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Variations of planum temporale asymmetries with Heschl’s Gyri duplications and association with cognitive abilities: MRI investigation of 428 healthy volunteers

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Abstract

In a large sample of 428 healthy adults balanced for gender and manual preference (MP), we investigated planum temporale (PT) surface area variability in relation with Heschl’s gyrus (HG) duplication pattern, MP, and familial sinistrality (FS), considering different PT definitions. In a sub-sample of 362 participants, we also investigated whether variability of PT asymmetry was associated with differences in verbal abilities. On each participant brain hemisphere MRI, we delineated a posterior PT area (PTpost), excluding the second Heschl gyrus in case of either complete posterior duplication (CPD) or common stem partial duplication (CSD). We then defined a total PT area (PTtot) as the union of PTpost and of the second HG when present, and a HGPT area as the union of PTtot and of the first HG. The HG duplication pattern of one hemisphere was found to significantly affect the PTpost surface area of the same hemisphere, a larger reduction being present in case of CPD than in case of CSD, leading to a strong impact of both left and right HG duplication patterns on PTpost asymmetry. The HG duplication pattern had no effect on PTtot surface areas, while a significant effect of the left HG duplication was present on PTtot asymmetry that was larger in case of a CSD as compared to a single HG. By contrast, the type of HG duplication did not affect HGPT and neither left nor right HG duplication pattern had an effect on HGPT asymmetry. Meanwhile, MP had no effect on PTpost, PTtot, HGPT, or their asymmetries. The absence of a left PTpost was associated with existence of FS (FS+) (7FS+ among nine without PTpost). Removing the nine individuals lacking PTpost, a lower left PTpost surface area was observed in FS+ participants with left CPD. In the sub-sample of 362 participants, we observed a significant interaction between PTpost asymmetry and cognitive abilities due to poorer lexical performances in individuals having a symmetric PTpost as compared to individuals having either a leftward or a rightward asymmetric PTpost. By contrast, there was no significant effect of PTtot or HGPT asymmetry on cognitive abilities. This study shows that HG duplication pattern mainly affects the surface area of the most posterior part of PT and its asymmetry, this PTpost area being specifically associated with variability in verbal performances. This study also shows, for the first time, an association between decreased performances and lack of PTpost anatomical asymmetry, being rightward asymmetrical having no deleterious effect on verbal abilities, thereby supporting the idea that anatomical lateralization is necessary for optimal verbal performances.

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References

  • Abdul-Kareem IA, Sluming V (2008) Heschl gyrus and its included primary auditory cortex: structural MRI studies in healthy and diseased subjects. J Magn Reson Imaging 28:287–299

    Article  PubMed  Google Scholar 

  • Altarelli I, Leroy F, Monzalvo K, Fluss J, Billard C, Dehaene-Lambertz G, Galaburda AM, Ramus F (2014) Planum temporale asymmetry in developmental dyslexia: revisiting an old question. Hum Brain Mapp 35:5717–5735

  • Baddeley A, Cocchini G, DellaSala S, Logie RH, Spinnler H (1999) Working memory and vigilance: evidence from normal aging and Alzheimer’s disease. Brain Cogn 41:87–108

    Article  CAS  PubMed  Google Scholar 

  • Barrick TR, Mackay CE, Prima S, Maes F, Vandermeulen D, Crow TJ, Roberts N (2005) Automatic analysis of cerebral asymmetry: an exploratory study of the relationship between brain torque and planum temporale asymmetry. Neuroimage 24:678–691

    Article  PubMed  Google Scholar 

  • Bhojraj TS, Francis AN, Rajarethinam R, Eack S, Kulkarni S, Prasad KM, Montrose DM, Dworakowski D, Diwadkar V, Keshavan MS (2009) Verbal fluency deficits and altered lateralization of language brain areas in individuals genetically predisposed to schizophrenia. Schizophr Res 115:202–208

    Article  PubMed  PubMed Central  Google Scholar 

  • Binois DR, Pichot DP (1956) Test de vocabulaire: manuel d’application. Editions du Centre de psychologie appliquée

  • Bishop DVM (2013) Cerebral asymmetry and language development: cause, correlate, or consequence? Science 340:1230531

    Article  PubMed  PubMed Central  Google Scholar 

  • Bishop DV, Holt G, Whitehouse AJ, Groen M (2014) No population bias to left-hemisphere language in 4-year-olds with language impairment. PeerJ 2:e507

    Article  PubMed  PubMed Central  Google Scholar 

  • Bloom JS, Garcia-Barrera MA, Miller CJ, Miller SR, Hynd GW (2013) Planum temporale morphology in children with developmental dyslexia. Neuropsychologia 51:1684–1692

    Article  PubMed  PubMed Central  Google Scholar 

  • Da Costa S, van der Zwaag W, Marques JP, Frackowiak RS, Clarke S, Saenz M (2011a) Human primary auditory cortex follows the shape of Heschl’s Gyrus. J Neurosci 31:14067–14075

  • Da Costa S, van der Zwaag W, Marques JP, Frackowiak RS, Clarke S, Saenz M (2011b) Human primary auditory cortex follows the shape of Heschl’s Gyrus. J Neurosci 31:14067–14075

  • Dalby MA, Elbro C, Stødkilde-Jørgensen H (1998) Temporal lobe asymmetry and dyslexia: Anin Vivostudy using MRI. Brain Lang 62:51–69

    Article  CAS  PubMed  Google Scholar 

  • Daneman M, Carpenter PA (1980) individual differences in working memory and reading. J Verb Learn Verb Behav 19:450–466

    Article  Google Scholar 

  • Desmette D, Hupet M, Schelstraete MA, Van der Linden M (1995) Adaptation en langue française du “Reading Span Test” de Daneman et Carpenter (1980). L’année Psychol 95:459–482

    Article  Google Scholar 

  • Diallo B, Dolidon F, Travere J-, Mazoyer B (1998) VoxeLine: a software for 3D real-time visualization of biomedical images. Comput Med Imaging Graph 22:275–289

    Article  CAS  PubMed  Google Scholar 

  • Galaburda A, Sanides F (1980) Cytoarchitectonic organization of the human auditory cortex. J Comp Neurol 190:597–610

    Article  CAS  PubMed  Google Scholar 

  • Galaburda AM, Sanides F, Geschwind N (1978) Human brain. Cytoarchitectonic left-right asymmetries in the temporal speech region. Arch Neurol 35:812–817

    Article  CAS  PubMed  Google Scholar 

  • Galaburda AM, Corsiglia J, Rosen GD, Sherman GF (1987) Planum temporale asymmetry, reappraisal since Geshwind and Levitsky. Neuropsychologia 25:853–868

    Article  Google Scholar 

  • Geschwind N, Levitsky W (1968) Human brain left-right asymmetries in temporal speech region. Science 161:186–187

    Article  CAS  PubMed  Google Scholar 

  • Golestani N, Pallier C (2007) Anatomical correlates of foreign speech sound production. Cereb Cortex 17:929–934

    Article  PubMed  Google Scholar 

  • Golestani N, Molko N, Dehaene S, LeBihan D, Pallier C (2007) Brain structure predicts the learning of foreign speech sounds. Cereb Cortex 17:575–582

    Article  PubMed  Google Scholar 

  • Golestani N, Price CJ, Scott SK (2011) Born with an ear for dialects? Structural plasticity in the expert phonetician brain. J Neurosci 31:4213–4220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guadalupe T, Willems RM, Zwiers MP, Arias Vasquez A, Hoogman M, Hagoort P, Fernandez G, Buitelaar J, Franke B, Fisher SE, Francks C (2014a) Differences in cerebral cortical anatomy of left- and right-handers. Front Psychol 5

  • Guadalupe T, Zwiers MP, Wittfeld K, Teumer A, Vasquez AA, Hoogman M, Hagoort P, Fernandez G, Buitelaar J, van Bokhoven H, Hegenscheid K, Völzke H, Franke B, Fisher SE, Grabe HJ, Francks C (2014b) Asymmetry within and around the human planum temporale is sexually dimorphic and influenced by genes involved in steroid hormone receptor activity. Cortex

  • Habas PA, Scott JA, Roosta A, Rajagopalan V, Kim K, Rousseau F, Barkovich AJ, Glenn OA, Studholme C (2012) Early folding patterns and asymmetries of the normal human brain detected from in utero MRI. Cereb Cortex 22:13–25

    Article  PubMed  Google Scholar 

  • Heiervang E, Hugdahl K, Steinmetz H, Inge SA, Stevenson J, Lund A, Ersland L, Lundervold A (2000) Planum temporale, planum parietale and dichotic listening in dyslexia. Neuropsychologia 38:1704–1713

    Article  CAS  PubMed  Google Scholar 

  • Hill J, Dierker D, Neil J, Inder T, Knutsen A, Harwell J, Coalson T, Van Essen D (2010) A surface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human infants. J Neurosci 30:2268–2276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isenberg AL, Vaden KI, Saberi K, Muftuler LT, Hickok G (2012) Functionally distinct regions for spatial processing and sensory motor integration in the planum temporale. Hum Brain Mapp 33:2453–2463

    Article  PubMed  Google Scholar 

  • Jäncke L, Steinmetz H (1993) Auditory lateralization and planum temporale asymmetry. Neuroreport 5:169–172

    Article  PubMed  Google Scholar 

  • Jäncke L, Schlaug G, Huang Y, Steinmetz H (1994) Asymmetry of the planum parietale. Neuroreport 5:1161–1163

    Article  PubMed  Google Scholar 

  • Kibby MY, Kroese JM, Morgan AE, Hiemenz JR, Cohen MJ, Hynd GW (2004) The relationship between perisylvian morphology and verbal short-term memory functioning in children with neurodevelopmental disorders. Brain Lang 89:122–135

    Article  PubMed  Google Scholar 

  • Kulynych JJ, Vladar K, Jones DW, Weinberger DR (1993) Three-dimentional surface rendering in MRI morphometry: a study of the planum temporale. J Comput Assist Tomogr 17:529–535

    Article  CAS  PubMed  Google Scholar 

  • Kushch A, Gross-Glenn K, Jallad B, Lubs H, Rabin M, Feldman E, Duara R (1993) Temporal lobe surface area measurements on MRI in normal and dyslexic readers. Neuropsychologia 31:811–821

    Article  CAS  PubMed  Google Scholar 

  • Leask SJ, Crow TJ (1997) How far does the brain lateralize?: an unbiased method for determining the optimum degree of hemispheric specialization. Neuropsychologia 35:1381–1387

    Article  CAS  PubMed  Google Scholar 

  • Leff AP, Schofield TM, Crinion JT, Seghier ML, Grogan A, Green DW, Price CJ (2009) The left superior temporal gyrus is a shared substrate for auditory short-term memory and speech comprehension: evidence from 210 patients with stroke. Brain 132:3401–3410

    Article  PubMed  PubMed Central  Google Scholar 

  • Leonard CM, Eckert MA (2008) Asymmetry and dyslexia. Dev Neuropsychol 33:663–681

    Article  PubMed  PubMed Central  Google Scholar 

  • Leonard CM, Puranik C, Kuldau JM, Lombardino LJ (1998) Normal variation in the frequency and location of human auditory cortex landmarks. Heschl’s gyrus: where is it? Cereb Cortex 8:397–406

    Article  CAS  PubMed  Google Scholar 

  • Leonard CM, Eckert MA, Lombardino LJ, Oakland T, Kranzler J, Mohr CM, King WM, Freeman A (2001) Anatomical risk factors for phonological dyslexia. Cereb Cortex 11:148–157

    Article  CAS  PubMed  Google Scholar 

  • Leonard CM, Lombardino LJ, Walsh K, Eckert MA, Mockler JL, Rowe LA, Williams S, DeBose CB (2002) Anatomical risk factors that distinguish dyslexia from SLI predict reading skill in normal children. J Commun Disord 35:501–531

    Article  PubMed  Google Scholar 

  • Ma Y, Koyama MS, Milham MP, Castellanos FX, Quinn BT, Pardoe H, Wang X, Kuzniecky R, Devinsky O, Thesen T, Blackmon K (2015) Cortical thickness abnormalities associated with dyslexia, independent of remediation status. Neuroimage Clin 7:177–186

    Article  PubMed  Google Scholar 

  • Marie D, Jobard G, Crivello F, Perchey G, Petit L, Mellet E, Joliot M, Zago L, Mazoyer B, Tzourio-Mazoyer N (2015) Descriptive anatomy of Heschl’s gyri in 430 healthy volunteers, including 198 left-handers. Brain Struct Funct 220:729–743

    Article  CAS  PubMed  Google Scholar 

  • Mazoyer BM, Tzourio-Mazoyer NG (2004) Planum temporale asymmetry and models of dominance for language: a reappraisal. Neuroreport 15:1057–1059

    Article  PubMed  Google Scholar 

  • Mazoyer B, Mellet E, Perchey G, Zago L, Crivello F, Jobard G, Delcroix N, Vigneau M, Leroux G, Petit L, Joliot M, Tzourio-Mazoyer N (2015) BIL&GIN: A neuroimaging, cognitive, behavioral, and genetic database for the study of human brain lateralization. Neuroimage 124:1225–1231

    Article  PubMed  Google Scholar 

  • McGettigan C, Warren JE, Eisner F, Marshall CR, Shanmugalingam P, Scott SK (2011) Neural correlates of sublexical processing in phonological working memory. J Cogn Neurosci 23:961–977

    Article  PubMed  Google Scholar 

  • Mellet E, Jobard G, Zago L, Crivello F, Petit L, Joliot M, Mazoyer B, Tzourio-Mazoyer N (2013) Relationships between hand laterality and verbal and spatial skills in 436 healthy adults balanced for handedness. Laterality 19:1–22

    Google Scholar 

  • Mellet E, Zago L, Jobard G, Crivello F, Petit L, Joliot M, Mazoyer B, Tzourio-Mazoyer N (2014) Weak language lateralization affects both verbal and spatial skills: an fMRI study in 297 subjects. Neuropsychologia 65:56–62

    Article  CAS  PubMed  Google Scholar 

  • Moffat SD, Hampson E, Lee DH (1998) Morphology of the planum temporale and corpus callosum in left handers with evidence of left and right hemisphere speech representation. Brain 121:2369–2379

    Article  PubMed  Google Scholar 

  • Morgan AE, Hynd GW (1998) Dyslexia, neurolinguistic ability, and anatomical variation of the planum temporale. Neuropsychol Rev 8:79–93

    Article  CAS  PubMed  Google Scholar 

  • Penhune VB, Zatorre RJ, MacDonald JD, Evans AC (1996) Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex 6:661–672

    Article  CAS  PubMed  Google Scholar 

  • Pillay SB, Stengel BC, Humphries C, Book DS, Binder JR (2014) Cerebral localization of impaired phonological retrieval during rhyme judgment. Ann Neurol 76:738–746

    Article  PubMed  PubMed Central  Google Scholar 

  • Rademacher J, Caviness VS, Steinmetz H, Galaburda AM (1993) Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. Cereb Cortex 3:313–329

    Article  CAS  PubMed  Google Scholar 

  • Raven JC (1960) Guide to the standard progressive matrices: sets A, B, C, D and E. HK Lewis, London

    Google Scholar 

  • Rey A (1958) L’examen clinique en psychologie. Presses Universitaires De France

  • Rosen GD, Sherman GF, Galaburda AM (1992) Biological substrates of anatomic asymmetry. Prog Neurobiol 39:507–515

    Article  CAS  PubMed  Google Scholar 

  • Schneider P, Scherg M, Dosch HG, Specht HJ, Gutschalk A, Rupp A (2002) Morphology of Heschl’s gyrus reflects enhanced activation in the auditory cortex of musicians. Nat Neurosci 5:688–694

    Article  CAS  PubMed  Google Scholar 

  • Schneider P, Sluming V, Roberts N, Scherg M, Goebel R, Specht HJ, Dosch HG, Bleeck S, Stippich C, Rupp A (2005) Structural and functional asymmetry of lateral Heschl’s gyrus reflects pitch perception preference. Nat Neurosci 8:1241–1247

    Article  CAS  PubMed  Google Scholar 

  • Shapleske J, Rossell SL, Woodruff PW, David AS (1999a) The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Rev 29:26–49

  • Simmonds AJ, Leech R, Collins C, Redjep O, Wise RJ (2014) Sensory-motor integration during speech production localizes to both left and right plana temporale. J Neurosci 34:12963–12972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinmetz H, Rademacher J, Huang Y, Hefter H, Zilles K, Thron A, Freund H (1989) Cerebral asymmetry: MR planimetry of the human planum temporale. J Comput Assist Tomogr 13:996–1005

    Article  CAS  PubMed  Google Scholar 

  • Steinmetz H, Rademacher J, Jäncke L, Huang Y, Thron A, Zilles K (1990) Total surface of temporoparietal intrasylvian cortex: diverging left-right asymmetries. Brain Lang 39:357–372

    Article  CAS  PubMed  Google Scholar 

  • Steinmetz H, Volkmann J, Jäncke L, Freund H (1991) Anatomical left-right asymmetry of language-related temporal cortex is different in left- and right-handers. Ann Neurol 29:315–319

    Article  CAS  PubMed  Google Scholar 

  • Teszner D, Tzavaras A, Gruner J, Hecaen H (1972) L’asymetrie droite-gauche du planum temporale; a propos de l’etude anatomique de 100 cerveaux. Rev Neurol (Paris) 126:444–449

    CAS  Google Scholar 

  • Tremblay P, Deschamps I, Gracco VL (2011) Regional heterogeneity in the processing and the production of speech in the human planum temporale. Cortex

  • Tzourio-Mazoyer N, Simon G, Crivello F, Jobard G, Zago L, Perchey G, Hervé PY, Joliot M, Petit L, Mellet E, Mazoyer B (2010) Effect of familial sinistrality on planum temporale surface and brain tissue asymmetries. Cereb Cortex 20:1476–1485

    Article  PubMed  Google Scholar 

  • Tzourio-Mazoyer N, Perrone-Bertolotti M, Jobard G, Mazoyer B, Baciu M (2016) Multi-factorial modulation of hemispheric specialization and plasticity for language in healthy and pathological conditions: a review. Cortex

  • Vandenberg S, Kuse A (1978) Mental rotations, a group test of three-dimensional spatial visualization. Percept Mot Skills 47:599–604

    Article  CAS  PubMed  Google Scholar 

  • Warrier C, Wong P, Penhune V, Zatorre R, Parrish T, Abrams D, Kraus N (2009) Relating structure to function: Heschl’s gyrus and acoustic processing. J Neurosci 29:61–69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia Z, Hoeft F, Zhang L, Shu H (2016) Neuroanatomical anomalies of dyslexia: disambiguating the effects of disorder, performance, and maturation. Neuropsychologia 81:68–78

    Article  PubMed  Google Scholar 

  • Zatorre RJ (2013) Predispositions and plasticity in music and speech learning: neural correlates and implications. Science 342:585–589

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Fabrice Crivello, Gael Jobard, Marc Joliot, Emmanuel Mellet, Guy Perchey, Laurent Petit, Mathieu Vigneau, and Laure Zago for their contribution to the BIL&GIN conception, acquisition, and/or analysis, and Fabrice Crivello and Emmanuel Mellet for their in-depth reading of the manuscript and thoughtful comments.

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Tzourio-Mazoyer, N., Mazoyer, B. Variations of planum temporale asymmetries with Heschl’s Gyri duplications and association with cognitive abilities: MRI investigation of 428 healthy volunteers. Brain Struct Funct 222, 2711–2726 (2017). https://doi.org/10.1007/s00429-017-1367-5

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