Skip to main content
SpringerLink
Log in

Nucleus accumbens subregions: hodological and immunohistochemical study in the domestic chick (Gallus domesticus)

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The nucleus accumbens was identified in avian species some time ago. However, the precise localization and extent of this nucleus is still a matter of controversy. We have used immunolabeling against calbindin, neuropeptide Y, and DARPP-32 (dopamine- and adenosine-related phosphoprotein, 32 kDa) for the selective marking of putative accumbens subdivisions and have followed the anterograde transport of biotinylated dextran amine injected to the nucleus tractus solitarii region of 7-day-old domestic chicks. The nucleus accumbens extending between rostrocaudal atlas coordinates A 10.6 and A 8.8 can be subdivided into the core and shell, the core corresponding to the ventromedial and juxtaventricular medial striatum laterodorsal to the bed nucleus of stria terminalis, and the shell representing an arched region situated ventrally and ventrolaterally to the core. Immunoreactivity to both calbindin and neuropeptide Y is more intense in the shell than in the core division. DARPP-32 immunolabeling does not differ in the two divisions but is markedly weaker in the bed nucleus of stria terminalis, enabling the separation of this nucleus from the surrounding accumbens subdivisions. Fibers from the nucleus solitarius predominantly terminate in the shell division, similar to the situation described in mammals. Whereas the suggested core lies entirely within the boundary of the medial striatum, the shell seems partially to overlap the ventral pallidum. We have been unable to subdivide the remaining part of accumbens lying rostral to A 10.6 into a putative shell and core by the methods employed in the present study. This region probably corresponds to the rostral pole of the nucleus accumbens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Acerbo MJ, Gargiulo PA, Krug I, Delius JD (2002) Behavioural consequences of nucleus accumbens dopaminergic stimulation and glutamatergic blocking in pigeons. Behav Brain Res 136:171–177

    Article  PubMed  CAS  Google Scholar 

  • Aoki N, Suzuki R, Izawa E, Csillag A, Matsushima T (2006) Localized lesions of ventral striatum, but not arcopallium, enhanced impulsiveness in choices based on anticipated spatial proximity of food rewards in domestic chicks. Behav Brain Res 168:1–12

    Article  PubMed  Google Scholar 

  • Arends JJ, Wild JM, Zeigler HP (1988) Projections of the nucleus of the tractus solitarius in the pigeon (Columba livia). J Comp Neurol 278:405–429

    Article  PubMed  CAS  Google Scholar 

  • Atoji Y, Wild JM (2004) Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions. J Comp Neurol 475:426–461

    Article  PubMed  CAS  Google Scholar 

  • Atoji Y, Wild JM, Yamamoto Y, Suzuki Y (2002) Intratelencephalic connections of the hippocampus in pigeons (Columba livia). J Comp Neurol 447:177–199

    Article  PubMed  Google Scholar 

  • Bailhache T, Balthazart J (1993) The catecholaminergic system of the quail brain: immunocytochemical studies of dopamine-b-hydroxylase and tyrosine hydroxylase. J Comp Neurol 329:230–256

    Article  PubMed  CAS  Google Scholar 

  • Brauer K, Häusser M, Härtig W, Arendt T (2000) The core-shell dichotomy of nucleus accumbens in the rhesus monkey as revealed by double-immunfluorescense and morphology of cholinergic interneuron. Brain Res 858:151–162

    Article  PubMed  CAS  Google Scholar 

  • Carrillo GD, Doupe AJ (2004) Is the songbird area X: striatal, pallidal, or both? An anatomical study. J Comp Neurol 473:415–437

    Article  PubMed  Google Scholar 

  • Cardinal RN, Pennicott DR, Sugathapala CL, Robbins TW, Everitt BJ (2001) Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 292:2499–2501

    Article  PubMed  CAS  Google Scholar 

  • Csiffáry A, Görcs T, Palkovits M (1990) Neuropeptide Y innervation of ACTH immunorective neurons in the arcuate nucleus of rats: a correlated light and electron microscopic double immunolabelling study. Brain Res 506:215–222

    Article  PubMed  Google Scholar 

  • Da Silva A, Marino-Neto J, Paschoalini MA (2003) Feeding induced by microinjections of NMDA and AMPA-kainate receptor antagonists into ventral striatal and ventral pallidal areas of the pigeon. Brain Res 966:76–83

    Article  PubMed  CAS  Google Scholar 

  • Davies DC, Csillag A, Székely AD, Kabai P (1997) Efferent connections of the domestic chick archistriatum: phaseolus lectin anterograde tracing study. J Comp Neurol 389:679–693

    Article  PubMed  CAS  Google Scholar 

  • Delfs JM, Zhu Y, Druhan JP, Aston-Jones GS (1998) Origin of noradrenergic afferents to the shell subregion of the nucleus accumbens: anterograde and retrograde tract-tracing studies in the rat. Brain Res 806:127–140

    Article  PubMed  CAS  Google Scholar 

  • Dubbeldam JL, De Boer-Visser AM, Bout RG (1997) Organization and efferent connections of the archistriatum of the mallard, Anas platyrhynchos L.: an anterograde and retrograde tracing study. J Comp Neurol 388:632–657

    Article  PubMed  CAS  Google Scholar 

  • Durstewitz D, Kröner S, Hemmings HC Jr, Güntürkün O (1998) The dopaminergic innervation of the pigeon telencephalon: distribution of DARPP-32 and co-occurrence with glutamate decarboxylase and tyrosine hydroxylase. Neuroscience 83:763–779

    Article  PubMed  CAS  Google Scholar 

  • Farries MA, Perkel DJ (2002) A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus. J Neurosci 22:3776–3787

    PubMed  CAS  Google Scholar 

  • Farries MA, Ding L, Perkel DJ (2005) Evidence for “direct” and “indirect” pathways through the song system basal ganglia. J Comp Neurol 484:93–104

    Article  PubMed  Google Scholar 

  • Gaspar P, Berger B, Alvarez C, Vigny A, Henry JP (1985) Catecholaminergic innervation of the septal area in man: immunocytochemical study using TH and DBH antibodies. J Comp Neurol 241:12–33

    Article  PubMed  CAS  Google Scholar 

  • Groenewegen HJ, Uylings HBM (2000) The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog Brain Res 126:3–28

    Article  PubMed  CAS  Google Scholar 

  • Guirado S, Davila JC, Real MA, Medina L (1999) Nucleus accumbens in the lizard Psammodromus algirus: chemoarchitecture and cortical afferent connections. J Comp Neurol 405:15–31

    Article  PubMed  CAS  Google Scholar 

  • Heimer L (2003) A new anatomical framework for neuropsychiatric disorders and drug abuse. Am J Psychiatry 160:1726–1739

    Article  PubMed  Google Scholar 

  • Heimer L, Alheid GF, Olmos JS de, Groenenwegen HJ, Haber SN, Harlan RE, Zahm DS (1997) The accumbens: beyond the core-shell dichotomy. J Neuropsychiatry Clin Neurosci 9:354–381

    PubMed  CAS  Google Scholar 

  • Hemmings HC Jr, Walaas SI, Ouimet CC, Greengard P (1987) Dopaminergic regulation of protein phosphorylation in the striatum: DARPP-32. Trends Neurosci 10:377–383

    Article  CAS  Google Scholar 

  • Izawa EI, Zachar G, Yanagihara S, Matsushima T (2003) Localized lesion of caudal part of lobus parolfactorius caused impulsive choice in the domestic chick: evolutionarily conserved function of ventral striatum. J Neurosci 23:1894–1902

    PubMed  CAS  Google Scholar 

  • Izawa E, Aoki N, Matsushima T (2005) Neural correlates of the proximity and quantity of anticipated food rewards in the ventral striatum of domestic chicks. Eur J Neurosci 22:1502–1512

    Article  PubMed  Google Scholar 

  • Jongen-Rêlo A, Voorn P, Groenewegen HJ (1994) Immunohistochemical characterization of the shell and core territories of the nucleus accumbens in the rat. Eur J Neurosci 6:1255–1264

    Article  PubMed  Google Scholar 

  • Kelley AE (1999) Neural integrative activities of nucleus accumbens subregions in relation to learning and motivation. Psychobiology 27:198–213

    Google Scholar 

  • Kelley AE, Swanson CJ (1997) Feeding induced by blockade of AMPA and kainate receptors within the ventral striatum: a microinfusion mapping study. Behav Brain Res 89:107–113

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Lindwall O, Stenevi U (1978) Dopamine and noradrenaline neurons projecting to the septal area in the rat. Cell Tissue Res 190:383–407

    Google Scholar 

  • Medina L, Reiner A (1997) The efferent projections of the dorsal and ventral pallidal parts of the pigeon basal ganglia studied with biotinylated dextran amine. Neuroscience 81:773–802

    Article  PubMed  CAS  Google Scholar 

  • Meredith GE, Pattiselanno A, Groenewegen HJ, Haber SN (1996) Shell and core in monkey and human nucleus accumbens identified with antibodies to calbindin-D28k. J Comp Neurol 365:628–639

    Article  PubMed  CAS  Google Scholar 

  • Mezey S, Csillag A (2002) Selective striatal connections of midbrain dopaminergic nuclei in the chick (Gallus domesticus). Cell Tissue Res 308:35–46

    Article  PubMed  CAS  Google Scholar 

  • Mogenson GJ, Jones DL, Yim CY (1980) From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14:69–97

    Article  PubMed  CAS  Google Scholar 

  • Moons L, D’Hondt E, Pijcke K, Vandesande F (1995) Noradrenergic system in the chicken brain: immunocytochemical study with antibodies to noradrenaline and dopamine-β-hydroxylase. J Comp Neurol 360:331–348

    Article  PubMed  CAS  Google Scholar 

  • Nauta WJH, Domesick WB (1976) Crossroads of limbic and striatal circuity: hypothalamo-nigral connections. In: Livingston KE, Hornykiewicz O (eds) The limbic system: functional organization and clinical disorders. Raven, New York, pp 75–93

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Reiner A, Medina L, Veenman CL (1998a) Structural and functional evolution of the basal ganglia in vertebrates. Brain Res Rev 28:235–285

    Article  PubMed  CAS  Google Scholar 

  • Reiner A, Perera M, Paullus R, Medina L (1998b) Immunohistochemical localization of DARPP32 in striatal projection neurons and striatal interneurons in pigeons. J Chem Neuroanat 16:17–33

    Article  PubMed  CAS  Google Scholar 

  • Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Gütürkün O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414

    Article  PubMed  Google Scholar 

  • Roberts TF, Hall WS, Brauth SE (2002) Organization of the avian basal forebrain: chemical anatomy in the parrot (Melopsittacus undulatus). J Comp Neurol 454:383–408

    Article  PubMed  Google Scholar 

  • Székely AD, Krebs JR (1996) Efferent connectivity of the hippocampal formation of the zebra finch (Taeniopygia guttata): an anterograde pathway tracing study using Phaseolus vulgaris leucoagglutinin. J Comp Neurol 368:198–214

    Article  PubMed  Google Scholar 

  • Swanson LW, Hartman BK (1975) The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J Comp Neurol 163:467–505

    Article  PubMed  CAS  Google Scholar 

  • Veenman CL, Wild JM, Reiner A (1995) Organization of the avian “corticostriatal” projection system: a retrograde and anterograde pathway tracing study in pigeons. J Comp Neurol 354:87–126

    Article  PubMed  CAS  Google Scholar 

  • Yanagihara S, Izawa E, Koga K, Matsushima T (2001) Reward-related neuronal activities in basal ganglia of domestic chicks. Neuroreport 12:1431–1435

    Article  PubMed  CAS  Google Scholar 

  • Záborszky L, Alheid GF, Beinfeld MC, Eiden LE, Heimer L, Palkovits M (1985) Cholecystokinin innervation of the ventral striatum: a morphological and radioimmunological study. Neuroscience 14:427–453

    Article  PubMed  Google Scholar 

  • Zahm DS, Brog JS (1992) On the significance of subterritories in the “accumbens” part of the rat ventral striatum. Neuroscience 50:751–767

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Semmelweis University, 58 Tuzolto utca, H-1450, Budapest, Hungary

    Eszter Bálint & András Csillag

Authors
  1. Eszter Bálint
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. András Csillag
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to András Csillag.

Additional information

This work was supported by Hungarian Research Fund OTKA T-043462 and Semmelweis University School of PhD Studies.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bálint, E., Csillag, A. Nucleus accumbens subregions: hodological and immunohistochemical study in the domestic chick (Gallus domesticus). Cell Tissue Res 327, 221–230 (2007). https://doi.org/10.1007/s00441-006-0295-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-006-0295-0

Keywords

Search

Navigation