Skip to main content

Advertisement

Log in

Direct diffusion-based parcellation of the human thalamus

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

Abstract

To assess stable anatomical features of the human thalamus, an unbiased diffusion tensor parcellation approach was used to segment thalamic substructures with similar spatial orientation. We determined localization, size and individual variations of 21 thalamic clusters in a group of 63 healthy human subjects (32 males/31 females). The laterality differences accounted for ±6 % and gender differences for ±4 % of the thalamic volume. Consecutively, five stable clusters in the anterior, medial, lateral and posterior thalamus were selected, which were common to 90 % of all subjects and contained at least 10 voxels. These clusters could be assigned to the anteroventral nucleus (AN) group, the mediodorsal (MD) nucleus, the medial pulvinar (PuM), and the lateral nuclei group. The subcortical and cortical connectivity of these clusters revealed that: (1) the oblique cranio-caudal-oriented fibers of the AN cluster mainly connect to limbic structures, (2) the numerous dorso-frontal-oriented fibers of MD mainly project to the prefrontal cortex and the medial temporal lobe, (3) the fibers of the PuM running in parallel with the x-axis project to medio-occipital and medio-temporal areas and connect visual areas with the hippocampus and amygdala and via intrathalamic pathways with medio-frontal areas, and (4) the oblique caudo-cranial fibers of the two lateral clusters located anteriorly in the motor and posteriorly in the sensory thalamus are routing sensory–motor information from the brain stem via the internal capsule to pre- and peri-central regions of the cortex.

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

Access this article

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
Fig. 7

Similar content being viewed by others

Abbreviations

AC:

Anterior commissure

Acc:

Nucleus accumbens

AD:

Anterodorsal nucleus

AM:

Anteromedial nucleus

Amy:

Amygdala

AN:

Anterior cluster

AV:

Anteroventral group

BS:

Brainstem

Cau:

Caudate nucleus

CoG:

Center of gravity

DDO:

Dominant diffusion orientations

Den:

Dentate nucleus

DTI:

Diffusion tensor imaging

EPI:

Echo planar imaging

Hip:

Hippocampus

LA:

Lateral-anterior cluster

LD:

Lateral dorsal group

LP:

Lateral-posterior cluster

MD:

Mediodorsal nucleus

MED:

Medial cluster

MRI:

Magnetic resonance imaging

Pal:

Pallidum

PC:

Posterior commissure

PO:

Posterior cluster

PuM:

Medial pulvinar

Put:

Putamen

Red:

Red nucleus

SD:

Standard deviation

T :

Tesla

TE:

Echo time

TR:

Repetition time

VA:

Ventral anterior

VLa:

Ventral lateral anterior

VLp:

Ventral lateral posterior

VM:

Ventral medial

VP:

Ventral posterior complex

VPI:

Ventral posterior inferior nucleus

VPL:

Ventral posterolateral

VPM:

Ventral posteromedial

References

  • Abosch A, Yacoub E, Ugurbil K, Harel N (2010) An assessment of current brain targets for deep brain stimulation surgery with susceptibility-weighted imaging at 7 Tesla. Neurosurgery 67:1745–1756

    Article  PubMed Central  PubMed  Google Scholar 

  • Aggleton JP, Mishkin M (1984) Projections of the amygdala to the thalamus in the cynomolgus monkey. J Comp Neurol 222:56–68

    Google Scholar 

  • Akert K (1964) Comparative anatomy of frontal cortex and thalamo-frontal connections. In: Warren JM, Akert K (eds) The frontal granular cortex and behavior. McGraw-Hill, NewYork, pp 372–396

  • Alexander DC, Pierpaoli C, Basser PJ, Gee JC (2001) Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans Med Imaging 20:1131–1139

    Article  CAS  PubMed  Google Scholar 

  • Amunts VV (2008) Individual variability in the structural asymmetry of the dorsomedial nucleus of the thalamus in men and women. Neurosci Behav Physiol 38:715–720

    Article  CAS  PubMed  Google Scholar 

  • Baas D, Aleman A, Kahn RS (2004) Lateralization of amygdala activation: a systematic review of functional neuroimaging studies. Brain Res Rev 45:96–103

    Article  PubMed  Google Scholar 

  • Baron-Cohen S, Wheelwright S (2004) The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Autism Dev Disord 34:163–175

    Article  PubMed  Google Scholar 

  • Behrens TEJ, Johansen-Berg H, Woolrich MW et al (2003a) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6:750–757

    Article  CAS  PubMed  Google Scholar 

  • Behrens TEJ, Woolrich MW, Jenkinson M et al (2003b) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077–1088

    Article  CAS  PubMed  Google Scholar 

  • Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132

    Article  PubMed  Google Scholar 

  • Cook P, Bai Y, Gilani N et al. (2006) Camino: open-source diffusion-MRI reconstruction and processing. In: 14th scientific meeting of the international society for magnetic resonance in medicine, vol. 2759

  • Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194

    Article  CAS  PubMed  Google Scholar 

  • De Sousa TB, de Santana MAD, Ade MS et al (2013) Mediodorsal thalamic nucleus receives a direct retinal input in marmoset monkey (Callithrix jacchus): a subunit B cholera toxin study. Ann Anat 195:32–38

    Article  PubMed  Google Scholar 

  • Deoni SCL, Rutt BK, Parrent AG, Peters TM (2007) Segmentation of thalamic nuclei using a modified k-means clustering algorithm and high-resolution quantitative magnetic resonance imaging at 1.5 T. NeuroImage 34:117–126

    Article  PubMed  Google Scholar 

  • Fischer J, Whitney D (2012) Attention gates visual coding in the human pulvinar. Nat Commun 3:1051

    Article  PubMed Central  PubMed  Google Scholar 

  • Friston KJ, Jezzard P, Turner R (1994) Analysis of functional MRI time-series. Hum Brain Mapp 1:153–171

    Article  Google Scholar 

  • Fuster JM (1997) The prefrontal cortex: anatomy, physiology, and neuropsychology of the frontal lobe. Lippincott-Raven, Philadelphia

  • Goebel R, Esposito F, Formisano E (2006) Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum Brain Mapp 27:392–401

    Article  PubMed  Google Scholar 

  • Granziera C, Hadjikhani N, Arzy S et al (2011) In-vivo magnetic resonance imaging of the structural core of the Papez circuit in humans. Neuroreport 22:227–231

    Google Scholar 

  • Gringel T, Schulz-Schaeffer W, Elolf E et al (2009) Optimized high-resolution mapping of magnetization transfer (MT) at 3 Tesla for direct visualization of substructures of the human thalamus in clinically feasible measurement time. J Magn Reson Imaging 29:1285–1292

    Article  PubMed  Google Scholar 

  • Hebb AO, Ojemann GA (2013) The thalamus and language revisited. Brain Lang 126:99–108

    Article  PubMed  Google Scholar 

  • Johansen-Berg H, Behrens TEJ, Sillery E et al (2005) Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cereb Cortex 15:31–39

    Article  PubMed  Google Scholar 

  • Jones EG (2007) The Thalamus 2 Volume Set. Cambridge University Press

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

    Article  PubMed  Google Scholar 

  • Krauth A, Blanc R, Poveda A et al (2010) A mean three-dimensional atlas of the human thalamus: generation from multiple histological data. Neuroimage 49:2053–2062

    Article  PubMed  Google Scholar 

  • Kumar K, Mang S, Grodd W (2010) Consistency of automatic thalamus segmentation using DTI. Poster presented at the 16th annual meeting of the organization for human brain mapping, Barcelona (see supplement material)

  • Kumar K, Mang S, Reiterer S., Grodd W. (2011) DTI of the human thalamus: hemispheric and gender variability. Oral presentation in 17th annual meeting of the organization for human brain mapping, Québec (see supplement material)

  • Leemans A, Jones DK (2009) The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61:1336–1349

    Article  PubMed  Google Scholar 

  • Lemaire J–J, Coste J, Ouchchane L et al (2007) Brain mapping in stereotactic surgery: a brief overview from the probabilistic targeting to the patient-based anatomic mapping. Neuroimage 37(Suppl 1):S109–S115

    Article  PubMed  Google Scholar 

  • Lemaire J–J, Sakka L, Ouchchane L et al (2010) Anatomy of the human thalamus based on spontaneous contrast and microscopic voxels in high-field magnetic resonance imaging. Neurosurgery 66:161–172

    Article  PubMed  Google Scholar 

  • Mai JK, Forutan F (2012) Thalamus. In: Mai Juergen K, Paxinos George (eds) Human nervous system, 3rd edn. Academic Press, San Diego, pp 618–677

    Chapter  Google Scholar 

  • Mai JK, Paxinos G, Voss T (2008) Atlas of the human brain. Academic Press, San Diego

    Google Scholar 

  • Mang SC, Busza A, Reiterer S et al (2012) Thalamus segmentation based on the local diffusion direction: a group study. Magn Reson Med 67:118–126

    Article  PubMed  Google Scholar 

  • Menzler K, Belke M, Wehrmann E et al (2011) Men and women are different: diffusion tensor imaging reveals sexual dimorphism in the microstructure of the thalamus, corpus callosum and cingulum. Neuroimage 54:2557–2562

    Article  CAS  PubMed  Google Scholar 

  • Morel A (2007) Stereotactic atlas of the human thalamus and basal ganglia. Informa Healthcare, New York, London

    Book  Google Scholar 

  • Niemann K, Mennicken VR, Jeanmonod D, Morel A (2000) The morel stereotactic atlas of the human thalamus: atlas-to-mr registration of internally consistent canonical model. NeuroImage 12:601–616

    Article  CAS  PubMed  Google Scholar 

  • Nieuwenhuys R, Voogd J, Huijzen CV et al (2008) The human central nervous system, 4th edn. Springer-Verlag, Berlin Heidelberg, New York

    Book  Google Scholar 

  • Padmala S, Lim S-L, Pessoa L (2010) Pulvinar and affective significance: responses track moment-to-moment stimulus visibility. Front Hum Neurosci 4:64

    Article  PubMed Central  PubMed  Google Scholar 

  • Papez JW (1937) A proposed mechanism of emotion. Arch Neural Psychiat 38:725–743

    Article  Google Scholar 

  • Percheron G, François C, Talbi B et al (1996) The primate motor thalamus. Brain Res Brain Res Rev 22:93–181

    Article  CAS  PubMed  Google Scholar 

  • Ray JP, Price JL (1992) The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain–prefrontal cortex topography. J Comp Neurol 323:167–197

    Google Scholar 

  • Rohde GK, Barnett AS, Basser PJ et al (2004) Comprehensive approach for correction of motion and distortion in diffusion-weighted MRI. Magn Reson Med 51:103–114

    Article  CAS  PubMed  Google Scholar 

  • Saalmann YB, Pinsk MA, Wang L et al (2012) The pulvinar regulates information transmission between cortical areas based on attention demands. Science 337:753–756

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schultz T (2011) Segmenting thalamic nuclei: what can we gain from HARDI? In: Fichtinger G, Martel A, Peters T (eds) Medical image computing and computer-assisted interventionMICCAI 2011. Springer, Berlin, Heidelberg, pp 141–148

    Chapter  Google Scholar 

  • Sherman SM, Guillery RW (2009) Exploring the thalamus and its role in cortical function. Mit Press, Cambridge

    Google Scholar 

  • Shipp S (2003) The functional logic of cortico-pulvinar connections. Philos Trans R Soc Lond B Biol Sci 358:1605–1624

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sladky R, Höflich A, Atanelov J et al (2012) Increased neural habituation in the amygdala and orbitofrontal cortex in social anxiety disorder revealed by fMRI. PLoS One 7:e50050

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219

    Article  PubMed  Google Scholar 

  • Spinks R, Magnotta VA, Andreasen NC et al (2002) Manual and automated measurement of the whole thalamus and mediodorsal nucleus using magnetic resonance imaging. Neuroimage 17:631–642

    Article  PubMed  Google Scholar 

  • Talairach J, David M, Tournoux P, Corredor H, Kvasina T (1957) Atlas d’Anatomie Ste′re′otaxique. Repe′rage Radiologique Indirect des Noyaux Gris Centraux, des Re′gions Me′sence′phalo-sous-Optique et Hypothalamique de l’Homme. Masson & Cie, Paris

  • Troiani V, Schultz RT (2013) Amygdala, pulvinar, and inferior parietal cortex contribute to early processing of faces without awareness. Front Hum Neurosci 7:241

    Article  PubMed Central  PubMed  Google Scholar 

  • Unrath A, Klose U, Grodd W et al (2008) Directional colour encoding of the human thalamus by diffusion tensor imaging. Neurosci Lett 434:322–327

    Article  CAS  PubMed  Google Scholar 

  • Vrtička P, Sander D, Vuilleumier P (2013) Lateralized interactive social content and valence processing within the human amygdala. Front Hum Neurosci 6:358

    PubMed Central  PubMed  Google Scholar 

  • Wager TD, Phan KL, Liberzon I, Taylor SF (2003) Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. NeuroImage 19:513–531

    Article  PubMed  Google Scholar 

  • Wiegell MR, Tuch DS, Larsson HB, Wedeen VJ (2003) Automatic segmentation of thalamic nuclei from diffusion tensor magnetic resonance imaging. NeuroImage 19:391–401

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The digital model of the 3D anatomy of the thalamus according to the atlas of Morel (Krauth et al. 2010) was obtained by a written consent with Prof. G. Székely from the Computer Vision Laboratory of the ETH Zürich. We thank Susanne Reiterer for providing the data, Klaus Scheffler for giving access to analysis facilities, Bernd Kardatzki for technical support, Ute Habel, and Eugene Datta for reviewing the manuscript. The German research council (DFG) Grant GR 833/9-1 in part supported this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wolfgang Grodd.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 7660 kb)

Supplementary material 2 (MP4 1483 kb)

Supplementary material 3 (MP4 1180 kb)

Supplementary material 4 (MP4 1364 kb)

Supplementary material 5 (MP4 1603 kb)

Supplementary material 6 (MP4 1467 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kumar, V., Mang, S. & Grodd, W. Direct diffusion-based parcellation of the human thalamus. Brain Struct Funct 220, 1619–1635 (2015). https://doi.org/10.1007/s00429-014-0748-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-014-0748-2

Keywords

Navigation