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The serotoninergic system in the brain of the Japanese quail

An immunohistochemical study

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Summary

The presence and topographical localization of the serotoninergic system in the brain of the Japanese quail (Coturnix coturnix japonica) have been studied by means of peroxidase-anti-peroxidase immunocytochemistry. The perimeter, diameter, area, and shape factor of immunoreactive cells have been recorded and analyzed morphometrically for intra- and interspecies comparison. The data reported here confirm and extend results previously obtained in the brain of other avian species. Serotonin-immunoreactive neurons of the quail are mainly located in the hypothalamic paraventricular organ and adjacent areas, and in the brainstem where they form three separate groups. The first of these groups consists of small-sized neurons located in the ventro-rostral mesencephalon. The second group is composed of medium-sized neurons located in the dorsal mesencephalo-pontine region. The third group is also formed by medium-sized neurons, and is located ventrally in the ponto-medullary region. In the quail brain, serotoninergic neurons are not restricted to nuclei located in the vicinity of the midsagittal plane, but show some lateralization, especially in the brainstem. The organization of the different groups of immunoreactive neurons based on this topographical distribution and morphometric analysis has been compared with descriptions of the serotoninergic system in other birds. Serotonin-immunoreactive nerve fibers are widely distributed throughout the brain, but appear to be particularly abundant in regions involved in the control of reproductive activities, such as the septal region, the medial preoptic nucleus, the nucleus intercollicularis, and the external zone of the median eminence. The data reported here have allowed the drawing of a map of serotoninimmunoreactive structure.

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Abbreviations

AVT :

area ventralis of Tsai

BC :

brachium conjunctivum

Cb :

cerebellum

CbI :

nucleus cerebellaris internus

CCV :

commissura cerebellaris ventralis

CNS :

central nervous system

CSF :

cerebrospinal fluid

CTz :

corpus trapezoideum

DIC :

differential interferential contrast

DL :

nucleus dorsolateralis thalami

DM :

nucleus dorsomedialis thalami

FIF :

formaldehyde-induced fluorescence

FLM :

fasciculus longitudinalis medialis

FRM :

formatio reticularis mesencephali

GCt :

substantia grisea centralis

GLv :

nucleus geniculatus ventralis

HB :

habenula

IO :

nucleus isthmo-opticus

IP :

nucleus interpeduncularis

IR :

immunoreactive

LC :

nucleus linearis caudalis

LHy :

nucleus lateralis hypothalami

LHRH :

luteinizing hormone-releasing hormone

LM :

lemniscus medialis

LoC :

locus coeruleus

LS :

lemniscus spinalis

MCC :

nucleus magnocellularis cochlearis

MnV :

nucleus motorius nervi trigemini

MPv :

nucleusmesencephalicus profundus, pars ventralis

N III :

nervus oculomotorius

nIV :

nucleus nervi trochlearis

N VI :

nervus abducens

N VIII :

nervus octavus

nDBC :

nucleus decussationis brachiorum conjunctivorum

nIX :

nucleus nervi glossopharyngei

nVI :

nucleus nervi abducentis

nX :

nucleus nervi vagi

nXII :

nucleus nervi hypoglossi

OI :

nucleus olivaris inferior

OM :

tractus occipito-mesencephalicus

OMd :

nucleus nervi oculomotorii, pars dorsalis

OMv :

nucleus nervi oculomotorii, pars ventralis

Ov :

nucleus ovoidalis

PAP :

peroxidase anti-peroxidase

PGL :

nucleus paragigantocellularis lateralis

PL :

nucleus pontis lateralis

PM :

nucleus pontis medialis

PVO :

paraventricular organ

QF :

tractus quintofrontalis

R :

nuclei raphes

Rgc :

nucleus reticularis, pars gigantocellularis

RP :

nucleus reticularis pontis caudalis

RPaM :

nucleus reticularis paramedianus

Rpc :

nucleus reticularis parvocellularis

RPgc :

nucleus reticularis pontis caudalis, pars gigantocellularis

RPO :

nucleus reticularis pontis oralis

Rt :

nucleus rotundus

Ru :

nucleus ruber

SC :

nucleus subcoeruleus

SG :

substantia gelatinosa Rolandi (trigemini)

ST :

nucleus subtrigeminalis

TPc :

nucleus tegmenti pedunculo-pontinus, pars compacta

Tu :

nucleus tuberis

TV :

nucleus tegmenti ventralis

VeD :

nucleus vestibularis dorsalis

VeL :

nucleus vestibularis lateralis

VeM :

nucleus vestibularis medialis

VeS :

nucleus vestibularis superior

References

  • Balthazart J, Surlemont C (1990) Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail preoptic area. Brain Res Bull 25:7–14

    Google Scholar 

  • Balthazart J, Libioulle JM, Sante P (1988) Stimulatory effects of the noradrenergic neurotoxin DSP4 on sexual behavior in male quail. Behav Proc 17:27–44

    Google Scholar 

  • Balthazart J, Gahr M, Surlemont C (1989) Distribution of estrogen receptors in the brain of the Japanese quail: an immunocytochemical study. Brain Res 501:205–214

    Google Scholar 

  • Baylé J-D, Ramade F, Oliver J (1974) Stereotaxic topography of the brain of the quail (Coturnix coturnix japonica). J Physiol (Paris) 68:219–241

    Google Scholar 

  • Bertler A, Falck B, Gottfries C-J, Ljunggren L, Rosengren E (1964) Some observations on adrenergic connections between the mesencephalon and cerebral hemispheres. Acta Pharmacol Toxicol 21:283–289

    Google Scholar 

  • Bitran D, Hull EM (1987) Pharmacological analysis of male rat sexual behavior. Neurosci Biobehav Rev 11:365–389

    Google Scholar 

  • Bogdaski DF, Bonomi L, Brodie BB (1963) Occurrence of serotonin and catecholamines in brain and peripheral organs of various vertebrate classes. Life Sci 1:80–84

    Google Scholar 

  • Chikazawa H, Fujioka T, Watanabe T (1982) Catecholamine-containing neurons in the mesencephalic tegmentum of the chicken. Light fluorescence and electron microscopic studies. Anat Embryol 164:303–313

    Google Scholar 

  • Chikazawa H, Fujioka T, Watanabe T (1983) Bulbar catecholaminergic neurons projecting to the thoracic spinal cord of the chicken. Evans blue labelling study in combination with catecholamine histofluorescence. Anat Embryol 167:411–423

    Google Scholar 

  • Correale P (1956) The occurrence and distribution of 5-hydroxytryptamine (enteramine) in the central nervous system of vertebrates. J Neurochem 1:22–31

    Google Scholar 

  • Crowley WR, Zemlan FP (1981) The neurochemical control of mating behavior. In: Adler NT (ed) Neuroendocrinology of reproduction. Physiology and behavior. Plenum Press, New York London, pp 451–484

    Google Scholar 

  • Dahlström A, Fuxe K (1964) Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brainstem neurons. Acta Physiol Scand 62: [Suppl 232]:1–55

    Google Scholar 

  • De Lanerolle NC, Youngren OM (1978) Chick vocalization and emotional behavior influenced by apomorphine. J Comp Physiol Psychol 92:416–430

    Google Scholar 

  • Dubé L, Parent A (1981) The monoamine-containing neurons in avian brain. I. A study of the brainstem of the chicken (Gallus domesticus) by means of fluorescence and acctylcholinesterase histochemistry. J Comp Neurol 196:695–708

    Google Scholar 

  • Eden AR, Correia MJ (1981) Vestibular efferent neurons and catecholamine cell groups in the reticular formation of the pigeon. Neurosci Lett 25:239–242

    Google Scholar 

  • Falck B, Hillarp N-Å, Thieme G, Torp Å (1962) Fluorescence of catecholamines and related compounds condensed with formaldehyde. J Histochem Cytochem 10:348–354

    Google Scholar 

  • Fehrer SC, Silsgy JL, El Halawani ME (1985) Serotoninergic influences on pituitary gland and hypothalamic induction of prolactin and luteinizing hormone release in the young turkey (Meleagris gallopavo). Biol Reprod 33:1064–1072

    Google Scholar 

  • Foster RG, Panzica GC, Parry DM, Viglietti-Panzica C (1988) Immunocytochemical studies on the LHRH system of the Japanese quail: influence by photoperiod and aspects of sexual differentiation. Cell Tissue Res 253:327–335

    Google Scholar 

  • Franzoni MF, Viglietti-Panzica C, Ramieri G, Panzica GC (1984) A Golgi study on the neuronal morphology in the hypothalamus of the Japanese quail (Coturnix coturnix japonica). I Tuberal and mammillary regions. Cell Tissue Res 236:357–364

    Google Scholar 

  • Furness JB, Costa M, Blessing WW (1977) Simultaneous fixation and production of catecholamine fluorescence in central nervous tissue by perfusion with aldehydes. Histochem J 9:745–750

    Google Scholar 

  • Fuxe K, Ljunggren L (1965) Cellular localization of monoamines in the upper brain stem of the pigeon. J Comp Neurol 125:355–382

    Google Scholar 

  • Gargiulo G, Nisticò G (1978) Time course of 5,6-dihydroxytryptamine neurotoxic effects on fowl diencephalon and upper brain stem monoaminergic pathways. J Anat 126:261–274

    Google Scholar 

  • Gérard-Ivanoff A (1974) Histogenèse des neurones aminergiques du diencéphale chez le poulet, Gallus gallus. Arch Anat Histol Embryol (Strasb) 57:115–134

    Google Scholar 

  • Gérard A, Gérard H, Grignon G (1979) Innervation sérotoninergique de l'organe paraventriculaire de l'embryon de poulet et du jeune poussin; étude par histofluorescence et par autoradiographie en microscopie optique et électronique. C R Acad Sci [III] 289:355–358

    Google Scholar 

  • Guglielmone R, Panzica GC (1982) Topographic morphologic and developmental characterization of the nuclei loci coerulei in the chicken. A Golgi and fluoresce-histochemical study. Cell Tissue Res 225:95–110

    Google Scholar 

  • Guglielmone R, Panzica GC (1983) Localization of catecholaminecontaining cell bodies in the posterior hypothalamus of chickenes Neurosci Lett Suppl 14:147

    Google Scholar 

  • Guglielmone R, Panzica GC (1984) Typology, distribution and development of the catecholamine-containing neurons in the chicken brain. Cell Tissue Res 237:67–79

    Google Scholar 

  • Guglielmone R, Panzica GC (1985) Early appearance of catecholaminergic neurons in the central nervous system of precocial and altricial avian species. A fluorescence-hístochemical study. Cell Tissue Res 240:381–384

    Google Scholar 

  • Hartwig H-G (1975) Neurobiologische Studien an photoneuroendokrinen Systemen. Thesis, Faculty of Medicine, University of Giessen

  • Ho RH, LaValley AL (1984) 5-Hydroxytryptamine in the spinal cord of the domestic fowl. Brain Res Bull 13:427–431

    Google Scholar 

  • Ikeda H, Gotoh J (1971) Distribution of monoamine-containing cells in the central nervous system of the chicken. Jpn J Pharmacol 21:763–784

    Google Scholar 

  • Karten HJ, Hodos W (1967) A stereotaxic atlas of the brain of the pigeon (Columba livia). John Hopkins University Press, Baltimore

    Google Scholar 

  • Katz DM, Karten HJ (1979) The discrete anatomical localization of vagal aortic afferents within a catecholamine-containing cell group in the nucleus solitarius. Brain Res 171:187–195

    Google Scholar 

  • Kiss JZ, Péczely P (1987) Distribution of tyrosine-hydroxylase (TH)-immunoreactive neurons in the diencephalon of the pigeon (Columba domestica livia). J Comp Neurol 257:333–346

    Google Scholar 

  • Kuenzel WJ, Masson M (1988) A stereotaxic atlas of the brain of the chick (Gallus domesticus). Johns Hopkins University Press, Baltimore London, pp 1–165

    Google Scholar 

  • Lewis JW, Ryan SM, Arnold AP, Butcher LL (1981) Evidence for a catecholaminergic projection to area X in the zebra finch. J Comp Neurol 196:347–354

    Google Scholar 

  • Martinez-Vargas MC, Stumpf WE, Sar M (1976) Anatomical distribution of estrogen target cells in the avian CNS: a comparison with the mammalian CNS. J. Comp Neurol 167:83–104

    Google Scholar 

  • Muhibullah M, Gargiulo G, Nisticò G, Stephenson JD (1983) Distribution of monoamine-containing neurons in the fowl brain (Gallus domesticus). In: Nisticò G, Bolis L (eds) Progress in nonmammalian brain research, vol 1. CRC Press, Boca Raton, Fla, USA, pp 81–112

    Google Scholar 

  • Ottinger MA (1983) Sexual behaviour and endocrine changes during reproductive maturation and ageing in the avian male. In: Balthazart J, Pröve E, Gilles R (eds) Hormones and behaviour in higher vertebrates. Springer, Berlin Heidelberg New York, pp 350–367

    Google Scholar 

  • Ottinger MA, Balthazart J (1987) Brain monoamines and sexual behavior in Japanese quail: effects of castration and steroid replacement therapy. Behav Proc 14:197–216

    Google Scholar 

  • Ottinger MA, Schumacher M, Clarke RN, Duchala CS, Turek R, Balthazart J (1986) Comparison of monoamine concentrations in the brains of adult male and female Japanese quail. Poultry Sci 65:1413–1420

    Google Scholar 

  • Panzica GC, Korf H-W, Ramieri G, Viglietti-Panzica C (1986) Golgi-type and immunocytochemical studies on the intrinsic organization of the periventricular layer of the avian paraventricular nucleus. Cell Tissue Res 243:317–322

    Google Scholar 

  • Panzica GC, Viglietti-Panzica C, Calcagni M, Anselmetti GC, Schumacher M, Balthazart J (1987a) Sexual differentiation and hormonal control of the sexually dimorphic medial preoptic nucleus in quail. Brain Res 416:59–68

    Google Scholar 

  • Panzica GC, Viglietti-Panzica C, Fiori MG, Calcagni M, Anselmetti GC, Balthazart J (1987b) Cytoarchitectural analysis of the quail preoptic area. Evidence for a sex-related dimorphism in the medial preoptic nucleus. Boll Zool 54:13817

    Google Scholar 

  • Panzica GC, Bellesia L, Boccaccio C, Balossino N (1989) Development of software for morphometrical analysis on low-cost personal computers. In: Fasolo A, Panzica GC, Calzà L, Giardino L (eds) Image analysis in neurohistology. CSI Piemonte, Torino, pp 87–97

    Google Scholar 

  • Panzica GC, Guglielmone R, Cozzi B, Aste N, Viglietti-Panzica C (1990) Distribution of catecholamines and serotonin in the brain of the Japanese quail. A histochemical and immunohistochemical study (abstracts). 15th Conf Europ Comp Endocrinol, Leuven, p 100

  • Potash LM (1970) Vocalizations elicited by electrical brain stimulation in Coturnix coturnix japonica. Behaviour 36:149–167

    Google Scholar 

  • Rabii J, Buonomo F, Scanes CG (1980) Studies on the hypothalamic regulation of luteinizing hormone secretion in the domestic fowl. Adv Physiol Sci 33:25–34

    Google Scholar 

  • Reiner A, Karten HJ, Solina AR (1983) Substance P: localization within paleostriatal-tegmental pathways in the pigeon. Neuroscience 9:61–85

    Google Scholar 

  • Sako H, Kojima T, Okado N (1986a) Immunohistochemical study on the development of serotoninergic neurones in the chick. I. Distribution of cell bodies and fibers in the brain. J Comp Neurol 253:61–78

    Google Scholar 

  • Sako H, Kojima T, Okado N (1986a) Immunohistochemical study on the development of serotoninergic neurones in the chick: I. Distribution of cell bodies and fibers in the spinal cord. J Comp Neurol 253:79–91

    Google Scholar 

  • Sano Y, Ueda S, Yamada H, Takeuchi Y, Goto M, Kawata M (1983) Immunohistochemical demonstration of serotonin-containìng CSF-contacting neurons in the submammalian paraventricular organ. Histochemistry 77:423–430

    Google Scholar 

  • Schrold J (1972) Behavioral effects of d-amphetamine alone and in combination with antidepressants, antihistimines or other psychotropic drugs in young chicks. Psychopharmacologia 23:115–124

    Google Scholar 

  • Sharp PJ, Follett BK (1968) The distribution of monoamines in the hypothalamus of the Japanese quail, Coturnix coturnix japonica. Z Zellforsch 90:245–262

    Google Scholar 

  • Sharp PJ, MacNamee MC, Talbot RT, Sterling RJ, Hall TR (1984) Aspects of the neuroendocrine control of ovulation and broodiness in the domestic hen. J Exp Zool 232:475–483

    Google Scholar 

  • Sharp PJ, Sterling RJ, Talbot RT, Huskisson NS (1989a) The role of hypothalamic vasoactive intestinal polypeptide in the maintenance of prolactin secretion in incubating bantam hens: using passive immunization, radioimmunoassay and immunohistochemistry. J Endocrinol 122:5–13

    Google Scholar 

  • Sharp PJ, Talbot RT, Macnamee MC (1989b) Evidence for the involvement of dopamine and 5-hydroxytryptamine in the regulation of preovulatory release of luteinizing hormone in the domestic hen. Gen Comp Endocrinol 76:205–213

    Google Scholar 

  • Shiosaka S, Takatsuki K, Inagaki S, Sakanaka M, Takagi H, Senba E, Matsuzaki T, Tohyama M (1981) Topographic atlas of somatostatin-containing neuron system in the avian brain in relation to catecholamine-containing neuron system. II. Mesencephalon, rhombencephalon and spinal cord. J Comp Neurol 202:115–124

    Google Scholar 

  • Silver R, Witkovsky P, Horvath P, Alones V, Barnstable CJ, Lehman MN (1988) Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contact neurons of the avian brain. Cell Tissue Res 253:189–198

    Google Scholar 

  • Simerly RB, Swanson LW, Gorski RA (1984) Demonstration of a sexual dimorphism in the distribution of serotonin-immunoreactive fibers in the medial preoptic nucleus of the rat. J Comp Neurol 225:151–166

    Google Scholar 

  • Takatsuki K, Shiosaka S, Inagaki S, Sakanaka M, Takagi H, Senba E, Matsuzaki T, Tohyama M (1981) Topographic atlas of somatostatin-containing neuron system in the avian brain in relation to catecholamine-containing neuron system. I. Telencephalon and diencephalon. J Comp Neurol 202:103–113

    Google Scholar 

  • Tohyama M, Maeda T, Hashimoto J, Shresta GR, Tamura O, Shimizu N (1974) Comparative anatomy of the locus coeruleus. I. Organization and ascending projections of the catecholamine containing neurons in the pontine region of the bird, Melopsittacus undulatus. J Hirnforsch 15:319–330

    Google Scholar 

  • VanderMaelen CP (1985) Serotonin. In: Rogawski MA, Barker JL (eds) Neurotransmitter actions. Plenum Press, New York, pp 201–240

    Google Scholar 

  • Vigh B, Tar E, Teichmann I (1968) The development of the paraventricular organ in the white leghorn chicken. Acta Biol Acad Sci Hung 19:215–225

    Google Scholar 

  • Viglietti-Panzica C, Panzica GC, Fiori MG, Calcagni M, Anselmetti GC, Balthazart J (1986) A sexually dimorphic nucleus in the quail preoptic area. Neurosci Lett 64:129–134

    Google Scholar 

  • Wallace JA (1982) Monoamines in the early chick embryo: demonstration of serotonin synthesis and regional distribution of serotonin-concentrating cells during morphogenesis. Am J Anat 165:261–276

    Google Scholar 

  • Wallace JA (1985) An immunocytochemical study of the development of central serotoninergic neurons in the chick embryo. J Comp Neurol 236:443–453

    Google Scholar 

  • Wallace JA, Allgold PC, Hoffman TJ, Mondragon RM, Maez RR (1986) Analysis of the change in number of serotoninergic neurons in the chick spinal cord during embryonic development. Brain Res Bull 17:297–305

    Google Scholar 

  • Warren Soest S, Farner DS, Oksche A (1973) Fluorescence microscopy of neurons containing primary catecholamines in the ventral hypothalamus of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Z Zellforsch 141:1–17

    Google Scholar 

  • Watson JT, Adkins-Reagan E (1989) Neuroanatomical localization of sex steroid concentrating cells in the Japanese quail (Coturnix japonica): autoradiography with [3H]-testosterone, [3H]-estradiol, and [3H]-dihydrotestosterone. Neuroendocrinology 49:51–64

    Google Scholar 

  • Yamada H, Sano Y (1985) Immunohistochemical studies on the serotonin neuron system in the brain of the chicken (Gallus domesticus). II. The distribution of the nerve fibers. Biogenic Amines 2:21–36

    Google Scholar 

  • Yamada H, Takeuchi Y, Sano Y (1984) Immunohistochemical studies on the serotonin neuron system in the brain of the chicken (Gallus domesticus). I. Distribution of the neuronal somata. Biogenic Amines 1:83–94

    Google Scholar 

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Cozzi, B., Viglietti-Panzica, C., Aste, N. et al. The serotoninergic system in the brain of the Japanese quail. Cell Tissue Res 263, 271–284 (1991). https://doi.org/10.1007/BF00318769

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