Exploring sex differences in the adult zebra finch brain: in vivo diffusion tensor imaging and ex vivo super-resolution track density imaging

Hamaide, J.; De Groof, G.; Van Steenkiste, G.; Jeurissen, B.; Van Audekerke, J.; Naeyaert, M.; Van Ruijssevelt, L.; Cornil, Charlotte; Sijbers, J.; Verhoye, M.; Van der Linden, A.

doi:10.1016/j.neuroimage.2016.09.067

Article (Scientific journals)

Exploring sex differences in the adult zebra finch brain: in vivo diffusion tensor imaging and ex vivo super-resolution track density imaging

Hamaide, J.; De Groof, G.; Van Steenkiste, G. et al.

2017 • In NeuroImage, 146, p. 789-803

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/205398

DOI
10.1016/j.neuroimage.2016.09.067

PubMed
27697612

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Keywords :

DTI; Zebra finch; Super-resolution reconstruction; Songbird; Tractography; Voxel-based analysis

Abstract :

[en] Zebra finches are an excellent model to study the process of vocal learning, a complex socially-learned tool of communication that forms the basis of spoken human language. So far, structural investigation of the zebra finch brain has been performed ex vivo using invasive methods such as histology. These methods are highly specific, however, they strongly interfere with performing whole-brain analyses and exclude longitudinal studies aimed at establishing causal correlations between neuroplastic events and specific behavioral performances. Therefore, the aim of the current study was to implement an in vivo Diffusion Tensor Imaging (DTI) protocol sensitive enough to detect structural sex differences in the adult zebra finch brain. Voxel-wise comparison of male and female DTI parameter maps shows clear differences in several components of the song control system (i.e. Area X surroundings, the high vocal center (HVC) and the lateral magnocellular nucleus of the anterior nidopallium (LMAN)), which corroborate previous findings and are in line with the clear behavioral difference as only males sing. Furthermore, to obtain additional insights into the 3-dimensional organization of the zebra finch brain and clarify findings obtained by the in vivo study, ex vivo DTI data of the male and female brain were acquired as well, using a recently established super-resolution reconstruction (SRR) imaging strategy. Interestingly, the SRR-DTI approach led to a marked reduction in acquisition time without interfering with the (spatial and angular) resolution and SNR which enabled to acquire a data set characterized by a 78μm isotropic resolution including 90 diffusion gradient directions within 44h of scanning time. Based on the reconstructed SRR-DTI maps, whole brain probabilistic Track Density Imaging (TDI) was performed for the purpose of super resolved track density imaging, further pushing the resolution up to 40μm isotropic. The DTI and TDI maps realized atlas-quality anatomical maps that enable a clear delineation of most components of the song control and auditory systems. In conclusion, this study paves the way for longitudinal in vivo and high-resolution ex vivo experiments aimed at disentangling

Disciplines :

Neurosciences & behavior

Author, co-author :

Hamaide, J.

De Groof, G.

Van Steenkiste, G.

Jeurissen, B.

Van Audekerke, J.

Naeyaert, M.

Van Ruijssevelt, L.

Cornil, Charlotte ; Université de Liège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau

Sijbers, J.

Verhoye, M.

Van der Linden, A.

Language :

English

Title :

Exploring sex differences in the adult zebra finch brain: in vivo diffusion tensor imaging and ex vivo super-resolution track density imaging

Publication date :

2017

Journal title :

NeuroImage

ISSN :

1053-8119

eISSN :

1095-9572

Publisher :

Elsevier Science, Orlando, United States - Florida

Volume :

146

Pages :

789-803

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

BELSPO - Service Public Fédéral de Programmation Politique scientifique

Available on ORBi :

since 16 January 2017

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Bibliography

Andersson, J.L.R., Skare, S., Ashburner, J., How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. NeuroImage 20 (2003), 870–888.
Aronov, D., Andalman, A.S., Fee, M.S., A specialized forebrain circuit for vocal babbling in the Juvenile songbird. Science 320 (2008), 630–634.
Aurobrata, G., Rachid, D., A survey of current trends in diffusion MRI for structural brain connectivity. J. Neural Eng., 13, 2016, 011001.
Azadbakht, H., Parkes, L.M., Haroon, H.A., Augath, M., Logothetis, N.K., de Crespigny, A., D'Arceuil, H.E., Parker, G.J.M., Validation of high-resolution tractography against in vivo tracing in the Macaque visual cortex. Cereb. Cortex., 2015.
Bai, Y., Alexander, D.C., 2008. Model-based registration to correct for motion between acquisitions in diffusion MR imaging. In: Proceedings of the Paper presented at: Biomedical Imaging: From Nano to Macro, 2008 ISBI 2008 5th IEEE International Symposium on.
Ball, G.F., Macdougall-Shackleton, S.A., Sex differences in songbirds 25 years later: what have we learned and where do we go?. Microsc. Res. Technol. 54 (2001), 327–334.
Bender, A.T., Veney, S.L., Treatment with the specific estrogen receptor antagonist ICI 182,780 demasculinizes neuron soma size in the developing zebra finch brain. Brain Res. 1246 (2008), 47–53.
Bottjer, S., Miesner, E., Arnold, A., Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224 (1984), 901–903.
Bottjer, S., Glaessner, S., Arnold, A., Ontogeny of brain nuclei controlling song learning and behavior in zebra finches. J. Neurosci. 5 (1985), 1556–1562.
Bottjer, S.W., Miesner, E.A., Arnold, A.P., Changes in neuronal number, density and size account for increases in volume of song-control nuclei during song development in zebra finches. Neurosci. Lett. 67 (1986), 263–268.
Brainard, M.S., Doupe, A.J., Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404 (2000), 762–766.
Brainard, M.S., Doupe, A.J., Translating birdsong: songbirds as a model for basic and applied medical research. Annu. Rev. Neurosci. 36 (2013), 489–517.
Calabrese, E., Badea, A., Cofer, G., Qi, Y., Johnson, G.A., A diffusion MRI tractography connectome of the mouse brain and comparison with neuronal tracer data. Cereb. Cortex, 2015.
Calamante, F., Tournier, J.-D., Jackson, G.D., Connelly, A., Track-density imaging (TDI): super-resolution white matter imaging using whole-brain track-density mapping. NeuroImage 53 (2010), 1233–1243.
Caruyer, E., Lenglet, C., Sapiro, G., Deriche, R., Design of multishell sampling schemes with uniform coverage in diffusion MRI. Magn. Reson. Med. 69 (2013), 1534–1540.
Chen, B., Guo, H., Song, A.W., Correction for direction-dependent distortions in diffusion tensor imaging using matched magnetic field maps. NeuroImage 30 (2006), 121–129.
Cornez, G., ter Haar, S.M., Cornil, C.A., Balthazart, J., Anatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets. PLoS One, 10, 2015, e0123199.
Dauguet, J., Peled, S., Berezovskii, V., Delzescaux, T., Warfield, S.K., Born, R., Westin, C.-F., Comparison of fiber tracts derived from in-vivo DTI tractography with 3D histological neural tract tracer reconstruction on a macaque brain. NeuroImage 37 (2007), 530–538.
De Groof, G., Van der Linden, A., Love songs, bird brains and diffusion tensor imaging. NMR Biomed. 23 (2010), 873–883.
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. 28 (2008), 2475–2485.
De Groof, G., Verhoye, M., Van Meir, V., Tindemans, I., Leemans, A., Van der Linden, A., In vivo diffusion tensor imaging (DTI) of brain subdivisions and vocal pathways in songbirds. NeuroImage 29 (2006), 754–763.
De Groof, G., Verhoye, M., Poirier, C., Leemans, A., Eens, M., Darras, V.M., Van der Linden, A., Structural changes between seasons in the songbird auditory forebrain. J. Neurosci. 29 (2009), 13557–13565.
Doupe, A.J., Kuhl, P.K., BIRDSONG AND HUMAN SPEECH: common themes and mechanisms. Annu. Rev. Neurosci. 22 (1999), 567–631.
Dyrby, T.B., Søgaard, L.V., Parker, G.J., Alexander, D.C., Lind, N.M., Baaré, W.F.C., Hay-Schmidt, A., Eriksen, N., Pakkenberg, B., Paulson, O.B., et al. Validation of in vitro probabilistic tractography. NeuroImage 37 (2007), 1267–1277.
Grisham, W., Arnold, A.P., Distribution of GABA-like immunoreactivity in the song system of the zebra finch. Brain Res. 651 (1994), 115–122.
Grisham, W., Arnold, A.P., A direct comparison of the masculinizing effects of testosterone, androstenedione, estrogen, and progesterone on the development of the zebra finch song system. J. Neurobiol. 26 (1995), 163–170.
Gurney, M., Hormonal control of cell form and number in the zebra finch song system. J. Neurosci. 1 (1981), 658–673.
Gurney, M.E., Behavioral correlates of sexual differentiation in the zebra finch song system. Brain Res. 231 (1982), 153–172.
Holland, D., Kuperman, J.M., Dale, A.M., Efficient correction of inhomogeneous static magnetic field-induced distortion in echo planar imaging. NeuroImage, 50, 2010, 175.
Jarvis, E.D., Learned birdsong and the neurobiology of human language. Ann. N. Y. Acad. Sci. 1016 (2004), 749–777.
Jarvis, E.D., Gunturkun, O., Bruce, L., Csillag, A., Karten, H., Kuenzel, W., Medina, L., Paxinos, G., Perkel, D.J., Shimizu, T., et al. Avian brains and a new understanding of vertebrate brain evolution. Nat. Rev. Neurosci. 6 (2005), 151–159.
Jbabdi, S., Johansen-Berg, H., Tractography – where do we go from here?. Brain Connect. 1 (2011), 169–183.
Jeurissen, B., Tournier, J.-D., Dhollander, T., Connelly, A., Sijbers, J., Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. NeuroImage 103 (2014), 411–426.
Jones, D.K., Horsfield, M.A., Simmons, A., Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn. Reson. Med. 42 (1999), 515–525.
Karten, H.J., Revzin, A.M., The afferent connections of the nucleus rotundus in the pigeon. Brain Res. 2 (1966), 368–377.
Karten, H.J., Hodos, W., Telencephalic projections of the nucleus rotundus in the pigeon (Columba livia). J. Comput. Neurol. 140 (1970), 35–51.
Karten, H.J., Shimizu, T., The origins of neocortex: connections and lamination as distinct events in evolution. J. Cogn. Neurosci. 1 (1989), 291–301.
Karten, H.J., Brzozowska-Prechtl, A., Lovell, P.V., Tang, D.D., Mello, C.V., Wang, H., Mitra, P.P., Digital atlas of the zebra finch (Taeniopygia guttata) brain: a high resolution photo atlas. J. Compar. Neurol. 521 (2013), 3702–3715.
Kirn, J., DeVoogd, T., Genesis and death of vocal control neurons during sexual differentiation in the zebra finch. J. Neurosci. 9 (1989), 3176–3187.
Konishi, M., Akutagawa, E., Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature 315 (1985), 145–147.
Konishi, M., Akutagawa, E., A critical period for estrogen action on neurons of the song control system in the zebra finch. Proc. Natl. Acad. Sci. USA 85 (1988), 7006–7007.
Le Bihan, D., The ‘wet mind’: water and functional neuroimaging. Phys. Med. Biol., 52, 2007, R57.
Lerch, J.P., Gazdzinski, L., Germann, J., Sled, J.G., Henkelman, R.M., Nieman, B.J., Wanted dead or alive? The tradeoff between in-vivo versus ex-vivo MR brain imaging in the mouse. Front. Neuroinform., 2012, 6.
MacDougall-Shackleton, S.A., Ball, G.F., Comparative studies of sex differences in the song-control system of songbirds. Trends Neurosci. 22 (1999), 432–436.
Mackenzie-Graham, A., In Vivo versus Ex Vivo magnetic resonance imaging in mice. Front. Neuroinform., 2012, 6.
Marty, B., Djemaï, B., Robic, C., Port, M., Robert, P., Valette, J., Boumezbeur, F., Le Bihan, D., Lethimonnier, F., Mériaux, S., Hindered diffusion of MRI contrast agents in rat brain extracellular micro-environment assessed by acquisition of dynamic T1 and T2 maps. Contrast Media Mol. Imaging 8 (2013), 12–19.
Meyer, C.E., Boroda, E., Nick, T.A., Sexually dimorphic perineuronal net expression in the songbird. Basal Ganglia 3 (2014), 229–237.
Mooney, R., Rao, M., Waiting periods versus early innervation: the development of axonal connections in the zebra finch song system. J. Neurosci. 14 (1994), 6532–6543.
Mori, S., Zhang, J., Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51 (2006), 527–539.
Nixdorf-Bergweiler, B., von Bohlen und Halbach, V., Major sex differences in the development of myelination are prominent in song system nucleus HVC but not lMAN. Anim. Biol. 54 (2004), 27–43.
Nixdorf-Bergweiler, B.E., Divergent and parallel development in volume sizes of telencephalic song nuclei in and female zebra finches. J. Comput. Neurol. 375 (1996), 445–456.
Nixdorf-Bergweiler, B.E., Lateral magnocellular nucleus of the anterior neostriatum (LMAN) in the zebra finch: neuronal connectivity and the emergence of sex differences in cell morphology. Microsc. Res. Technol. 54 (2001), 335–353.
Nixdorf-Bergweiler, B., Bischof, H.-J., 2007. Atlas of The Brain of The Zebra Finch, Taeniopygia Guttata: With Special Emphasis on Telencephalic Visual and Song System Nuclei in Transverse and Sagittal Sections.
Nottebohm, F., Arnold, A., Sexual dimorphism in vocal control areas of the songbird brain. Science 194 (1976), 211–213.
Nottebohm, F., Arnold, A.P., Sexual dimorphism in vocal control areas of the songbird brain. Science 194 (1976), 211–213.
Ölveczky, B.P., Andalman, A.S., Fee, M.S., Vocal experimentation in the Juvenile songbird requires a Basal Ganglia circuit. PLoS Biol., 3, 2005, e153.
Paton, J., O'Loughlin, B., Nottebohm, F., Cells born in adult canary forebrain are local interneurons. J. Neurosci. 5 (1985), 3088–3093.
Person, A.L., Gale, S.D., Farries, M.A., Perkel, D.J., Organization of the songbird basal ganglia, including area X. J. Comput. Neurol. 508 (2008), 840–866.
Pinaud, R., Mello, C.V., GABA immunoreactivity in auditory and song control brain areas of zebra finches. J. Chem. Neuroanat. 34:1 (2007), 1–2.
Poirier, C., Vellema, M., Verhoye, M., Van Meir, V., Wild, J.M., Balthazart, J., Van Der Linden, A., A three-dimensional MRI atlas of the zebra finch brain in stereotaxic coordinates. NeuroImage 41 (2008), 1–6.
Poot, D.H.J., Van Meir, V., Sijbers, J., General and efficient super-resolution method for multi-slice MRI. Jiang, T., Navab, N., Pluim, J.W., Viergever, M., (eds.) Medical Image Computing and Computer-Assisted Intervention – MICCAI 2010, 2010, Springer, Berlin Heidelberg, 615–622.
Porter, D.A., Heidemann, R.M., High resolution diffusion-weighted imaging using readout-segmented echo-planar imaging, parallel imaging and a two-dimensional navigator-based reacquisition. Magn. Reson. Med. 62 (2009), 468–475.
Reiner, A., Laverghetta, A.V., Meade, C.A., Cuthbertson, S.L., Bottjer, S.W., An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch. J. Comput. Neurol. 469 (2004), 239–261.
Reisinger, C., Gluecker, T., Jacob, A.L., Bongartz, G., Bilecen, D., Dynamic magnetic resonance angiography of the arteries of the hand. A comparison between an extracellular and an intravascular contrast agent. Eur. Radiol. 19 (2008), 495–502.
Scharff, C., Nottebohm, F., 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 (1991), 2896–2913.
Schmidt, A., Bischof, H.-J., Integration of information from both eyes by single neurons of nucleus rotundus, ectostriatum and lateral neostriatum in the zebra finch (Taeniopygia guttata castanotis Gould). Brain Res. 923 (2001), 20–31.
Simpson, H., Vicario, D., Brain pathways for learned and unlearned vocalizations differ in zebra finches. J. Neurosci. 10 (1990), 1541–1556.
Tax, C.M.W., Jeurissen, B., Vos, S.B., Viergever, M.A., Leemans, A., Recursive calibration of the fiber response function for spherical deconvolution of diffusion MRI data. NeuroImage 86 (2014), 67–80.
Thomas, C., Ye, F.Q., Irfanoglu, M.O., Modi, P., Saleem, K.S., Leopold, D.A., Pierpaoli, C., Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc. Natl. Acad. Sci. USA 111 (2014), 16574–16579.
Toga, A.W., Thompson, P.M., Mapping brain asymmetry. Nat. Rev. Neurosci. 4 (2003), 37–48.
Tournier, J.D., Calamante, F., Connelly, A., Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage 35 (2007), 1459–1472.
Tournier, J.D., Calamante, F., Connelly, A., MRtrix: diffusion tractography in crossing fiber regions. Int. J. Imaging Syst. Technol. 22 (2012), 53–66.
Tournier, J.C., F., Connelly, A., 2010. Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions. Paper presented at: International Society for Magnetic Resonance in Medicine (ISMRM), Stockholm.
Van der Linden, A., Verhoye, M., Van Audekerke, J., Peeters, R., Eens, M., Newman, S.W., Smulders, T., Balthazart, J., DeVoogd, T.J., Noninvasive in vivo anatomical studies of the oscine brain by high resolution MRI microscopy. J. Neurosci. Methods 81 (1998), 45–52.
Van Steenkiste, G., Jeurissen, B., Veraart, J., den Dekker, A.J., Parizel, P.M., Poot, D.H.J., Sijbers, J., Super-resolution reconstruction of diffusion parameters from diffusion-weighted images with different slice orientations. Magn. Reson. Med. 75 (2016), 181–195.
Verhoye, M., Van der Linden, A., Van Audekerke, J., Sijbers, J., Eens, M., Balthazart, J., Imaging birds in a bird cage: in-vivo FSE 3D MRI of bird brain. Magn. Reson. Mater. Phys. Biol. Med. 6 (1998), 22–27.
Wade, J., Arnold, A.P., Sexual differentiation of the zebra finch song system. Ann. N. Y. Acad. Sci. 1016 (2004), 540–559.
Wang, J., Sakaguchi, H., Sokabe, M., Sex differences in the vocal motor pathway of the zebra finch revealed by real-time optical imaging technique. NeuroReport 10 (1999), 2487–2491.
Wild, J.M., Descending projections of the songbird nucleus robustus archistriatalis. J. Comput. Neurol. 338 (1993), 225–241.
Wild, J.M., Neural pathways for the control of birdsong production. J. Neurobiol. 33 (1997), 653–670.
Yu, A.C., Margoliash, D., Temporal hierarchical control of singing in birds. Science 273 (1996), 1871–1875.
Zatorre, R.J., Fields, R.D., Johansen-Berg, H., Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat. Neurosci. 15 (2012), 528–536.