oscines; song-control nuclei; magnetic resonance imaging; in vivo tract tracing; in vivo axonal transport; sex differences
Abstract :
[en] Injection of manganese (Mn2+), a paramagnetic tract tracing agent and calcium analogue, into the high vocal center of starlings labeled within a few hours the nucleus robustus archistriatalis and area X as observed by in vivo magnetic resonance imaging. Structures highlighted by Mn2+ accumulation assumed the expected tri-dimensional shape of the nucleus robustus archistriatalis and area X as identified by classical histological or neurochemical methods. The volume of these nuclei could be accurately calculated by segmentation of the areas highlighted by Mn2+. Besides confirming previously established volumetric sex differences, Mn2+ uptake into these nuclei revealed new functional sex differences affecting Mn2+ transport. A faster transport was observed in males than in females and different relative amounts of Mn2+ were transported to nucleus robustus archistriatalis and area X in males as compared to females. This new in vivo approach, allowing repeated measures, opens new vistas to study the remarkable seasonal plasticity in size and activity of song-control nuclei and correlate neuronal activity with behavior. It also provides new insights on in vivo axonal transport and neuronal activity in song-control nuclei of oscines. (C) 2002 IBRO. Published by Elsevier Science Ltd. All rights reserved.
Disciplines :
Neurosciences & behavior
Author, co-author :
Van der Linden, A.
Verhoye, M.
Van Meir, V.
Tindemans, I.
Eens, M.
Absil, Philippe ; Université de Liège - ULiège > Centre de recherches du cyclotron
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
In vivo manganese-enhanced magnetic resonance imaging reveals connections and functional properties of the songbird vocal control system
Publication date :
2002
Journal title :
Neuroscience
ISSN :
0306-4522
eISSN :
1873-7544
Publisher :
Pergamon-Elsevier Science Ltd, Oxford, United Kingdom
Alvarez-Buylla A., Kirn J.R., Nottebohm F. (1990) Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 249:1444-1446.
Alvarez-Buylla A., Kirn J.R. (1997) Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J. Neurobiol. 33:585-601.
Ball G.F., Casto J.M., Bernard D.J. (1994) Sex differences in the volume of avian song control nuclei: Comparative studies and the issue of brain nucleus delineation. Psychoneuroendocrinology 19:485-504.
Balthazart J., Absil P. (1997) Identification of catecholaminergic inputs to and outputs from aromatase-containing brain areas of the Japanese quail by retrograde tracing combined with tyrosine hydroxylase immunocytochemistry. J. Comp. Neurol. 382:401-428.
Bernard D.J., Casto J.M., Ball G.F. (1993) Sexual dimorphism in the volume of the song control nuclei in European starlings: Assessment by a Nissl stain and autoradiography for muscarinic cholinergic receptors. J. Comp. Neurol. 334:559-570.
Bernard D.J., Eens M., Ball G.F. (1996) Age- and behavior-related variation in volumes of song control nuclei in male European starlings. J. Neurobiol. 30:329-339.
Brenowitz E.A. (1997) Comparative approaches to the avian song system. J. Neurobiol. 33:517-531.
Brenowitz E.A., Smith G.T. (1997) Letter to the Editor. TINS 20:345.
Dermon C.R., Stamatakis A., Tlemçani O., Balthazart J. (1999) Performance of appetitive or consummatory components of male sexual behavior is mediated by different brain areas: A 2-deoxyglucose autoradiographic study. Neuroscience 94:1261-1277.
Doupe A.J., Kuhl P.K. (1999) Birdsong and human speech: Common themes and mechanisms. Annu. Rev. Neurosci. 22:567-631.
Duffy D.L., Bentley G.E., Ball G.F. (1999) Does sex or photoperiodic condition influence ZENK induction in response to song in European starlings?. Brain Res. 844:78-82.
Eens M. (1997) Understanding the complex song of the European starling: An integrated ethological approach. Adv. Study Anim. Behav. 26:355-434.
Gahr M. (1990) Delineation of a brain nucleus: Comparisons of cytochemical, hodological, and cytoarchitectural views of the song control nucleus HVC of the adult canary. J. Comp. Neurol. 294:30-36.
Gahr M. (1997) How should brain nuclei be delineated? Consequences for developmental mechanisms and for correlations of area size, neuron numbers, and functions of brain nuclei. TINS 20:58-62.
Gallez B., Demeure R., Baudelet C., Abdelahouab N., Beghein N., Jordan B.F., Geurts M., Roels H. (2000) Non invasive quantification of manganese deposits in the rat brain by measurement of Tl. Abstract in Proc. Intl. Soc. Mag. Reson. Med. , Denver, CO; 8:2013.
Grafstein B., Forman D. (1980) Intracellular transport in neurons. Physiol. Rev. 60:1167-1283.
Holloway C.C., Clayton D.F. (2001) Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat. Neurosci. 4:170-175.
Jarvis E.D., Nottebohm F. (1997) Motor-driven gene expression. Proc. Natl. Acad. Sci. USA 94:4097-4102.
Jarvis E.D., Scharff C., Grossman M.R., Ramos J.A., Nottebohm F. (1998) For whom the birds sings: Context-dependent gene expression. Neuron 21:775-788.
Kelley D.B., Nottebohm F. (1979) Projections of a telencephalic auditory nucleus - Field L - in the canary. J. Comp. Neurol. 183:455-470.
Konishi M., Akutagawa E. (1985) Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch. Nature 315:145-147.
Kroodsma D., Konishi M. (1991) A suboscine bird (Eastern phoebe, Sayornis phoebe) develops normal song without auditory feedback. Anim. Behav. 42:477-487.
Lin Y., Koretsky A.P. (1997) Manganese ion enhances T1-weighted MRI during brain activation: An approach to direct imaging of brain function. Magn. Reson. Med. 38:378-388.
MacDougall-Shackleton S.A., Ball G.F. (1999) Comparative studies of sex differences in the song-control system of songbirds. TINS 22:432-436.
Marler P. (1991) Song-learning: The interface with neuroethology. TINS 14:199-206.
Meddle S.L., Foidart A., Wingfield J.C., Ramenofsky M., Balthazart J. (1999) Effects of sexual interactions with a male on Fos-like immunoreactivity in the female quail brain. J. Neuroendocrinol. 11:771-784.
Meddle S.L., King V.M., Follett B.K., Wingfield J.C., Ramenofsky M., Foidart A., Balthazart J. (1997) Copulation activates Fos-like immunoreactivity in the male quail forebrain. Behav. Brain Res. 85:143-159.
Mello C.V., Ribeiro S. (1998) ZENK protein regulation by song in the brain of songbirds. J. Comp. Neurol. 393:426-438.
Mello C.V., Vates G.E., Okuhata S., Nottebohm F. (1998) Descending auditory pathways in the adult male zebra finch (Taeniopygia guttata). J. Comp. Neurol. 395:137-160.
Narita K., Kawasaki F., Kita H. (1990) Mn and Mg influxes through Ca channels of motor terminals are prevented by verapamil in frogs. Brain Res. 510:289-329.
Nottebohm F. (1981) A brain for all seasons: Cyclical anatomical changes in song-control nuclei of the canary brain. Science 214:1368-1370.
Nottebohm F. (1991) Reassessing the mechanisms and origins of vocal learning in birds. TINS 14:206-211.
Nottebohm F. (1993) The search for neural mechanisms that define the sensitive period for song learning in birds. Neth. J. Zool. 43:193-234.
Pautler R.G., Silva A.C., Koretsky A.P. (1998) In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging. MRM 40:740-748.
Pautler R.G., Koretsky A.P. (2000) Manganese enhanced MRI neuronal tract tracing in response to odor stimulation in mice. Abstract in Proc. Intl. Soc. Mag. Reson. Med. , Denver, CO, USA, 1-7 April 2000; 2014.
Van der Linden A., Verhoye M., Van Audekerke J., Peeters R., Eens M., Newman S.W., Smulders T., Balthazart J., Devoogd T.J. (1998) Non invasive in vivo anatomical studies of the oscine brain by high resolution MRI microscopy. J. Neurosci. Methods 81:45-52.
Vates G.E., Broome B.E., Mello C.V., Nottebohm F. (1996) Auditory patways of caudal telencephalon and their relation to the song system of male zebra finches (Taeniopygia guttata). J. Comp. Neurol. 366:613-642.
Verhoye M., Van der Linden A., Van Audekerke J., Sijbers J., Eens M., Balthazart J. (1998) Imaging birds in a bird cage: In vivo FSE 3D MRI of bird brain. Magma 6:22-27.
Wang J., Sakaguchi H., Sokabe M. (1999) Sex differences in the vocal motor pathway of the zebra finch revealed by real-time optical imaging technique. NeuroReport 10:2487-2491.