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
starling; songbird; song control nuclei; HVC; RA; area X; brain plasticity; testosterone; manganese enhanced-MRI
Abstract :
[en] Nucleus HVC (formerly called high vocal center) of songbirds contains two types of projecting neurons connecting HVC respectively to the nucleus robustus archistriatalis, RA, or to area X. These two neuron classes exhibit multiple neurochemical differences and are differentially replaced by new neurons during adult life: high rates of neuronal replacement are observed in RA-projecting neurons only. The activity of these two types of neurons may also be modulated differentially by steroids. We analyzed by magnetic resonance imaging the effect of testosterone on the volume of RA and area X and on the dynamics of Mn2+ accumulation in RA and area X of female starlings that had been injected with MnCl2 through a permanent cannula implanted in HVC. Repeated visualization 6 weeks apart (before and after testosterone treatment) identified a volume increase of both nuclei in testosterone-treated birds associated with a concomitant decrease in controls. Following testosterone treatment, the total amount of Mn2+ transported to RA and area X increased but the dynamics of accumulation, reflecting in part the activity of HVC neurons, was specifically altered in area X but not in RA. These data indicate that testosterone differentially affects the RA- and area X-projecting neurons in HVC. Manganese-enhanced magnetic resonance imaging (ME-MRI) thus provides repeated measures of connected brain areas and demonstrates testosterone-dependent regionally specific changes in brain activity and functional connectivity. The slow time scales investigated by this technique (compared to functional MRI) appear ideally suited for characterizing slow processes such as those involved in brain plasticity and learning. (C) 2004 Elsevier Inc. All rights reserved.
Disciplines :
Neurosciences & behavior Radiology, nuclear medicine & imaging
Author, co-author :
Van Meir, V.
Verhoye, M.
Absil, Philippe ; Université de Liège - ULiège > Centre de recherches du cyclotron
Eens, M.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Van der Linden, A.
Language :
English
Title :
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
Publication date :
March 2004
Journal title :
NeuroImage
ISSN :
1053-8119
eISSN :
1095-9572
Publisher :
Academic Press Inc Elsevier Science, San Diego, United States - California
Adkins-Regan E., Ascenzi M. Sexual differentiation of behavior in the zebra finch: effect of early gonadectomy or androgen treatment. Horm. Behav. 24:1990;114-127.
Alvarez-Buylla A., Kirn J.R. Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J. Neurobiol. 33:1997;585-601.
Aoki I., Tanaka C., Takegami T., Ebisu T., Umeda M., Fukunaga M., Fukuda K., Silva A.C., Koretsky A.P., Naruse S. Dynamic activity-induced manganese-dependent contrast magnetic resonance imaging (DAIM MRI). Magn. Reson. Med. 48:2002;927-933.
Arnold A.P. Effects of androgens on volumes of sexually dimorphic brain regions in the zebra finch. Brain Res. 185:1980;441-444.
Ball G.F., Wingfield J.C. Changes in plasma levels of luteinizing-hormone and sex steroid hormones in relation to multiple- broodedness and nest-site density in male starlings. Physiol. Zool. 60:1987;191-199.
Ball G.F., Riters L.V., Balthazart J. Neuroendocrinology of song behavior and avian brain plasticity: multiple sites of action of sex steroid hormones. Front. Neuroendocrinol. 23:2002;137-178.
Balthazart J., Absil P., Foidart A., Houbart M., Harada N., Ball G.F. Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J. Neurobiol. 31:1996;129-148.
Bernard D.J., Bentley G.E., Balthazart J., Turek F.W., Ball G.F. Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology. 140:1999;4633-4643.
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. Auditory feedback in learning and maintenance of vocal behaviour. Nat. Rev., Neurosci. 1:2000;31-40.
Brenowitz E.A., Margoliash D., Nordeen K.W. An introduction to birdsong and the avian song system. J. Neurobiol. 33:1997;495-500.
Brown S.D., Bottjer S.W. Testosterone-induced changes in adult canary brain are reversible. J. Neurobiol. 24:1993;627-640.
De Ridder E., Pinxten R., Mees V., Eens M. Short- and long-term effects of male-like concentrations of testosterone on female European starlings (Sturnus vulgaris). Auk. 119:2002;487-497.
Del Negro C., Edeline J.M. Sex and season influence the proportion of thin spike cells in the canary HVC. NeuroReport. 13:2002;2005-2009.
Duffy D.L., Bentley G.E., Drazen D.L., Ball G.F. Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav. Ecol. 11:2000;654-662.
Duong T.Q., Silva A.C., Lee S.P., Kim S.G. Functional MRI of calcium-dependent synaptic activity: cross correlation with CBF and BOLD measurements. Magn. Reson. Med. 43:2000;383-392.
Eens M. Understanding the complex song of the European starling: an integrated ethological approach. Adv. Study Behav. 26:1997;355-434.
Eens M., Van Duyse E., Berghman L., Pinxten R. Shield characteristics are testosterone-dependent in both male and female moorhens. Horm. Behav. 37:2000;126-134.
Fusani L., Hutchison J.B., Gahr M. Testosterone regulates the activity and expression of aromatase in the canary neostriatum. J. Neurobiol. 49:2001;1-8.
Grafstein B., Forman D.S. Intracellular transport in neurons. Physiol. Rev. 60:1980;1167-1283.
Gurney M.E. Hormonal control of cell form and number in the zebra finch song system. J. Neurosci. 1:1981;658-673.
Hausberger M., Henry L., Richard M.A. Testosterone-induced singing in female European starlings (Sturnus vulgaris). Ethology. 99:1995;193-208.
Hessler N.A., Doupe A.J. Singing-related neural activity in a dorsal forebrain-basal ganglia circuit of adult zebra finches. J. Neurosci. 19:1999;10461-10481.
Jarvis E.D., Scharff C., Grossman M.R., Ramos J.A., Nottebohm F. For whom the bird sings: context-dependent gene expression. Neuron. 21:1998;775-788.
Johnson F., Bottjer S.W. Differential estrogen accumulation among populations of projection neurons in the higher vocal center of male canaries. J. Neurobiol. 26:1995;87-108.
Lin Y.J., Koretsky A.P. Manganese ion enhances T1-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn. Reson. Med. 38:1997;378-388.
Metzdorf R., Gahr M., Fusani L. Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds. J. Comp. Neurol. 407:1999;115-129.
Mooney R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J. Neurosci. 20:2000;5420-5436.
Mooney R., Rosen M.J., Sturdy C.B. A bird's eye view: top down intracellular analyses of auditory selectivity for learned vocalisations. J. Comp. Physiol., A. 188:2002;879-895.
Narita K., Kawasaki F., Kita H. Mn and Mg influxes through Ca channels of motor nerve terminals are prevented by verapamil in frogs. Brain Res. 510:1990;289-295.
Nottebohm F. Testosterone triggers growth of brain vocal control nuclei in adult female canaries. Brain Res. 189:1980;429-436.
Nottebohm F., Stokes T.M., Leonard C.M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165:1976;457-486.
Pautler R.G., Koretsky A.P. Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging. NeuroImage. 16:2002;441-448.
Pautler R.G., Silva A.C., Koretsky A.P. In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging. Magn. Reson. Med. 40:1998;740-748.
Rasika S., Nottebohm F., Alvarez-Buylla A. Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc. Natl. Acad. Sci. 91:1994;7854-7858.
Riters L.V., Baillien M., Eens M., Pinxten R., Foidart A., Ball G.F., Balthazart J. Seasonal variation in androgen-metabolizing enzymes in the diencephalon and telencephalon of the male European starling (Sturnus vulgaris). J. Neuroendocrinol. 13:2001;985-997.
Saldanha C.J., Tuerk M.J., Kim Y.H., Fernandes A.O., Arnold A.P., Schlinger B.A. Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J. Comp. Neurol. 423:2000;619-630.
Saleem K.S., Pauls J.M., Augath M., Trinath T., Prause B.A., Hashikawa T., Logothetis N.K. Magnetic resonance imaging of neuronal connections in the macaque monkey. Neuron. 34:2002;685-700.
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.
Shen P., Schlinger B.A., Campagnoni A.T., Arnold A.P. An atlas of aromatase mRNA expression in the zebra finch brain. J. Comp. Neurol. 360:1995;172-184.
Sloot W.N., Gramsbergen J.B. Axonal transport of manganese and its relevance to selective neurotoxicity in the rat basal ganglia. Brain Res. 657:1994;124-132.
Sohrabji F., Nordeen K.W., Nordeen E.J. Projections of androgen-accumulating neurons in a nucleus controlling avian song. Brain Res. 488:1989;253-259.
Steel R.G.D., Torrie J.H. Principles and Procedures of Statistics. A Biometrical Approach. second ed. 1980;McGraw-Hill Book Company, New York. (633 pp.).
Tindemans I., Verhoye M., Balthazart J., Van der Linden A. In vivo dynamic ME-MRI reveals differential functional responses of RA- and area X-projecting neurones in the HVC of canaries exposed to conspecific song. Eur. J. Neurosci. 18:2003;1-9.
Tramontin A.D., Brenowitz E.A. Seasonal plasticity in the adult brain. Trends Neurosci. 23:2000;251-258.
Vallee R.B., Bloom G.S. Mechanisms of fast and slow axonal transport. Annu. Rev. Neurosci. 14:1991;59-92.
Van der Linden A., Verhoye M., Van Meir V., Tindemans I., Eens M., Absil P., Balthazart J. In vivo manganese-enhanced magnetic resonance imaging reveals connections and functional properties of the songbird vocal control system. Neuroscience. 112:2002;467-474.
Vockel A., Prove E., Balthazart J. Effects of castration and testosterone treatment on the activity of testosterone-metabolizing enzymes in the brain of male and female zebra finches. J. Neurobiol. 21:1990;808-825.
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.