Seasonal rewiring of the songbird brain: An in vivo MRI study

European Journal of Neuroscience

Volumn 28, Issue 12, 2008, Pages 2475-2485

  De Groof, Geert ^a   Verhoye, Marleen ^a   Van Meir, Vincent ^a   Balthazart, Jacques ^b   Van Der Linden, Annemie ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Diffusion tensor imaging; Optic chiasma; Seasonal plasticity; Song control system; Starling (sturnus vulgaris)

Indexed keywords

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BREEDING; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; IN VIVO STUDY; MALE; MYELINATED NERVE; NERVE CELL PLASTICITY; NONHUMAN; OPTIC CHIASM; PRIORITY JOURNAL; SEASONAL VARIATION; SONGBIRD;

ANIMALS; BRAIN; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; MALE; NEURAL PATHWAYS; NEURONAL PLASTICITY; SEASONS; SEXUAL BEHAVIOR, ANIMAL; STARLINGS; VOCALIZATION, ANIMAL;

EID: 57449091874     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06545.x     Document Type: Article

References (83)

1. Alvarez-Buylla, A., Theelen, M. Nottebohm, F. (1988) Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning. Proc. Natl Acad. Sci U S A, 85, 8722 8726.
2. Ball, G.F., Riters, L.V. Balthazart, J. (2002) Neuroendocrinology of song behavior and avian brain plasticity: multiple sites of action of sex steroid hormones. Front. Neuroendocrinol., 23, 137 178.
3. Ball, G.F., Auger, C.J., Bernard, D.J., Charlier, T.D., Sartor, J.J., Riters, L.V. Balthazart, J. (2004) Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann. N. Y. Acad. Sci., 1016, 586 610.
4. Basser, P.J., Mattiello, J. LeBihan, D. (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J. Magn. Reson. B, 103, 247 254.
5. Beaulieu, C. (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed., 15, 435 455.
6. Bernard, D.J. Ball, G.F. (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.
7. Bernard, D.J. Ball, G.F. (1997) Photoperiodic condition modulates the effects of testosterone on song control nuclei volumes in male European starlings. Gen. Comp. Endocrinol., 105, 276 283.
8. Bernard, D.J., Bentley, G.E., Balthazart, J., Turek, F.W. Ball, G.F. (1999) Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology, 140, 4633 4643.
9. Bottjer, S.W., Halsema, K.A., Brown, S.A. Miesner, E.A. (1989) Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J. Comp. Neurol., 279, 312 326.
10. Brainard, M.S. Doupe, A.J. (2000) Auditory feedback in learning and maintenance of vocal behaviour. Nat. Rev. Neurosci., 1, 31 40.
11. Brenowitz, E.A. (2004) Plasticity of the adult avian song control system. Ann. N. Y. Acad. Sci., 1016, 560 585.
12. Brenowitz, E.A., Nalls, B., Wingfield, J.C. Kroodsma, D.E. (1991) Seasonal changes in avian song nuclei without seasonal changes in song repertoire. J. Neurosci., 11, 1367 1374.
13. Brenowitz, E.A., Baptista, L.F., Lent, K. Wingfield, J.C. (1998) Seasonal plasticity of the song control system in wild Nuttall's white- crowned sparrows. J. Neurobiol., 34, 69 82.
14. Caro, S.P., Lambrechts, M.M. Balthazart, J. (2005) Early seasonal development of brain song control nuclei in male blue tits. Neurosci. Lett., 386, 139 144.
15. Cascio, C.J., Gerig, G. Piven, J. (2007) Diffusion tensor imaging: application to the study of the developing brain. J. Am. Acad. Child Adolesc. Psychiatry., 46, 213 223.
16. Celotti, F., Melcangi, R.C., Negri-Cesi, P., Ballabio, M. Martini, L. (1987) Differential distribution of the 5-alpha-reductase in the central nervous system of the rat and the mouse: are the white matter structures of the brain target tissue for testosterone action? J. Steroid. Biochem., 26, 125 129.
17. Dawson, A. (1983) Plasma gonadal steroid levels in wild starlings (Sturnus vulgaris) during the annual cycle and in relation to the stages of breeding. Gen. Comp. Endocrinol., 49, 286 294.
18. De Groof, G., Verhoye, M., Van Meir, V., Tindemans, I., Leemans, A. Van der Linden, A. (2006) In vivo diffusion tensor imaging (DTI) of brain subdivisions and vocal pathways in songbirds. Neuroimage, 29, 754 763.
19. Eens, M. (1997) Understanding the complex song of the European starling: an integrated ethological approach. Adv. Study. Anim. Behav., 26, 355 434.
20. Fusani, L., Van't Hof, T., Hutchison, J.B. Gahr, M. (2000) Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. J. Neurobiol., 43, 254 268.
21. Hessler, N.A. Doupe, A.J. (1999) Singing-related neural activity in a dorsal forebrain-basal ganglia circuit of adult zebra finches. J. Neurosci., 19, 10461 10481.
22. Hidalgo, A., Barami, K., Iversen, K. Goldman, S.A. (1995) Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J. Neurobiol., 27, 470 487.
23. Hill, K.M. DeVoogd, T.J. (1991) Altered daylength affects dendritic structure in a song-related brain region in red-winged blackbirds. Behav. Neural Biol., 56, 240 250.
24. Holloway, C.C. Clayton, D.E. (2001) Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat. Neurosci., 4, 170 175.
25. Huppi, P.S. Dubois, J. (2006) Diffusion tensor imaging of brain development. Semin. Fetal. Neonatal Med., 11, 489 497.
26. Ishibashi, T., Dakin, K.A., Stevens, B., Lee, P.R., Kozlov, S.V., Stewart, C.L. Fields, R.D. (2006) Astrocytes promote myelination in response to electrical impulses. Neuron, 49, 823 832.
27. Jarvis, E.D. Nottebohm, F. (1997) Motor-driven gene expression. Proc. Natl Acad. Sci U S A, 94, 4097 4102.
28. Kirn, J.R. Nottebohm, F. (1993) Direct evidence for loss and replacement of projection neurons in adult canary brain. J. Neurosci., 13, 1654 1663.
29. Kirn, J.R., Clower, R.P., Kroodsma, D.E. DeVoogd, T.J. (1989) Song-related brain regions in the red-winged blackbird are affected by sex and season but not repertoire size. J. Neurobiol., 20, 139 163.
30. Konishi, M. Akutagawa, E. (1985) Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature, 315, 145 147.
31. Kozhevnikov, A.A. Fee, M.S. (2007) Singing-related activity of identified HVC neurons in the zebra finch. J. Neurophysiol., 97, 4271 4283.
32. Le Bihan, D., Mangin, J.F., Poupon, C., Clark, C.A., Pappata, S., Molko, N. Chabriat, H. (2001) Diffusion tensor imaging: concepts and applications. J. Magn. Reson. Imaging., 13, 534 546.
33. Lebel, C., Walker, L., Leemans, A., Phillips, L. Beaulieu, C. (2008) Microstructural maturation of the human brain from childhood to adulthood. NeuroImage, 40, 1044 1055.
34. Leemans, A., Sijbers, J. Parizel, P. (2005). "A Graphical Toolbox for Exploratory Diffusion Tensor Imaging and Fiber Tractography", Section for Magnetic Resonance Technologists (SMRT) - 14th Annual Meeting in Miami Beach. Florida, USA.
35. Maes, F., Collignon, A., Vandermeulen, D., Marchal, G. Suetens, P. (1997) Multimodality image registration by maximization of mutual information. IEEE. Trans. Med Imaging., 16, 187 198.
36. Magnaghi, V., Cavarretta, I., Zucchi, I., Susani, L., Rupprecht, R., Hermann, B., Martini, L. Melcangi, R.C. (1999) Po gene expression is modulated by androgens in the sciatic nerve of adult male rats. Brain Res. Mol. Brain Res., 70, 36 44.
37. Magnaghi, V., Ballabio, M., Gonzalez, L.C., Leonelli, E., Motta, M. Melcangi, R.C. (2004) The synthesis of glycoprotein Po and peripheral myelin protein 22 in sciatic nerve of male rats is modulated by testosterone metabolites. Brain Res. Mol. Brain Res., 126, 67 73.
38. Mattiello, J., Basser, P.J. Le Bihan, D. (1997) The b matrix in diffusion tensor echo-planar imaging. Magn. Reson. Med., 37, 292 300.
39. Meitzen, J., Perkel, D.J. Brenowitz, E.A. (2007) Seasonal changes in intrinsic electrophysiological activity of song control neurons in wild song sparrows. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol., 193, 677 683.
40. Melcangi, R.C., Celotti, F., Ballabio, M., Poletti, A., Castano, P. Martini, L. (1988) Testosterone 5 alpha-reductase activity in the rat brain is highly concentrated in white matter structures and in purified myelin sheaths of axons. J. Steroid Biochem., 31, 173 179.
41. Mori, S. Zhang, J. (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron, 51, 527 539.
42. Nottebohm, F. (1981) A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science, 214, 1368 1370.
43. Nottebohm, F., Stokes, T.M. Leonard, C.M. (1976) Central control of song in the canary, Serinus canarius. J. Comp. Neurol., 165, 457 486.
44. Nottebohm, F., Kelley, D.B. Paton, J.A. (1982) Connections of vocal control nuclei in the canary telencephalon. J. Comp. Neurol., 207, 344 357.
45. Olveczky, B.P., Andalman, A.S. Fee, M.S. (2005) Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol, 3, e153.
46. Park, K.H., Meitzen, J., Moore, I.T., Brenowitz, E.A. Perkel, D.J. (2005) Seasonal-like plasticity of spontaneous firing rate in a songbird pre-motor nucleus. J. Neurobiol., 64, 181 191.
47. Partridge, S.C., Mukherjee, P., Henry, R.G., Miller, S.P., Berman, J.I., Jin, H., Lu, Y., Glenn, O.A., Ferriero, D.M., Barkovich, A.J. Vigneron, D.B. (2004) Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. NeuroImage, 22, 1302 1314.
48. Paton, J.A., O'Loughlin, B.E. Nottebohm, F. (1985) Cells born in adult canary forebrain are local interneurons. J. Neurosci., 5, 3088 3093.
49. Phillmore, L.S., Hoshooley, J.S., Sherry, D.F. dougall-Shackleton, S.A. (2006) Annual cycle of the black-capped chickadee: seasonality of singing rates and vocal-control brain regions. J. Neurobiol., 66, 1002 1010.
50. Pierpaoli, C. Basser, P.J. (1996) Toward a quantitative assessment of diffusion anisotropy. Magn. Reson. Med., 36, 893 906.
51. Poletti, A. Martini, L. (1999) Androgen-activating enzymes in the central nervous system. J. Steroid Biochem. Mol. Biol., 69, 117 122.
52. Rasika, S., Nottebohm, F. Alvarez-Buylla, A. (1994) Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc. Natl Acad. Sci U S A, 91, 7854 7858.
53. Reiner, A., Perkel, D.J., Bruce, L.L., Butler, A.B., Csillag, A., Kuenzel, W., Medina, L., Paxinos, G., Shimizu, T., Striedter, G., Wild, M., Ball, G.F., Durand, S., Guturkun, O., Lee, D.W., Mello, C.V., Powers, A., White, S.A., Hough, G., Kubikova, L., Smulders, T.V., Wada, K., Dugas, F., Husband, S., Yamamoto, K., Yu, J., Siang, C. Jarvis, E.D. (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol., 473, 377 414.
54. Riters, L.V., Baillien, M., Eens, M., Pinxten, R., Foidart, A., Ball, G.F. Balthazart, J. (2001) Seasonal variation in androgen-metabolizing enzymes in the diencephalon and telencephalon of the male European starling (Sturnus vulgaris). J. Neuroendocrinol., 13, 985 997.
55. Rose, S.E., Chen, F., Chalk, J.B., Zelaya, F.O., Strugnell, W.E., Benson, M., Semple, J. Doddrell, D.M. (2000) Loss of connectivity in Alzheimer's disease: an evaluation of white matter tract integrity with colour coded MR diffusion tensor imaging. J. Neurol. Neurosurg. Psychiatry., 69, 528 530.
56. Rosen, M.J. Mooney, R. (2006) Synaptic interactions underlying song-selectivity in the avian nucleus HVC revealed by dual intracellular recordings. J. Neurophysiol., 95, 1158 1175.
57. Saldanha, C.J., Tuerk, M.J., Kim, Y.H., Fernandes, A.O., Arnold, A.P. Schlinger, B.A. (2000) Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J. Comp. Neurol., 423, 619 630.
58. Schlinger, B. (2002) Neural and hormonal control of birdsong. In Schlinger, B.A. Brenowitz, E. (Eds Hormones, Brain and Behavior. Academic Press, San Diego, pp. 799 839.
59. Schmidt, M.F., Ashmore, R.C. Vu, E.T. (2004) Bilateral control and interhemispheric coordination in the avian song motor system. Ann. N. Y. Acad. Sci., 1016, 171 187.
60. Shen, P., Schlinger, B.A., Campagnoni, A.T. Arnold, A.P. (1995) An atlas of aromatase mRNA expression in the zebra finch brain. J. Comp. Neurol., 360, 172 184.
61. Smith, G.T. (1996) Seasonal plasticity in the song nuclei of wild rufous-sided towhees. Brain Res., 734, 79 85.
62. Smith, G.T., Brenowitz, E.A., Wingfield, J.C. Baptista, L.F. (1995) Seasonal changes in song nuclei and song behavior in Gambel's white- crowned sparrows. J. Neurobiol., 28, 114 125.
63. Soma, K.K., Tramontin, A.D., Featherstone, J. Brenowitz, E.A. (2004) Estrogen contributes to seasonal plasticity of the adult avian song control system. J. Neurobiol., 58, 413 422.
64. Song, S.K., Sun, S.W., Ramsbottom, M.J., Chang, C., Russell, J. Cross, A.H. (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage, 17, 1429 1436.
65. Song, S.K., Yoshino, J., Le, T.Q., Lin, S.J., Sun, S.W., Cross, A.H. Armstrong, R.C. (2005) Demyelination increases radial diffusivity in corpus callosum of mouse brain. NeuroImage, 26, 132 140.
66. Stocker, S., Guttinger, H.R. Herth, G. (1994) Exogenous testosterone differentially affects myelination and neurone soma sizes in the brain of canaries. Neuroreport, 5, 1449 1452.
67. Stokes, T.M., Leonard, C.M. Nottebohm, F. (1974) The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J. Comp. Neurol., 156, 337 374.
68. Striedter, G.F. Vu, E.T. (1998) Bilateral feedback projections to the forebrain in the premotor network for singing in zebra finches. J. Neurobiol., 34, 27 40.
69. Taber, K.H., Pierpaoli, C., Rose, S.E., Rugg-Gunn, F.J., Chalk, J.B., Jones, D.K. Hurley, R.A. (2002) The future for diffusion tensor imaging in neuropsychiatry. J. Neuropsychiatry Clin. Neurosci., 14, 1 5.
70. Thompson, C.K. Brenowitz, E.A. (2005) Seasonal change in neuron size and spacing but not neuronal recruitment in a basal ganglia nucleus in the avian song control system. J. Comp. Neurol., 481, 276 283.
71. Thompson, C.K., Bentley, G.E. Brenowitz, E.A. (2007) Rapid seasonal-like regression of the adult avian song control system. Proc. Natl Acad. Sci U S A, 104, 15520 15525.
72. Tindemans, I., Verhoye, M., Balthazart, J. Van der Linden, A. (2003) In vivo dynamic ME-MRI reveals differential functional responses of RA- and area X-projecting neurons in the HVC of canaries exposed to conspecific song. Eur. J. Neurosci., 18, 3352 3360.
73. Tramontin, A.D. Brenowitz, E.A. (1999) A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning. J. Neurobiol., 40, 316 326.
74. Tramontin, A.D. Brenowitz, E.A. (2000) Seasonal plasticity in the adult brain. Trends Neurosci., 23, 251 258.
75. Ulug, A.M., Moore, D.F., Bojko, A.S. Zimmerman, R.D. (1999) Clinical use of diffusion-tensor imaging for diseases causing neuronal and axonal damage. AJNR Am. J. Neuroradiol., 20, 1044 1048.
76. Van der Linden, A., Van Meir, V., Tindemans, I., Verhoye, M. Balthazart, J. (2004) Applications of manganese-enhanced magnetic resonance imaging (MEMRI) to image brain plasticity in song birds. NMR Biomed., 17, 602 612.
77. Van Meir, V., Verhoye, M., Absil, P., Eens, M., Balthazart, J. Van der Linden, A. (2004) Differential effects of testosterone on neuronal populations and their connections in a sensorimotor brain nucleus controlling song production in songbirds: a manganese enhanced-magnetic resonance imaging study. Neuroimage, 21, 914 923.
78. Van Meir, V., Pavlova, D., Verhoye, M., Pinxten, R., Balthazart, J., Eens, M. Van der Linden, A. (2006) In vivo MR imaging of the seasonal volumetric and functional plasticity of song control nuclei in relation to song output in a female songbird. NeuroImage, 31, 981 992.
79. Vates, G.E. Nottebohm, F. (1995) Feedback circuitry within a song-learning pathway. Proc. Natl Acad. Sci U S A, 92, 5139 5143.
80. Waxman, S.G. (1977) Conduction in myelinated, unmyelinated, and demyelinated fibers. Arch. Neurol., 34, 585 589.
81. Wild, J.M. (1993) Descending projections of the songbird nucleus robustus archistriatalis. J. Comp. Neurol., 338, 225 241.
82. Wild, J.M. (2004) Functional neuroanatomy of the sensorimotor control of singing. Ann. N. Y. Acad. Sci., 1016, 438 462.
83. Wimberger, D.M., Roberts, T.P., Barkovich, A.J., Prayer, L.M., Moseley, M.E. Kucharczyk, J. (1995) Identification of "premyelination" by diffusion-weighted MRI. J. Comput. Assist. Tomogr., 19, 28 33.