Skip to main content
SpringerLink
Log in

Anatomo-functional correspondence in the superior temporal sulcus

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

Abstract

The superior temporal sulcus (STS) is an intriguing region both for its complex anatomy and for the multiple functions that it hosts. Unfortunately, most studies explored either the functional organization or the anatomy of the STS only. Here, we link these two aspects by investigating anatomo-functional correspondences between the voice-sensitive cortex (Temporal Voice Areas) and the STS depth. To do so, anatomical and functional scans of 116 subjects were processed such as to generate individual surface maps on which both depth and functional voice activity can be analyzed. Individual depth profiles of manually drawn STS and functional profiles from a voice localizer (voice > non-voice) maps were extracted and compared to assess anatomo-functional correspondences. Three major results were obtained: first, the STS exhibits a highly significant rightward depth asymmetry in its middle part. Second, there is an anatomo-functional correspondence between the location of the voice-sensitive peak and the deepest point inside this asymmetrical region bilaterally. Finally, we showed that this correspondence was independent of the gender and, using a machine learning approach, that it existed at the individual level. These findings offer new perspectives for the understanding of anatomo-functional correspondences in this complex cortical region.

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
Fig. 5

Similar content being viewed by others

References

  • Allison T, Puce A, McCarthy G (2000) Social perception from visual cues: role of the STS region. Trends Cogn Sci 7(4):267–278

    Article  Google Scholar 

  • Andics A, Gacsi M, Farago T, Kis A, Miklosi A (2014) Voice-sensitive regions in the dog and human brain are revealed by comparative fMRI. Curr Biol 24(5):574–578

    Article  CAS  PubMed  Google Scholar 

  • Arhens M-M, Hasan BAS, Giordano B, Belin P (2014) Gender differences in the temporal voice areas. Front Neurosci 8:228

    Google Scholar 

  • Auzias G, Lefevre J, Le Troter A, Fischer C, Perrot M, Régis J, Coulon O (2013) Model-driven harmonic parameterization of the cortical surface: HIP-HOP. IEEE Trans Med Imaging 32(5):873–887

    Article  CAS  PubMed  Google Scholar 

  • Auzias G, Brun L, Deruelle C, Coulon O (2015) Deep sulcal landmarks: algorithmic and conceptual improvements in the definition and extraction of sulcal pits. NeuroImage 111:12–25. doi:10.1016/j.neuroimage.2015.02.008

    Article  CAS  PubMed  Google Scholar 

  • Belin P, Zatorre RJ, Lafaille P, Ahad P, Pike B (2000) Voice-selective areas in human auditory cortex. Nature 403(20):309–312

    Article  CAS  PubMed  Google Scholar 

  • Belin P, Zatorre RJ, Ahad P (2002) Human temporal-lobe response to vocal sounds. Cogn Brain Res 13:17–26

    Article  Google Scholar 

  • Blasi A, Mercure E, Lloyd-Fox S, Thomson A, Brammer M, Sauter D, Deeley Q et al (2011) Early specialization for voice and emotion processing in the infant brain. Curr Biol 21(14):1220–1224. doi:10.1016/j.cub.2011.06.009

    Article  CAS  PubMed  Google Scholar 

  • Boling W, Olivier A, Bittar RG, Reutens D (1999) Localization of hand motor activation in Broca’s Pli de Passage Moyen. J Neurosurg 91(6):903–910

    Article  CAS  PubMed  Google Scholar 

  • Bonte M, Frost MA, Rutten S, Ley A, Formisano E, Goebel R (2013) Development from childhood to adulthood increases morphological and functional inter-individual variability in the right superior temporal cortex. Neuroimage 83:739–750

    Article  PubMed  Google Scholar 

  • Brodersen KH, Ong CS, Stephan KE, Buhmann JM (2010) The balanced accuracy and its posterior distribution. In: 2010 20th international conference on pattern recognition (ICPR). IEEE, pp 3121–3124

  • Charest I, Pernet C, Latinus M, Crabbe F, Belin P (2013) Cerebral processing of voice gender studied using a continuous carryover FMRI design. Cereb Cortex 23(4):958–966

    Article  PubMed  Google Scholar 

  • Chi JG, Dooling EC, Gilles FH (1977) Gyral development of the human brain. Ann Neurol 1(1):86–93. doi:10.1002/ana.410010109

    Article  CAS  PubMed  Google Scholar 

  • Cykowski MD, Coulon O, Kochunov PV, Amunts K, Lancaster JL, Laird AR, Glahn DC, Fox PT (2008) The central sulcus: an observer-independent characterization of sulcal landmarks and depth asymmetry. Cereb Cortex 18(9):1999–2009

    Article  PubMed  Google Scholar 

  • Deen B, Koldewyn K, Kanwisher N, Saxe R (2015) Functional organization of social perception and cognition in the superior temporal sulcus. Cereb Cortex 25(11):4596–4609. doi:10.1093/cercor/bhv111

    Article  PubMed  PubMed Central  Google Scholar 

  • Dubois J, Benders M, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, Sizonenko SV, Borradori-Tolsa C, Mangin JF, Hüppi PS (2008) Mapping the early cortical folding process in the preterm newborn brain. Cereb Cortex 18(6):1444–1454. doi:10.1093/cercor/bhm180

    Article  CAS  PubMed  Google Scholar 

  • Ethofer T, Bretscher J, Gschwind M, Kreifelts B, Wildgruber D, Vuilleumier P (2012) Emotional voice areas: anatomic location, functional properties, and structural connections revealed by combined fMRI/DTI. Cereb Cortex 22(1):191–200. doi:10.1093/cercor/bhr113

    Article  PubMed  Google Scholar 

  • Glasel H, Leroy F, Dubois J, Hertz-Pannier L, Mangin JF, Dehaene-Lambertz G (2011) A robust cerebral asymmetry in the infant brain: the rightward superior temporal sulcus. Neuroimage 3(58):716–723

    Article  Google Scholar 

  • Grossmann T, Oberecker R, Koch SP, Friederici AD (2010) The developmental origins of voice processing in the human brain. Neuron 65(6):852–858. doi:10.1016/j.neuron.2010.03.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8(5):393–402. doi:10.1038/nrn2113

    Article  CAS  PubMed  Google Scholar 

  • Hopkins WD, Meguerditchian A, Coulon O, Bogard SL, Mangin JF, Sherwood CC, Grabowki MW et al (2014) Evolution of the central sulcus morphology in primates. Brain Behav Evol 84:19–30

    Article  PubMed  PubMed Central  Google Scholar 

  • Im K, Jo HJ, Mangin J-F, Evans AC, Kim SI, Lee J-M (2010) Spatial distribution of deep sulcal landmarks and hemispherical asymmetry on the cortical surface. Cereb Cortex 20(3):602–611. doi:10.1093/cercor/bhp127

    Article  PubMed  Google Scholar 

  • Kasprian G, Langs G, Brugger PC, Bittner M, W M, Arantes M, Prayer D (2011) The prenatal origin of hemispheric asymmetry: an in utero neuroimaging study. Cereb Cortex 21(5):1076–1083. doi:10.1093/cercor/bhq179

    Article  PubMed  Google Scholar 

  • Kisilevsky BS, Hains SMJ, Lee K, Xie X, Huang H, Ye HH, Zhang K, Wang Zengping (2003) Effects of experience on fetal voice recognition. Psychol Sci 14(3):220–224

    Article  PubMed  Google Scholar 

  • Kreifelts B, Ethofer T, Shiozawa T, Grodd W, Wildgruber D (2009) Cerebral representation of non-verbal emotional perception: fMRI reveals audiovisual integration area between voice- and face-sensitive regions in the superior temporal sulcus. Neuropsychologia 47(14):3059–3066. doi:10.1016/j.neuropsychologia.2009.07.001

    Article  PubMed  Google Scholar 

  • Lahnkoski JM, Glerean E, Salmi J, Jaaskelainen LP, Sams M, Hari R, Nummenmaa L (2012) Naturalistic fMRI mapping reveals superior temporal sulcus as the hub for the distributed brain network for social perception. Front Hum Neurosci 6(233). http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3417167/

  • Latinus M, McAleer P, Bestelmeyer PEG, Belin P (2013) Norm-based coding of voice identity in human auditory cortex. Curr Biol 23(12):1075–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Troter A, Rivière D, Coulon O (2011) An interactive sulcal fundi editor in BrainVisa. In: 17th international conference on human brain mapping. Organization for Human Brain Mapping

  • Leroy F, Cai Q, Bogart SL, Dubois J, Coulon O, Monzalvo K, Fischer C et al (2015) New human-specific brain landmark: the depth asymmetry of superior temporal sulcus. Proc Natl Acad Sci 112(4):1208–1213. doi:10.1073/pnas.1412389112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li G, Nie J, Wang L, Shi F, Lyall AE, Lin W, Gilmore JH, Shen D (2014) Mapping longitudinal hemispheric structural asymmetries of the human cerebral cortex from birth to 2 years of age. Cereb Cortex 24(5):1289–1300. doi:10.1093/cercor/bhs413

    Article  CAS  PubMed  Google Scholar 

  • Lohmann G, Von Cramon DY, Steinmetz H (1999) Sulcal variability of twins. Cereb Cortex 9(7):754–763. doi:10.1093/cercor/9.7.754

    Article  CAS  PubMed  Google Scholar 

  • Mangin JF, Rivière D, Cachia A, Duchesnay E, Cointepas Y, Papadopoulos-Orfanos D, Collins DL, Evans AC, Régis J (2004) Object-based morphometry of the cerebral cortex. IEEE Trans Med Imaging 23(8):968–982. doi:10.1109/TMI.2004.831204

    Article  CAS  PubMed  Google Scholar 

  • Meng Y, Li G, Lin W, Gilmore JH, Shen D (2014) Spatial distribution and longitudinal development of deep cortical sulcal landmarks in infants. NeuroImage 100(October):206–218. doi:10.1016/j.neuroimage.2014.06.004

    Article  PubMed  PubMed Central  Google Scholar 

  • Ochiai T, Grimault S, Scarvada D, Roch G, Hori T, Rivière D, Mangin J-F, Regis J (2004) Sulcal pattern and morphology of the superior temporal sulcus. Neuroimage 2(22):706–719

    Article  Google Scholar 

  • Ockleford EM, Vince MA, Layton C, Reader MR (1988) Responses of neonates to parents’ and others’ voices. Early Hum Dev 18(1):27–36

    Article  CAS  PubMed  Google Scholar 

  • Operto G, Bulot R, Anton J-L, Coulon O (2008) Projection of fMRI data onto the cortical surface using anatomically-informed convolution kernels. NeuroImage 39(1):127–135. doi:10.1016/j.neuroimage.2007.08.039

    Article  CAS  PubMed  Google Scholar 

  • Pelphrey KA, Morris JP, Michelich CR, Allison T, McCarthy G (2005) Functional anatomy of biological motion perception in posterior temporal cortex: an fMRI study of eye, mouth and hand movements. Cereb Cortex 15(12):1866–1876. doi:10.1093/cercor/bhi064

    Article  PubMed  Google Scholar 

  • Pernet CR, McAleer P, Latinus M, Gorgolewski KJ, Charest Ian, Bestelmeyer PEG, Watson RH et al (2015) The human voice areas: spatial organization and inter-individual variability in temporal and extra-temporal cortices. NeuroImage 119:164–174. doi:10.1016/j.neuroimage.2015.06.050

    Article  PubMed  PubMed Central  Google Scholar 

  • Petkov CI, Kayser C, Steudel T, Whittingstall K, Augath M, Logothetis NK (2008) A voice region in the monkey brain. Nat Neurosci 11:367–374

    Article  CAS  PubMed  Google Scholar 

  • Rettmann ME, Han X, Chenyang X, Prince JL (2002) Automated sulcal segmentation using watersheds on the cortical surface. NeuroImage 15(2):329–344. doi:10.1006/nimg.2001.0975

    Article  PubMed  Google Scholar 

  • Ronan L, Fletcher PC (2015) From genes to folds: a review of cortical gyrification theory. Brain Struct Funct 220(5):2475–2483. doi:10.1007/s00429-014-0961-z

    Article  CAS  PubMed  Google Scholar 

  • Sadagopan S, Temiz-Karayol NZ, Voss HU (2015) High-field functional magnetic resonance imaging of vocalization processing in marmosets. Sci Rep 5(June):10950. doi:10.1038/srep10950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sastre-Janer FA, Regis J, Belin P, Mangin JF, Dormont D, Masure MC, Remy P, Frouin V, Samson Y (1998) Three-dimensional reconstruction of the human central sulcus reveals a morphological correlate of the hand area. Cereb Cortex 8(7):641–647

    Article  CAS  PubMed  Google Scholar 

  • Sun ZY, Pinel P, Rivière D, Moreno A, Dehaene S, Mangin J-F (2015) Linking morphological and functional variability in hand movement and silent reading. Brain Struct Funct. doi:10.1007/s00429-015-1106-8

    Google Scholar 

  • Van Essen DC (2005) A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. NeuroImage 28(3):635–662. doi:10.1016/j.neuroimage.2005.06.058

    Article  PubMed  Google Scholar 

  • Weiner KS, Golarai G, Caspers J, Chuapoco MR, Mohlberg H, Zilles K, Amunts K, Grill-Spector K (2014) The mid-fusiform sulcus: a landmark identifying both cytoarchitectonic and functional divisions of human ventral temporal cortex. Neuroimage 84:453–465

    Article  PubMed  Google Scholar 

  • Xu G, Knutsen AK, Dikranian K, Kroenke CD, Bayly PV, Taber LA (2010) Axons pull on the brain, but tension does not drive cortical folding. J Biomech Eng 132(7):71013. doi:10.1115/1.4001683

    Article  Google Scholar 

  • Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P (1997) Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120(1):141–157

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the support of Grant AJE201214 by the Fondation pour la Recherche Médicale (France) to P.B, and of Labex BLRI (Aix-Marseille Universtité, France) to CB. Research supported by Grants ANR-16-CONV-0002 (ILCB), ANR-11-LABX-0036 (BLRI) and ANR-11-IDEX-0001-02 (A*MIDEX).

Author information

Authors and Affiliations

  1. Institut de Neurosciences de la Timone, CNRS UMR7289, Aix-Marseille Université, Marseille, France

    C. Bodin, S. Takerkart, P. Belin & O. Coulon

  2. Institute for Language, Communication and the Brain, Aix-Marseille Université, Marseille, France

    C. Bodin, P. Belin & O. Coulon

  3. Centre for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, UK

    P. Belin

  4. International Laboratories for Brain, Music and Sound, Department of Psychology, University of Montréal, McGill University, Montreal, QC, Canada

    P. Belin

Authors
  1. C. Bodin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Takerkart
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Belin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. Coulon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Bodin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

429_2017_1483_MOESM1_ESM.png

Figure A: All > Silence contrast analysis. Top panel: Averaged surface-based functional maps of the All > silence contrast projected on the HipHop138 template for the left (L) and right (R) hemisphere. The color bar indicates the mean t value of the functional activity. Lower panel: Anatomical (black dotted line) and functional averaged profiles (blue line for upper profile and green line for lower profile (± SEM)) were represented together with the STAP region (orange overlay). The stars line indicates the significant upper-lower differences along the STS (Mann–Whitney, p < 0.05 Bonferroni corrected). (PNG 494 kb)

429_2017_1483_MOESM2_ESM.png

Figure B: Effect of the integration distance on the anatomo-functional correspondence. Functional averaged profiles were computed with different distances of integration from the STS fundus (from 5 to 30 mm), represented by the different colored lines. STS depth (right vertical axis) was also plotted in order to see the anatomo-functional correspondence. Observation of functional curves of the right hemisphere indicates that functional activity is maximal around 25 mm from the sulcal fundus both for the upper and lower banks of the STS. This corresponds to the maximal depth of the STS in this same region, meaning that functional peaks are located on the top of the STS banks, i.e., STG and MTG on the right hemisphere. On the left hemisphere, functional activity is maximal around 25 mm on the upper bank, and around 5 mm on the lower bank. Given that sulcal depth doesn’t exceed 15 mm in this region, the maximal activity is located on the STG and beyond, and also near the sulcal fundus on the left hemisphere. This is in agreement with maps on Fig. 3. The distance (25 mm) chosen in this paper was represented by a thicker blue line. This distance was chosen because it captured the entire functional information in both hemispheres: from 5 to 25 mm the functional activity is increasing, but from 25 to 30 mm no such addition is noticed. Lupper: left upper functional profile; Llower: left lower functional profile; Rupper: right upper functional profile; Rlower: right lower functional profile. MTG: middle temporal gyrus; STG: superior temporal gyrus. (PNG 72 kb)

429_2017_1483_MOESM3_ESM.png

Figure C: Flow chart summarizing how many subjects was analyzed for each stage of the procedure (A, B, C). From the initial 116 subjects, two subjects were removed because of a segmentation problem that was specific to their images and 19 were removed due to a failure of the profile extraction algorithm that met complex triangle configurations on the cortical surface mesh. Amongst the 95 subjects left, 21 were discarded during functional profile extraction. This problem was due to a memory leak in the HipHop process (BrainVisa 4.5), that was used to compute the orthogonal direction to the sulcus (page 8 in the manuscript), and had no consequence on the quality of the results for remaining subjects. Both problems occurred most of the time on only one of the two hemispheres of each subject, but such subjects had to be entirely discarded of the analysis in order to keep a consistent set with no missing data. (PNG 92 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bodin, C., Takerkart, S., Belin, P. et al. Anatomo-functional correspondence in the superior temporal sulcus. Brain Struct Funct 223, 221–232 (2018). https://doi.org/10.1007/s00429-017-1483-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-017-1483-2

Keywords

Search

Navigation