Identification of the Origin of Catecholaminergic Inputs to Hvc in Canaries by Retrograde Tract Tracing Combined with Tyrosine Hydroxylase Immunocytochemistry
[en] The telencephalic nucleus HVc (sometimes referred to as the high vocal center) plays a key role in the production and perception of birdsong. Although many afferent and efferent connections to this nucleus have been described, it has been clear for many years, based on chemical neuroanatomical criteria, that there are projections to this nucleus that remain undescribed. A variety of methods including high performance liquid chromatography, immunohistochemistry and receptor autoradiography have identified high levels of catecholamine transmitters, the presence of enzymes involved in the synthesis of catecholamines such as tyrosine hydroxylase and a variety of catecholamine receptor sub-types in the HVc of several songbird species. However, no definitive projections to HVc have been described from cells groups known to synthesize catecholamines. These projections were analyzed in the present study by retrograde tract tracing combined with immunocytochemistry for tyrosine hydroxylase. The origin of the catecholaminergic inputs to HVc were determined based exclusively on birds in which injections of the retrograde tracer (latex fluospheres) were confined within the cytoarchitectonic boundaries of the nucleus. Retrogradely transported latex fluospheres were found mainly in cells of two dopaminergic nuclei, the mesencephalic central gray (A11) and, to a lesser extend, the area ventralis of Tsai (A10; homologous to the ventral tegmental area of mammals). A few retrogradely-labelled cells were also found in the noradrenergic nucleus subceruleus (A6). Most of these retrogradely-labelled cells were also tyrosine hydroxylase-positive. Other catecholaminergic nuclei were devoid of retrograde label. These data converge with others studies to indicate that HVc receives discrete dopaminergic and noradrenergic inputs. These inputs may influence the steroid regulation of HVc, attentional processes related to song and modulate sensory inputs to the song system.
Disciplines :
Neurosciences & behavior
Author, co-author :
Appeltants, D.
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
Ball, G. F.
Language :
English
Title :
Identification of the Origin of Catecholaminergic Inputs to Hvc in Canaries by Retrograde Tract Tracing Combined with Tyrosine Hydroxylase Immunocytochemistry
Bailhache T., Balthazart J. The catecholaminergic system of the quail brain: immunocytochemical studies of dopamine β-hydroxylase and tyrosine hydroxylase. J. Comp. Neurol. 329:1993;230-256.
Ball G.F. Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars. Brain Behav. Evol. 44:1994;234-246.
Ball G.F. Neuroendocrine basis of seasonal changes in vocal behavior among songbirds. Hauser M., Konishi M. Neural Mechanisms of Communication. 1999;MIT Press, Cambridge, MA.
Balthazart J., Absil P. Identification of catecholaminergic inputs to and outputs from aromatase-containing brain areas of the Japanese quail by tract tracing combined with tyrosine hydroxylase immunocytochemistry. J. Comp. Neurol. 382:1997;401-428.
Balthazart J., Ball G.F. Identification of catecholaminergic cell groups in the brainstem of the canary, zebra finch, white-throated sparrow and budgerigar by tyrosine hydroxylase immunocytochemistry. Belg. J. Zool. 126:1996;65-78.
Barclay S.R., Harding C.F. Androstenedione modulation of monoamine levels and turnover in hypothalamic and vocal control nuclei in the male zebra finch: steroid effects on brain monoamines. Brain Res. 459:1988;333-343.
Barclay S.R., Harding C.F. Differential modulation of monoamine levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches. Brain Res. 523:1990;251-262.
Barclay S.R., Harding C.F., Waterman S.A. Correlations between catecholamine levels and sexual behavior in male zebra finches. Pharmacol. Biochem. Behav. 41:1992;195-201.
Barclay S.R., Harding C.F., Waterman S.A. Central DSP-4 treatment decreases norepinephrine levels and courtship behavior in male zebra finches. Pharmacol. Biochem. Behav. 53:1996;213-220.
Bernard D.J., Ball G.F. Two histological markers reveal a similar photoperiodic difference in the volume of the high vocal center in male European starlings. J. Comp. Neurol. 360:1995;726-734.
Bernard D.J., Ball G.F. Photoperiodic condition modulates the effects of testosterone on song control nuclei volumes in male European starlings. Gen. Comp. Endocrinol. 105:1997;276-283.
Blaustein J.D., Tetel M.J., Meredith J.M. Neurobiological regulation of hormonal response by progestin and estrogen receptors. Micevych P.E., Hammer R.P. Jr Neurobiological Effects of Sex Steroid Hormones. 1995;324-349 Cambridge University Press, Cambridge.
Bottjer S.W. The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. J. Neurobiol. 24:1993;51-69.
Bottjer S.W., Johnson F. Circuits, hormones, and learning: vocal behavior in songbirds. J. Neurobiol. 33:1997;602-618.
Brenowitz E.A. Evolution of the vocal control system in the avian brain. Semin. Neurosci. 3:1991;399-407.
Brenowitz E.A. Comparative approaches to the avian song system. J. Neurobiol. 33:1997;517-531.
Brenowitz E.A., Margoliash D., Nordeen K.W. An introduction to birdsong and the avian song system. J. Neurobiol. 33:1997;495-500.
Burd G.D., Paton H., Hemmings H., Heintz J., Nottebohm F. Dopamine innervation of newly-generated neurons in the forebrain of adult canaries. J. Histochem. Cytochem. 34:1986;109.
Cabot J.B., Reiner A., Bogan N. Avian bulbo-spinal pathways: anterograde and retrograde studies of cells of origin, funicular trajectories and laminar terminations. Kuypers H.G.J.M., Martin G.F. Progress in Brain Research. 1982;79-108 Elsevier, Amsterdam.
Casto J.M., Ball G.F. Characterization and localization of D1 dopamine receptors in the sexually dimorphic vocal control nucleus, area X, and the basal ganglia of European starlings. J. Neurobiol. 25:1994;767-780.
Casto J.M., Ball G.F. Early administration of 17β-estradiol partially masculinizes song control regions and a2-adrenergic receptor distribution in European starlings (Sturnus vulgaris). Horm. Behav. 30:1996;387-406.
Dave A.S., Yu A.C., Margoliash D. Behavioral state modulation of auditory activity in a vocal motor system. Science. 282:1998;2250-2254.
Divac I., Mogensen J. The prefrontal 'cortex' in the pigeon catecholamine histofluorescence. Neuroscience. 15:1985;677-682.
Doupe A., Solis M.M. Song- and order-selective neurons develop in the songbird anterior forebrain pathway during vocal learning. J. Neurobiol. 33:1997;694-709.
Etgen A.M., Vathy I., Petitti N., Ungar S., Karkanias G.B. Ovarian steroids, female reproductive behavior and norepinephrine neurotransmission in the hypothalamus. Balthazart J. Hormones, Brain and Behaviour in Vertebrates. 2. Behavioural Activation in Males and Females - Social Interactions and Reproductive Physiology. Compartaive Physiology. 9s:1990;116-128 Karger, Basel.
Etgen A.M., Ungar S., Petitti N. Estradiol and progesterone modulation of norepinephrine neurotransmission: implications for the regulation of female reproductive behavior. J. Neuroendocrinol. 4:1992;255-271.
Fallon J.H. Collateralization of monoamine neurons: mesotelencephalic dopamine projections to caudate, septum, and frontal cortex. J. Neurosci. 1:1981;1361-1368.
Hessler N.A., Doupe A.J. Social context modulates singing-related neural activity in the songbird forebrain. Nat. Neurosci. 2:1999;209-211.
Jarvis E.D., Nottebohm F. Motor-driven gene expression. Proc. Natl. Acad. Sci. USA. 94:1997;4097-4102.
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;87-105.
Kimpo R.R., Doupe A.J. FOS is induced by singing in distinct neuronal populations in a motor network. Neuron. 18:1997;315-325.
Kitt C.A., Brauth S.E. Telencephalic projections from midbrain and isthmal cell groups in the pigeon. II. The nigral complex. J. Comp. Neurol. 247:1986;92-110.
Kroodsma D., Konishi M. A suboscine bird (Eastern phoebe, Sayornis phoebe) develops normal song without auditory feedback. Anim. Behav. 42:1991;477-487.
Lewis J.W., Ryan S.M., Arnold A.P., Butcher L.L. Evidence for catecholamine projection to area X in the zebra finch. J. Comp. Neurol. 196:1981;347-354.
Maney D.L., Bernard D.J., Turek F.W., Ball G.F. Localization of androgen receptor and estrogen receptor alpha mRNA in catecholaminergic cell groups of the canary brain. Soc. Neurosci. Abstr. 25:1999;866.
Margoliash D. Functional organization of forebrain pathways for song production and perception. J. Neurobiol. 33:1997;671-693.
Mello C.V., Pinaud R., Ribeiro S. Noradrenergic system of the zebra finch brain: Immunocytochemical study of dopamine-β-hydroxylase. J. Comp. Neurol. 400:1998;207-228.
McGaugh J.L. Peripheral and central adrenergic influences on brain systems involved in the modulation of memory storage. Ann. N.Y. Acad. Sci. 444:1985;150-161.
Nicholls T.J., Golsmith A.R., Dawson A. Photorefractoriness in birds and comparison with mammals. Physiol. Rev. 68:1988;133-176.
Nock B., Feder H.H. Neurotransmitter modulation of steroid action in target cells that mediate reproduction and reproductive behavior. Neurosci. Biobehav. Rev. 5:1981;437-447.
Nottebohm F. Brain pathways for vocal learning in birds: a review of the first 10 years. Sprague J.M., Epstein A.N. Progress in Psychobiology and Physiological Psychology. 9:1980;85-214 Academic Press, New York.
Nottebohm F. A brain for all seasons: cyclical anatomical changes in song-control nuclei of the canary brain. Science. 214:1981;1368-1370.
Nottebohm F. The search for neural mechanisms that define the sensitive period for song learning in birds. Neth. J. Zool. 43:1993;193-234.
Nottebohm F., Stokes T.M., Leonard C.M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165:1976;457-486.
Nottebohm F., Kelley D.B., Paton J.A. Connections of vocal control nuclei in the canary telencephalon. J. Comp. Neurol. 207:1982;344-357.
Pasqualini C., Olivier V., Guibert B., Frain O., Leviel V. Acute stimulatory effect of estradiol on striatal dopamine synthesis. J. Neurochem. 65:1995;1651-1657.
Reiner A., Karle E.J., Anderson K.D., Medina L. Catecholaminergic perikarya and fibers in the avian nervous system. Smeets W.J.A.J., Reiner A. Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates. 1994;135-181 Cambridge University Press, Cambridge.
Sakaguchi H., Saito N. The acetylcholine and catecholamine contents in song control nuclei of zebra finch during song ontogeny. Dev. Brain Res. 47:1989;313-317.
Salamone J.D. Complex motor and sensori-motor functions of striatal and accumbens dopamine: involvement in instrumental behavior processes. Psychopharmacology. 107:1992;160-174.
Schlinger B.A. Sex steroids and their actions on the birdsong system. J. Neurobiol. 33:1997;619-631.
Simpson H.B., Vicario D.S. Brain pathways for learned and unlearned vocalizations differ in zebra finches. J. Neurosci. 10:1990;1541-1556.
Skagerberg G., Lindvall O. Organization of diencephalic dopamine neurons projecting to the spinal cord in the rat. Brain Res. 342:1985;340-351.
Smeets W.J.A.J., Reiner A. Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates. 1994;Cambridge University Press, Cambridge.
Soha J.A., Shimizu T., Doupe A.J. Development of the catecholaminergic innervation of the song system of the male zebra finch. J. Neurobiol. 29:1996;473-489.
Stokes T.M., Leonard C.M., Nottebohm F. The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J. Comp. Neurol. 156:1974;337-374.
Storey C.R., Nicholls T.J. Some effects of manipulation of daily photoperiod on the rate of onset of a photorefractory state in canaries (Serinus canarius). Gen. Comp. Endocrinol. 30:1976;204-208.
Takada M. The A11 catecholamine cell group: another origin of the dopaminergic innervation of the amygdala. Neurosci. Lett. 118:1990;271-285.
Takada M., Li Z.K., Hattori T. Single thalamic dopaminergic neurons project to both the neocortex and spinal cord. Brain Res. 455:1988;346-352.
Waldmann C., Güntürkün O. The dopaminergic innervation of the pigeon caudolateral forebrain: immunocytochemical evidence for a 'prefrontal cortex' in birds? Brain Res. 600:1993;225-234.
Yu A.C., Margolisah D. Temporal hierarchical control of singing in birds. Science. 273:1996;1871-1875.