Skip to main content
Log in

A three-dimensional digital atlas of the starling brain

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Because of their sophisticated vocal behaviour, their social nature, their high plasticity and their robustness, starlings have become an important model species that is widely used in studies of neuroethology of song production and perception. Since magnetic resonance imaging (MRI) represents an increasingly relevant tool for comparative neuroscience, a 3D MRI-based atlas of the starling brain becomes essential. Using multiple imaging protocols we delineated several sensory systems as well as the song control system. This starling brain atlas can easily be used to determine the stereotactic location of identified neural structures at any angle of the head. Additionally, the atlas is useful to find the optimal angle of sectioning for slice experiments, stereotactic injections and electrophysiological recordings. The starling brain atlas is freely available for the scientific community.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Absil P, Pinxten R, Balthazart J, Eens M (2003) Effect of age and testosterone on autumnal neurogenesis in male European starlings (Sturnus vulgaris). Behav Brain Res 143:15–30. doi:10.1016/s0166-4328(03)00006-8

    Article  CAS  PubMed  Google Scholar 

  • Adret-Hausberger M (1982) Social influences on the whistled songs of starlings. Behav Ecol Sociobiol 11:241–246

    Article  Google Scholar 

  • Alger SJ, Riters LV (2006) Lesions to the medial preoptic nucleus differentially affect singing and nest box-directed behaviors within and outside of the breeding season in European starlings (Sturnus vulgaris). Behav Neurosci 120:1326–1336

    Article  PubMed  PubMed Central  Google Scholar 

  • Alger SJ, Maasch SN, Riters LV (2009) Lesions to the medial preoptic nucleus affect immediate early gene immunolabeling in brain regions involved in song control and social behavior in male European starlings. Eur J Neurosci 29:970–982. doi:10.1111/j.1460-9568.2009.06637.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Amin N, Gastpar M, Theunissen FE (2013) Selective and efficient neural coding of communication signals depends on early acoustic and social environment. PLoS One 8:e61417. doi:10.1371/journal.pone.0061417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asher L, Bateson M (2008) Use and husbandry of captive European starlings (Sturnus vulgaris) in scientific research: a review of current practice. Lab Anim 42:111–126. doi:10.1258/la.2007.007006

    Article  CAS  PubMed  Google Scholar 

  • Austad SN (2011) Candidate bird species for use in aging research. ILAR J 52:89–96

    Article  CAS  PubMed  Google Scholar 

  • Ball GF, Balthazart J (2001) Ethological concepts revisited: immediate early gene induction in response to sexual stimuli in birds. Brain Behav Evol 57:252–270. doi:10.1159/000047244

    Article  CAS  PubMed  Google Scholar 

  • Ball GF, Bentley GE (2000) Neuroendocrine mechanisms mediating the photoperiodic and social regulation of seasonal reproduction in birds. In: Wallen K, Schneider F (eds) Reproduction in context. MIT Press, Cambridge, MA, pp 129–158

  • Ball GF, Wingfield JC (1987) Changes in plasma levels of sex steroids in relation to multiple broodedness and nest site density in male starlings. Physiol Zool 60:191–196

    Article  CAS  Google Scholar 

  • Ball GF, Casto JM, Bernard DJ (1994) Sex-differences in the volume of avian song control nuclei—comparative-studies and the issue of brain nucleus delineation. Psychoneuroendocrinology 19:485–504

    Article  CAS  PubMed  Google Scholar 

  • Ball GF, Bernard DJ, Foidart A et al (1999) Steroid sensitive sites in the avian brain: does the distribution of the estrogen receptor alpha and beta types provide insight into their function? Brain Behav Evol 54:28–40

    Article  CAS  PubMed  Google Scholar 

  • Bee MA, Klump GM (2004) Primitive auditory stream segregation: a neurophysiological study in the songbird forebrain. J Neurophysiol 92:1088–1104. doi:10.1152/jn.00884.2003

    Article  PubMed  Google Scholar 

  • Bentley GE, Van’t Hof TJ, Ball GF (1999) Seasonal neuroplasticity in the songbird telencephalon: a role for melatonin. Proc Natl Acad Sci USA 96:4674–4679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernard DJ, Ball GF (1997) Photoperiodic condition modulates the effects of testosterone on song control nuclei volumes in male European starlings. Gen Comp Endocrinol 105:276–283

    Article  CAS  PubMed  Google Scholar 

  • Bernard DJ, Casto JM, Ball GF (1993) Sexual dimorphism in the volume of song control nuclei in European starlings: assessment by a Nissl stain and autoradiography for muscarinic cholinergic receptors. J Comp Neurol 334:559–570. doi:10.1002/cne.903340405

    Article  CAS  PubMed  Google Scholar 

  • Bernard DJ, Eens M, Ball GF (1996) Age- and behavior-related variation in volumes of song control nuclei in male European starlings. J Neurobiol 30:329–339. doi:10.1002/(SICI)1097-4695(199607)30:3<329:AID-NEU2>3.0.CO;2-6

    Article  CAS  PubMed  Google Scholar 

  • Bigalke-Kunz B, Rübsamen R, Dörrscheidt GJ (1987) Tonotopic organization and functional characterization of the auditory thalamus in a songbird, the European starling. J Comp Physiol A 161:255–265. doi:10.1007/BF00615245

    Article  CAS  PubMed  Google Scholar 

  • Bolhuis JJ, Eda-Fujiwara H (2003) Bird brains and songs: neural mechanisms of birdsong perception and memory. Anim Biol 53:129–145. doi:10.1163/157075603769700331

    Article  Google Scholar 

  • Bullough WS (1942) The reproductive cycles of the British and continental races of the starling (Sturnus vulgaris L.). Phil trans R Soc Lond B 231:165–246

    Article  Google Scholar 

  • Cousillas HH, George II, Alcaix SS et al (2013) Seasonal female brain plasticity in processing social vs. sexual vocal signals. Eur J Neurosci 37:728–734. doi:10.1111/ejn.12089

    Article  PubMed  Google Scholar 

  • Datta R, Lee J, Duda J et al (2012) A digital atlas of the dog brain. PLoS One 7:e52140. doi:10.1371/journal.pone.0052140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson A, Howe PD (1983) Plasma corticosterone in wild starlings (Sturnus vulgaris) immediately following capture and in relation to body weight during the annual cycle. Gen Comp Endocrinol 51:303–308

    Article  CAS  PubMed  Google Scholar 

  • De Groof G, Verhoye M, Van Meir V et al (2008) Seasonal rewiring of the songbird brain: an in vivo MRI study. Eur J Neurosci 28:2475–2485. doi:10.1111/j.1460-9568.2008.06545.x (discussion 2474)

    Article  PubMed  Google Scholar 

  • De Groof G, Verhoye M, Poirier C et al (2009) Structural changes between seasons in the songbird auditory forebrain. J Neurosci 29:13557–13565. doi:10.1523/JNEUROSCI.1788-09.2009

    Article  PubMed  Google Scholar 

  • De Groof G, Poirier C, George I et al (2013) Functional changes between seasons in the male songbird auditory forebrain. Front Behav Neurosci 7:196. doi:10.3389/fnbeh.2013.00196

    Article  PubMed  PubMed Central  Google Scholar 

  • Ellis JMS, Riters LV (2013) Patterns of FOS protein induction in singing female starlings. Behav Brain Res 237:148–156. doi:10.1016/j.bbr.2012.09.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eng ML, Williams TD, Letcher RJ, Elliott JE (2014) Assessment of concentrations and effects of organohalogen contaminants in a terrestrial passerine, the European starling. Sci Total Environ 473:589–596. doi:10.1016/j.scitotenv.2013.12.072

    Article  PubMed  Google Scholar 

  • Feinkohl A, Klump G (2011) Processing of transient signals in the visual system of the European starling (Sturnus vulgaris) and humans. Vis Res 51:21–25. doi:10.1016/j.visres.2010.09.020

    Article  PubMed  Google Scholar 

  • Gale SD, Perkel DJ (2006) Physiological properties of zebra finch ventral tegmental area and substantia nigra pars compacta neurons. J Neurophysiol 96:2295–2306. doi:10.1152/jn.01040.2005

    Article  PubMed  Google Scholar 

  • Gentner TQ, Hulse SH, Duffy D, Ball GF (2001) Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J Neurobiol 46:48–58

    Article  CAS  PubMed  Google Scholar 

  • George I, Cousillas H (2012) How social experience shapes song representation in the brain of starlings. J Physiol Paris. doi:10.1016/j.jphysparis.2012.12.002

    PubMed  Google Scholar 

  • George I, Vernier B, Richard JP et al (2004) Hemispheric specialization in the primary auditory area of awake and anesthetized starlings (*Sturnus vulgaris*). Behav Neurosci 118:597–610. doi:10.1037/0735-7044.118.3.597

    Article  PubMed  Google Scholar 

  • Grue CE, Franson LP (1986) Use of captive starlings to determine effects of environmental contaminants on passerine reproduction—pen characteristics and nestling food-requirements. Bull Environ Contam Toxicol 37:655–663

    Article  CAS  PubMed  Google Scholar 

  • Güntürkün O, Verhoye M, De Groof G, Van der Linden A (2013) A 3-dimensional digital atlas of the ascending sensory and the descending motor systems in the pigeon brain. Brain Struct Funct 218:269–281. doi:10.1007/s00429-012-0400-y

    Article  PubMed  Google Scholar 

  • Hausberger M, Cousillas H (1995) Categorization in birdsong: from behavioural to neuronal responses. Behav Process 35:83–91

    Article  CAS  Google Scholar 

  • Hausberger M, Richard-Yris MA, Henry L et al (1995) Song sharing reflects the social organization in a captive group of European starlings (Sturnus vulgaris). J Comp Psychol 109:222–241

    Article  Google Scholar 

  • Hausberger M, Forasté MA, Richard-Yris CN (1997) Differential response of female starlings to shared and nonshared song types. Etologia 5:31–38

    Google Scholar 

  • Heimovics SA, Cornil CA, Ellis JMS et al (2011) Seasonal and individual variation in singing behavior correlates with alpha 2-noradrenergic receptor density in brain regions implicated in song, sexual, and social behavior. Neuroscience 182:133–143. doi:10.1016/j.neuroscience.2011.03.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henry L, Hausberger M, Jenkins PF (1994) The use of song repertoire changes with pairing status in male European starling. Bioacoustics 5:261–266

    Article  Google Scholar 

  • Henry L, Bourguet C, Coulon M et al (2013) Sharing mates and nest boxes is associated with female “friendship” in European starlings, Sturnus vulgaris. J Comp Psychol 127:1–13. doi:10.1037/a0029975

    Article  PubMed  Google Scholar 

  • Jarvis ED, Nottebohm F (1997) Motor-driven gene expression. Proc Natl Acad Sci USA 94:4097–4102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

  • Kirn JR, Fishman Y, Sasportas K et al (1999) Fate of new neurons in adult canary high vocal center during the first 30 days after their formation. J Comp Neurol 411:487–494. doi:10.1002/(SICI)1096-9861(19990830)411:3<487:AID-CNE10>3.0.CO;2-M

    Article  CAS  PubMed  Google Scholar 

  • Kumazawa-Manita N, Katayama M, Hashikawa T, Iriki A (2013) Three-dimensional reconstruction of brain structures of the rodent Octodon degus: a brain atlas constructed by combining histological and magnetic resonance images. Exp Brain Res Exp Hirnforsch Exp Cereb 231:65–74. doi:10.1007/s00221-013-3667-1

    Article  Google Scholar 

  • Leppelsack HJ, Vogt M (1976) Responses of auditory neurons in forebrain of a songbird to stimulation with species-specific sounds. J Comp Physiol 107:263–274

    Article  Google Scholar 

  • Lima SL (1983) Patch sampling behavior of starlings foraging in simple patchy environments. Am Zool 23:897

    Google Scholar 

  • Ma Y, Hof PR, Grant SC et al (2005) A three-dimensional digital atlas database of the adult C57BL/6J mouse brain by magnetic resonance microscopy. Neuroscience 135:1203–1215. doi:10.1016/j.neuroscience.2005.07.014

    Article  CAS  PubMed  Google Scholar 

  • Meitzen J, Weaver AL, Brenowitz EA, Perkel DJ (2009) Plastic and stable electrophysiological properties of adult avian forebrain song-control neurons across changing breeding conditions. J Neurosci 29:6558–6567. doi:10.1523/JNEUROSCI.5571-08.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Metzdorf R, Gahr M, Fusani L (1999) Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds. J Comp Neurol 407:115–129

    Article  CAS  PubMed  Google Scholar 

  • Mooney R, Prather JF (2005) The HVC microcircuit: the synaptic basis for interactions between song motor and vocal plasticity pathways. J Neurosci 25:1952–1964. doi:10.1523/JNEUROSCI.3726-04.2005

    Article  CAS  PubMed  Google Scholar 

  • Muñoz-Moreno E, Arbat-Plana A, Batalle D et al (2013) A magnetic resonance image based atlas of the rabbit brain for automatic parcellation. PLoS One 8:e67418. doi:10.1371/journal.pone.0067418

    Article  PubMed  PubMed Central  Google Scholar 

  • Nie B, Chen K, Zhao S et al (2013) A rat brain MRI template with digital stereotaxic atlas of fine anatomical delineations in paxinos space and its automated application in voxel-wise analysis. Hum Brain Mapp 34:1306–1318. doi:10.1002/hbm.21511

    Article  PubMed  PubMed Central  Google Scholar 

  • Nixdorf-Bergweiler BE, Bischof HJ (2007) A stereotaxic atlas of the brain of the zebra finch Taeniopygia guttata with special emphasis on telencephalic visual and song system nuclei in transverse and sagittal sections. National Library of Medicine, Bethesda

    Google Scholar 

  • Poirier C, Vellema M, Verhoye M et al (2008) A three-dimensional MRI atlas of the zebra finch brain in stereotaxic coordinates. Neuroimage 41:1–6. doi:10.1016/j.neuroimage.2008.01.069

    Article  PubMed  Google Scholar 

  • Poirier C, Boumans T, Verhoye M et al (2009) Own-song recognition in the songbird auditory pathway: selectivity and lateralization. J Neurosci 29:2252–2258. doi:10.1523/JNEUROSCI.4650-08.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powell G (1974) Experimental analysis of social value of flocking by starlings (Sturnus vulgaris) in relation to predation and foraging. Anim Behav 22:501–505. doi:10.1016/S0003-3472(74)80049-7

    Article  Google Scholar 

  • Puelles L, Martinez-de-la-Torre M, Paxinos G et al (2007) The chick brain in stereotaxic coordinates: an atlas featuring neurometric subdivisions and mammalian homologies. Academic Press, San Diego

    Google Scholar 

  • Riters LV, Eens M, Pinxten R et al (2000) Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm Behav 38:250–261

    Article  CAS  PubMed  Google Scholar 

  • Roberts TF, Klein ME, Kubke MF et al (2008) Telencephalic neurons monosynaptically link brainstem and forebrain premotor networks necessary for song. J Neurosci 28:3479–3489. doi:10.1523/JNEUROSCI.0177-08.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saleem KS, Logothetis NK (2007) A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates. Academic Press, San Diego

    Google Scholar 

  • Stokes TM, Leonard CM, Nottebohm F (1974) The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J Comp Neurol 156:337–374

    Article  CAS  PubMed  Google Scholar 

  • Tinbergen JM (1981) Foraging decisions in starlings (Sturnus vulgaris L). Ardea 69:1–67

    Google Scholar 

  • Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23:251–258

    Article  CAS  PubMed  Google Scholar 

  • Tramontin AD, Smith GT, Breuner CW, Brenowitz EA (1998) Seasonal plasticity and sexual dimorphism in the avian song control system: stereological measurement of neuron density and number. J Comp Neurol 396:186–192

    Article  CAS  PubMed  Google Scholar 

  • Ullmann JFP, Watson C, Janke AL et al (2014) An MRI atlas of the mouse basal ganglia. Brain Struct Funct 219:1343–1353. doi:10.1007/s00429-013-0572-0

    Article  PubMed  Google Scholar 

  • Van Essen DC (2005) A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. Neuroimage 28:635–662. doi:10.1016/j.neuroimage.2005.06.058

    Article  PubMed  Google Scholar 

  • Van Meir V, Boumans T, De Groof G et al (2005) Spatiotemporal properties of the BOLD response in the songbirds’ auditory circuit during a variety of listening tasks. Neuroimage 25:1242–1255. doi:10.1016/j.neuroimage.2004.12.058

    Article  PubMed  Google Scholar 

  • Van Ruijssevelt L, De Groof G, Van der Kant A et al (2013) Functional magnetic resonance imaging (FMRI) with auditory stimulation in songbirds. J Vis Exp. doi:10.3791/4369

    PubMed  PubMed Central  Google Scholar 

  • Vellema M, Verschueren J, Van Meir V, Van der Linden A (2011) A customizable 3-dimensional digital atlas of the canary brain in multiple modalities. Neuroimage 57:352–361. doi:10.1016/j.neuroimage.2011.04.033

    Article  PubMed  Google Scholar 

  • Voss HU, Tabelow K, Polzehl J et al (2007) Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography. Proc Natl Acad Sci USA 104:10667–10672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We are grateful to Steven Staelens and Steven Deleye from MICA (Universiteit Antwerpen) for support during CT scans. This research was supported by a joint “Tournesol” Grant (Project No. 20371TA) from the Flemish and French governments to I. G., a “PICS” Grant (Project No. 5992) from the French CNRS to I. G. and G. DG and Grants from the Research Foundation—Flanders (FWO, Project No. G030213N and G044311N), the Hercules Foundation (Grant No. AUHA0012), Concerted Research Actions (GOA Funding) from the University of Antwerp and Interuniversity Attraction Poles (IAP) (‘PLASTOCINE’: P7/17) to A.VdL. I. G., H. C. and M. H. are supported by the University of Rennes 1 and by the French CNRS. O. G. was supported by the DFG via SFB874. G. DG is a Postdoctoral Fellow of the Research Foundation—Flanders (FWO).

Ethical standard

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Geert De Groof.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

De Groof, G., George, I., Touj, S. et al. A three-dimensional digital atlas of the starling brain. Brain Struct Funct 221, 1899–1909 (2016). https://doi.org/10.1007/s00429-015-1011-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-015-1011-1

Keywords