Skip to main content
SpringerLink
Log in

Topography of the human acoustic radiation as revealed by ex vivo fibers micro-dissection and in vivo diffusion-based tractography

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

Abstract

The acoustic radiation is a compact bundle of fibers conveying auditory information from the medial geniculate nucleus of the thalamus to the auditory cortex. Topographical knowledge of this bundle in primates is scarce and in vivo diffusion-based tractography reconstructions in humans remains challenging, especially with the most widely used MRI acquisition protocols. Therefore, the AR represents a notable anatomical omission in the neurobiological investigation of acoustic and linguistic functional mechanisms in humans. In this study, we combine blunt micro-dissections and advanced diffusion tractography methods to provide novel insights into the topographical anatomy of this bundle in humans. Evidences from ex vivo blunt micro-dissection in three human (two right) hemispheres are compared to the 3D profile of this bundle as reconstructed by tractography techniques in four healthy adult data sets provided by the Human Connectome Project. Both techniques show the unique trajectory of the AR, a transversal course from the midline to the lateral convexity of the posterior temporal lobe. Blunt dissections demonstrated three portions of this bundle that we defined as the genu, stem, and fan, revealing the intimate relationships that each of these components has with neighboring association and projection pathways. Probabilistic tractography and ultra-high b values provided results comparable to blunt micro-dissections and highlighted the main limitations in tracking the AR. This is, to our knowledge, the first ex vivo/in vivo integrated study providing novel and reliable information about the precise anatomy of the AR, which will be important for future investigations in the neuroscientific, clinical, and surgical field.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexander DC, Barker GJ (2005) Optimal imaging parameters for fiber-orientation estimation in diffusion MRI. Neuroimage 27:357–367. doi:10.1016/j.neuroimage.2005.04.008

    Article  PubMed  Google Scholar 

  • Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259–267. doi:10.1016/S0006-3495(94)80775-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behrens TEJ, Berg HJ, Jbabdi S, Rushworth MFS, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34:144–155. doi:10.1016/j.neuroimage.2006.09.018

    Article  CAS  PubMed  Google Scholar 

  • Berman JI, Lanza MR, Blaskey L, Edgar JC, Roberts TPL (2013) High angular resolution diffusion imaging probabilistic tractography of the auditory radiation. Am J Neuroradiol 34:1573–1578. doi:10.3174/ajnr.A3471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bürgel U, Amunts K, Hoemke L, Mohlberg H, Gilsbach JM, Zilles K (2006) White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability. Neuroimage 29:1092–1105. doi:10.1016/j.neuroimage.2005.08.040

    Article  PubMed  Google Scholar 

  • Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77–94. doi:10.1006/nimg.2002.1136

    Article  PubMed  Google Scholar 

  • Catani M, Jones DK, Donato R, Ffytche DH (2003) Occipito-temporal connections in the human brain. Brain 126:2093–2107. doi:10.1093/brain/awg203

    Article  PubMed  Google Scholar 

  • Catani M, Jones DK, Ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57:8–16. doi:10.1002/ana.20319

    Article  PubMed  Google Scholar 

  • Chamberland M, Whittingstall K, Fortin D, Mathieu D, Descoteaux M (2014) Real-time multi-peak tractography for instantaneous connectivity display. Front Neuroinform 8:1–15. doi:10.3389/fninf.2014.00059

    Article  Google Scholar 

  • Chang Y, Lee SH, Lee YJ, Hwang MJ, Bae SJ, Kim MN, Kang DS (2004) Auditory neural pathway evaluation on sensorineural hearing loss using diffusion tensor imaging. NeuroReport 15(11):1699–1703

    Article  PubMed  Google Scholar 

  • Crippa A, Lanting CP, van Dijk P, Roerdink JBTM (2010) A diffusion tensor imaging study on the auditory system and tinnitus. Open Neuroimaging J 4:16–25. doi:10.2174/1874440001004010016

    Article  Google Scholar 

  • De Benedictis A, Petit L, Descoteaux M, Marras CE, Barbareschi M, Corsini F, Dallabona M, Chioffi F, Sarubbo S (2016) New insights in the homotopic and heterotopic connectivity of the frontal portion of the human corpus callosum revealed by microdissection and diffusion tractography. Hum Brain Mapp 37:4718–4735. doi:10.1002/hbm.23339

    Article  PubMed  Google Scholar 

  • Dejerine J (1895) Anatomie des Centres Nerveux. Reuff, Paris

    Google Scholar 

  • Dell’Acqua F, Catani M (2012) Structural human brain networks: hot topics in diffusion tractography. Curr Opin Neurol 25:375–383. doi:10.1097/WCO.0b013e328355d544

    PubMed  Google Scholar 

  • Dell’Acqua F, Scifo P, Rizzo G, Catani M, Simmons A, Scotti G, Fazio F (2010) A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution. Neuroimage 49:1446–1458. doi:10.1016/j.neuroimage.2009.09.033

    Article  PubMed  Google Scholar 

  • Descoteaux M, Deriche R, Knosche T, Anwander A (2009) Deterministic and probabilistic tractography based on complex fiber orientation distribution. IEEE Trans Med Imaging 28:269–286

    Article  PubMed  Google Scholar 

  • Duffau H, Moritz-Gasser S, Mandonnet E (2014) A re-examination of neural basis of language processing: proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang 131:1–10. doi:10.1016/j.bandl.2013.05.011

    Article  PubMed  Google Scholar 

  • Fan Q, Witzel T, Nummenmaa A, Van Dijk KRA, Van Horn JD, Drews MK, Somerville LH, Sheridan MA, Santillana RM, Snyder J, Hedden T, Shaw EE, Hollinshead MO, Renvall V, Zanzonico R, Keil B, Cauley S, Polimeni JR, Tisdall D, Buckner RL, Wedeen VJ, Wald LL, Toga AW, Rosen BR (2015) MGH-USC Human Connectome Project datasets with ultra-high b-value diffusion MRI. Neuroimage. doi:10.1016/j.neuroimage.2015.08.075

    Google Scholar 

  • Fernández-Miranda JC, Wang Y, Pathak S, Stefaneau L, Verstynen T, Yeh F-C (2015) Asymmetry, connectivity, and segmentation of the arcuate fascicle in the human brain. Brain Struct Funct 220:1665–1680. doi:10.1007/s00429-014-0751-7

    Article  PubMed  Google Scholar 

  • Flechsig P (1920) Anatomie des menschlichen Gehirns und Rucken-marks auf myellogenetischer Grundlage. Erster Band, Georg Thieme Verlag, Leipzig

    Google Scholar 

  • Hackett TA, Stepniewska I, Kaas JH (1998) Thalamocortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol 400:271–286

    Article  CAS  PubMed  Google Scholar 

  • Hickok G, Poeppel D (2004) Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language. Cognition 92:67–99. doi:10.1016/j.cognition.2003.10.011

    Article  PubMed  Google Scholar 

  • Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8:393–402. doi:10.1038/nrn2113

    Article  CAS  PubMed  Google Scholar 

  • Javad F, Warren JD, Micallef C, Thornton JS, Golay X, Yousry T, Mancini L (2014) Auditory tracts identified with combined fMRI and diffusion tractography. Neuroimage 84:562–574. doi:10.1016/j.neuroimage.2013.09.007

    Article  PubMed  PubMed Central  Google Scholar 

  • Jbabdi S, Johansen-Berg H (2011) Tractography: where do we go from here? Brain Connect 1(3):169–183

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeurissen B, Leemans A, Tournier JD, Jones DK, Sijbers J (2013) Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum Brain Mapp 34:2747–2766. doi:10.1002/hbm.22099

    Article  PubMed  Google Scholar 

  • Jeurissen B, Tournier J-D, Dhollander T, Connelly A, Sijbers J (2014) Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. Neuroimage 103:411–426. doi:10.1016/j.neuroimage.2014.07.061

    Article  PubMed  Google Scholar 

  • Jones DK, Cercignani M (2010) Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed 23:803–820. doi:10.1002/nbm.1543

    Article  PubMed  Google Scholar 

  • Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang M-C, Christensen GE, Collins DL, Gee J, Hellier P, Song JH, Jenkinson M, Lepage C, Rueckert D, Thompson P, Vercauteren T, Woods RP, Mann JJ, Parsey RV (2009) Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 46:786–802. doi:10.1016/j.neuroimage.2008.12.037

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee YJ, Bae SJ, Lee SH, Lee JJ, Lee KY, Kim MN, Kim YS, Baik SK, Woo S, Chang Y (2007) Evaluation of white matter structures in patients with tinnitus using diffusion tensor imaging. J Clin Neurosci 14:515–519. doi:10.1016/j.jocn.2006.10.002

    Article  PubMed  Google Scholar 

  • Lin Y, Wang J, Wu C, Wai Y, Yu J, Ng S (2008) Diffusion tensor imaging of the auditory pathway in sensorineural hearing loss: changes in radial diffusivity and diffusion anisotropy. J Magn Reson Imaging 28(3):598–603

    Article  PubMed  Google Scholar 

  • Maffei C, Soria G, Prats-Galino A, Catani M (2015) Imaging white-matter pathways of the auditory system with diffusion imaging tractography. In: Celesia GG, Hickok G (eds) The human auditory system: fundamental organization and clinical disorders. Elsevier Inc., Amsterdam

    Google Scholar 

  • Martino J, Vergani F, Robles SG, Duffau H (2010) New insights into the anatomic dissection of the temporal stem with special emphasis on the inferior fronto-occipital fasciculus. Oper Neurosurg 66:4–12. doi:10.1227/01.NEU.0000348564.28415

    Article  Google Scholar 

  • Mesulam MM, Pandya DN (1973) The projections of the medial geniculate complex within the sylvian fissure of the rhesus monkey. Brain Res 60:315–333

    Article  CAS  PubMed  Google Scholar 

  • Patenaude B, Smith SM, Kennedy D, Jenkinson M (2012) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 56:907–922. doi:10.1016/j.neuroimage.2011.02.046

    Article  Google Scholar 

  • Pfeifer R (1920) Myelogenetisch-anatomische Untersuchungen uber das kortikale Ende der Horleitung. Abh Math Phys Kl Sachs Akad Wiss 37:1–54

    Google Scholar 

  • Poeppel D, Emmorey K, Hickok G, Pylkkänen L (2012) Towards a new neurobiology of language. J Neurosci 32:14125–14131. doi:10.1523/JNEUROSCI.3244-12.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rademacher J, Bürgel U, Zilles K (2002) Stereotaxic localization, intersubject variability, and interhemispheric differences of the human auditory thalamocortical system. Neuroimage 17:142–160

    Article  CAS  PubMed  Google Scholar 

  • Saffran EM, Marin OS, Yeni-Komshian GH (1976) An analysis of speech perception in word deafness. Brain Lang 3:209–228

    Article  CAS  PubMed  Google Scholar 

  • Sarubbo S, De Benedictis A, Milani P, Paradiso B, Barbareschi M, Rozzanigo U, Colarusso E, Tugnoli V, Farneti M, Granieri E, Duffau H, Chioffi F (2015) The course and the anatomo-functional relationships of the optic radiation: a combined study with “post mortem” dissections and “in vivo” direct electrical mapping. J Anat 226:47–59. doi:10.1111/joa.12254

    Article  PubMed  Google Scholar 

  • Sarubbo S, De Benedictis A, Merler S, Mandonnet E, Barbareschi M, Dallabona M, Chioffi F, Duffau H (2016) Structural and functional integration between dorsal and ventral language streams as revealed by blunt dissection and direct electrical stimulation. Hum Brain Mapp 37:3858–3872. doi:10.1002/hbm.23281

    Article  PubMed  Google Scholar 

  • Saur D, Kreher BW, Schnell S, Kümmerer D, Kellmeyer P, Vry M-S, Umarova R, Musso M, Glauche V, Abel S, Huber W, Rijntjes M, Hennig J, Weiller C (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci USA 105:18035–18040. doi:10.1073/pnas.0805234105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmahmann J, Pandya D (2006) Fiber pathways of the brain. Oxford University Press, Oxford

    Book  Google Scholar 

  • Smith RE, Tournier J-D, Calamante F, Connelly A (2012) Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage 62:1924–1938. doi:10.1016/j.neuroimage.2012.06.005

    Article  PubMed  Google Scholar 

  • Stefanatos GA, Gershkoff A, Madigan S (2005) On pure word deafness, temporal processing, and the left hemisphere. J Int Neuropsychol Soc 11:456–470

    Article  PubMed  Google Scholar 

  • Tardif E, Clarke S (2001) Intrinsic connectivity of human auditory areas: a tracing study with DiI. Eur J Neurosci 13:1045–1050

    Article  CAS  PubMed  Google Scholar 

  • Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’Acqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DGM, Catani M (2011) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage 54:49–59. doi:10.1016/j.neuroimage.2010.07.055

    Article  PubMed  Google Scholar 

  • Tournier JD, Yeh CH, Calamante F, Cho KH, Connelly A, Lin CP (2008) Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage 42:617–625. doi:10.1016/j.neuroimage.2008.05.002

    Article  PubMed  Google Scholar 

  • Tournier J-D, Mori S, Leemans A (2011) Diffusion tensor imaging and beyond. Magn Reson Med 65:1532–1556. doi:10.1002/mrm.22924

    Article  PubMed  PubMed Central  Google Scholar 

  • Tournier JD, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22:53–66. doi:10.1002/ima.22005

    Article  Google Scholar 

  • Wang Y, Fernandez-Miranda JC, Verstynen T, Pathak S, Schneider W, Yeh FC (2012) Rethinking the role of the middle longitudinal fascicle in language and auditory pathways. Cereb Cortex 23:2347–2356. doi:10.1093/cercor/bhs225

    Article  PubMed  Google Scholar 

  • Wang X, Pathak S, Stefaneanu L, Yeh F-C, Li S, Fernandez-Miranda JC (2016) Subcomponents and connectivity of the superior longitudinal fasciculus in the human brain. Brain Struct Funct 221:2075–2092. doi:10.1007/s00429-015-1028-5

    Article  PubMed  Google Scholar 

  • Westerhausen R, Gruner R, Specht K, Hugdahl K (2009) Functional relevance of interindividual differences in temporal lobe callosal pathways: a DTI tractography study. Cereb Cortex 19:1322–1329. doi:10.1093/cercor/bhn173

    Article  PubMed  Google Scholar 

  • Zatorre RJ, Belin P, Penhune VB (2002) Structure and function of auditory cortex: music and speech. Trends Cogn Sci 6:37–46

    Article  PubMed  Google Scholar 

  • Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden markov random field model and the expectation-maximization algorithm 20:45–57

    CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Andrea Anderle, nurse and artist, for his artwork illustrating the course and main relationships of acoustic radiation as emerged by micro-dissection and tractography.

Author information

Authors and Affiliations

  1. CIMeC Center for Mind/Brain Sciences, Trento University, Trento, Italy

    Chiara Maffei & Jorge Jovicich

  2. Neurosurgery Unit, Department of Neuroscience and Neurorehabilitation, Bambino Gesù Children’s Hospital, IRCCS, Rome, Italy

    Alessandro De Benedictis

  3. Division of Neurosurgery, Structural and Functional Connectivity Lab (SFC-LSB) Project, Department of Neurosciences, “S. Chiara” Hospital, Trento APSS, 9, Largo Medaglie d’Oro, 38122, Trento, Italy

    Francesco Corsini, Franco Chioffi & Silvio Sarubbo

  4. Department of Histopathology, “S. Chiara” Hospital, Trento APSS, Trento, Italy

    Mattia Barbareschi

Authors
  1. Chiara Maffei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Jovicich
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alessandro De Benedictis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francesco Corsini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mattia Barbareschi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Franco Chioffi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Silvio Sarubbo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Silvio Sarubbo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (JPEG 7494 kb)

Supplementary material 2 (JPEG 7116 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maffei, C., Jovicich, J., De Benedictis, A. et al. Topography of the human acoustic radiation as revealed by ex vivo fibers micro-dissection and in vivo diffusion-based tractography. Brain Struct Funct 223, 449–459 (2018). https://doi.org/10.1007/s00429-017-1471-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-017-1471-6

Keywords

Search

Navigation