shackleton SA. Effects of early song experience on song preferences and song control and auditory brain regions in female house finches (Carpodacus mexicanus). J Neurobiol 2004; 59: 247-258. PMID: 15085541
41. Terpstra NJ, Bolhuis JJ, Riebel K, van der Burg JM, den Boer-Visser AM. Localized brain activation specific to auditory memory in a female songbird. J Comp Neurol 2006; 494: 784-791. PMID: 16374807
42. Bolhuis JJ, Gahr M. Neural mechanisms of birdsong memory. Nat Rev Neurosci 2006; 7: 347-357. PMID: 16760915
43. Wild JM, Williams MN, Suthers RA. Parvalbumin-positive projection neurons characterise the vocal premotor pathway in male, but not female, zebra finches. Brain Res 2001; 917: 235-252. PMID: 11640910
44. Sun L, Wang R, Zeng S, Geng Z, Zhang X, Zuo M. Identification of male-biased gene: parvalbumin in song control nuclei of the Bengalese finch. Neurosci Res 2010; 68: 22-34. doi: 10.1016/j.neures.2010.05.003 PMID: 20566402
45. Meyer CA, Boroda E, Nick TA. Sexually dimorphic perineuronal net expression in the songbird. Basal Ganglia 2014; 3: 229-237.
46. 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: 1248-1251. PMID: 12424383
47. 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: 8517-8522. PMID: 16709670
48. Fortune ES, Rodriguez C, Li D, Ball GF, Coleman MJ. Neural mechanisms for the coordination of duet singing in wrens. Science 2011; 334: 666-670. doi: 10.1126/science.1209867 PMID: 22053048
49. Nottebohm F. Testosterone triggers growth of brain vocal control nuclei in adult female canaries. Brain Res 1980; 189: 429-436. PMID: 7370785
50. Madison FN, Rouse ML Jr., Balthazart J, Ball GF. 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 2014.
51. Eens M. Understanding the complex song of the European starling: an integrated ethological approach. Adv Study Anim Behav 1997; 26: 355-434.
52. Noirot IC, Adler HJ, Cornil CA, Harada N, Dooling RJ, Balthazart J, et al. Presence of aromatase and estrogen receptor alpha in the inner ear of zebra finches. Hear Res 2009; 252: 49-55. doi: 10.1016/j.heares.2009.04.012 PMID: 19397967
53. Peterson RS, Yarram L, Schlinger BA, Saldanha CJ. Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proc Biol Sci 2005; 272: 2089-2096. PMID: 16191621
54. Rohman KN, Saldanha CJ. Sex and brain area differences in the microsomal compartmentalization of telencephalic aromatase in the adult zebra finch. Horm Behav 2005; 48: 125.
55. Lucas JR, Freeberg TM, Long GR, Krishnan A. Seasonal variation in avian auditory evoked responses to tones: a comparative analysis of Carolina chickadees, tufted titmice, and white-breasted nuthatches. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2007; 193: 201-215. PMID: 17066303
56. Noirot IC, Adler HJ, Cornil CA, Balthazart J, Ball GF, Dooling RJ. Sex differences in the auditory system of zebra finches (Taeniopygia guttata): a role for sex steroids in the avian inner ear? Abst Soc for Neurosc Nbr 672 2007.
57. Gall MD, Henry KS, Lucas JR. Two measures of temporal resolution in brown-headed cowbirds (Molothrus ater). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2012; 198: 61-68. doi: 10.1007/s00359-011-0687-9 PMID: 21987264
58. Handa RJ, McGivern RF. Steroid Hormones, Receptors, and Perceptual and Cognitive Sex Differences in the Visual System. Curr Eye Res 2014: 1-18.
59. Evrard HC, Harada N, Balthazart J. Immunocytochemical localization of aromatase in sensory and integrating nuclei of the hindbrain in Japanese quail (Coturnix japonica). J Comp Neurol 2004; 473: 194-212. PMID: 15101089
60. MacLusky NJ, Toran-Alllerand CD. Estrogen biosynthesis in the developing rat brain: regional and temporal aspects. Abst Soc for Neurosc Nbr 3911 1989.
61. Horvath TL, Wikler KC. Aromatase in developing sensory systems of the rat brain. J Neuroendocrinol 1999; 11: 77-84. PMID: 10048462
62. Sheridan PJ. Estrogen binding in the neonatal neocortex. Brain Res 1979; 178: 201-206. PMID: 91415
63. MacLusky NJ, Chaptal C, McEwen BS. The development of estrogen receptor systems in the rat brain and pituitary: postnatal development. Brain Res 1979; 178: 143-160. PMID: 497857
64. Gerlach JL, McEwen BS, Toran-Allerand CD, Friedman WJ. Perinatal development of estrogen receptors in mouse brain assessed by radioautography, nuclear isolation and receptor assay. Brain Res 1983; 313: 7-18. PMID: 6661666
65. Juraska JM. Sex differences in "cognitive" regions of the rat brain. Psychoneuroendocrinology 1991; 16: 105-109. PMID: 1961834
66. Van Meir V, Boumans T, De Groof G, Van Audekerke J, Smolders A, Scheunders P, et al. Spatiotemporal properties of the BOLD response in the songbirds' auditory circuit during a variety of listening tasks. Neuroimage 2005; 25: 1242-1255. PMID: 15850742
67. McRae PA, Rocco MM, Kelly G, Brumberg JC, Matthews RT. Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci 2007; 27: 5405-5413. PMID: 17507562
68. Gati G, Morawski M, Lendvai D, Matthews RT, Jager C, Zachar G, et al. Chondroitin sulphate proteoglycan-based perineuronal net establishment is largely activity-independent in chick visual system. J Chem Neuroanat 2010; 40: 243-247. doi: 10.1016/j.jchemneu.2010.07.002 PMID: 20621181