Duplicated Heschl's gyrus associations with phonological decoding.

Heschl’s Gyrus Phonological decoding Sulcal/Gyral variability Template-matching

Journal

Brain structure & function

ISSN: 1863-2661

Titre abrégé: Brain Struct Funct

Pays: Germany

ID NLM: 101282001

Informations de publication

Date de publication:
16 Jul 2024

Historique:

received: 08 10 2023

accepted: 06 07 2024

medline: 16 7 2024

pubmed: 16 7 2024

entrez: 16 7 2024

Statut: aheadofprint

Résumé

The reason(s) for why a complete duplication of the left hemisphere Heschl's gyrus (HG) has been observed in people with reading disability are unclear. This study was designed to replicate and advance understanding of the HG and phonological decoding association, as well as test competing hypotheses that this HG duplication association is specifically localized to the HG or could be due to co-occurring atypical development of other brain regions that support reading and language development. Participants were selected on the basis of having a duplicated left hemisphere HG (N = 96) or a single HG (N = 96) and matched according to age, sex, and research site in this multi-site study. Duplicated and single HG morphology specific templates were created to determine the extent to which HG sizes were related to phonological decoding within each HG morphology group. The duplicated HG group had significantly lower phonological decoding (F = 4.48, p = 0.04) but not verbal IQ (F = 1.39, p = 0.41) compared to the single HG group. In addition, larger HG were significantly associated with lower phonological decoding in the duplicated HG group, with effects driven by the size of the lateral HG after controlling for age, sex, research site, and handedness (ps < 0.05). Brain regions that exhibited structural covariance with HG did not clearly explain the HG and phonological decoding associations. Together, the results suggest that presence of a duplicated HG indicates some risk for lower phonological decoding ability compared to verbal IQ, but the reason(s) for this association remain unclear.

Identifiants

DOI: 10.1007/s00429-024-02831-2 PMID: 39012481

pubmed: 39012481

doi: 10.1007/s00429-024-02831-2

pii: 10.1007/s00429-024-02831-2

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Informations de copyright

Références

Alotaibi S, Alsaleh A, Wuerger S, Meyer G (2023) Rapid neural changes during novel speech-sound learning: an fMRI and DTI study. Brain Lang 245:105324. https://doi.org/10.1016/j.bandl.2023.105324

doi: 10.1016/j.bandl.2023.105324 pubmed: 37741162

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(12):5717–5735. https://doi.org/10.1002/hbm.22579

doi: 10.1002/hbm.22579 pubmed: 25044828 pmcid: 6869664

Andoh J, Matsushita R, Zatorre RJ (2015) Asymmetric interhemispheric transfer in the auditory network: evidence from TMS, resting-state fMRI, and diffusion imaging. J Neurosci 35(43):14602–14611. https://doi.org/10.1523/JNEUROSCI.2333-15.2015

doi: 10.1523/JNEUROSCI.2333-15.2015 pubmed: 26511249 pmcid: 6605461

Ashburner J (2009) Computational anatomy with the SPM software. Magn Reson Imaging 27(8):1163–1174. https://doi.org/10.1016/j.mri.2009.01.006

doi: 10.1016/j.mri.2009.01.006 pubmed: 19249168

Avants BB, Tustison N, Song G (2009) Advanced normalization tools (ANTS). Insight j 2(365):1–35

Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Phil Trans R Soc B 360(1457):1001–1013. https://doi.org/10.1098/rstb.2005.1634

doi: 10.1098/rstb.2005.1634 pubmed: 16087444 pmcid: 1854918

Beer AL, Plank T, Greenlee MW (2011) Diffusion tensor imaging shows white matter tracts between human auditory and visual cortex. Exp Brain Res 213:299–308. https://doi.org/10.1007/s00221-011-2715-y

doi: 10.1007/s00221-011-2715-y pubmed: 21573953

Benner J, Wengenroth M, Reinhardt J, Stippich C, Schneider P, Blatow M (2017) Prevalence and function of Heschl’s gyrus morphotypes in musicians. Brain Struct Funct 222(8):3587–3603. https://doi.org/10.1007/s00429-017-1419-x

doi: 10.1007/s00429-017-1419-x pubmed: 28397108

Berke JJ (1960) The claustrum, the external capsule and the extreme capsule of Macaca mulatta. J Comp Neurol 115(3):297–331. https://doi.org/10.1002/cne.901150304

doi: 10.1002/cne.901150304 pubmed: 26827384

Bishop-Liebler P, Welch G, Huss M, Thomson JM, Goswami U (2014) Auditory temporal processing skills in musicians with dyslexia. Dyslexia 20(3):261–279. https://doi.org/10.1002/dys.1479

doi: 10.1002/dys.1479 pubmed: 25044949

Blau V, van Atteveldt N, Ekkebus M, Goebel R, Blomert L (2009) Reduced neural integration of letters and speech sounds links phonological and reading deficits in adult dyslexia. Curr Biol 19(6):503–508. https://doi.org/10.1002/dys.1479

doi: 10.1002/dys.1479 pubmed: 19285401

Booth JR, Mehdiratta N, Burman DD, Bitan T (2008) Developmental increases in effective connectivity to brain regions involved in phonological processing during tasks with orthographic demands. Brain Res 1189:78–89. https://doi.org/10.1016/j.brainres.2007.10.080

doi: 10.1016/j.brainres.2007.10.080 pubmed: 18068690

Brett M, Anton JL, Valabregue R, Poline JB (2002) Region of interest analysis using the MarsBar toolbox for SPM 99. NeuroImage 16(2):S497

Church JA, Coalson RS, Lugar HM, Petersen SE, Schlaggar BL (2008) A developmental fMRI study of reading and repetition reveals changes in phonological and visual mechanisms over age. Cereb Cortex 18(9):2054–2065. https://doi.org/10.1093/cercor/bhm228

doi: 10.1093/cercor/bhm228 pubmed: 18245043 pmcid: 2517103

Da Costa S, van der Zwaag W, Marques JP, Frackowiak RS, Clarke S, Saenz M (2011) Human primary auditory cortex follows the shape of Heschl’s gyrus. J Neurosci 31(40):14067–14075. https://doi.org/10.1523/JNEUROSCI.2000-11.2011

doi: 10.1523/JNEUROSCI.2000-11.2011 pubmed: 21976491 pmcid: 6623669

Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Nat Acad Sci 103(37):13848–13853. https://doi.org/10.1073/pnas.0601417103

doi: 10.1073/pnas.0601417103 pubmed: 16945915 pmcid: 1564249

Dick AS, Tremblay P (2012) Beyond the arcuate fasciculus: Consensus and controversy in the connectional anatomy of language. Brain 135(12):3529–3550. https://doi.org/10.1093/brain/aws222

doi: 10.1093/brain/aws222 pubmed: 23107648

Eckert MA, Lombardino LJ, Leonard CM (2001) Planar asymmetry tips the phonological playground and environment raises the bar. Child Dev 72(4):988–1002. https://doi.org/10.1111/1467-8624.00330

doi: 10.1111/1467-8624.00330 pubmed: 11480950

Eckert MA, Leonard CM, Molloy EA, Blumenthal J, Zijdenbos A, Giedd JN (2002) The epigenesis of planum temporale asymmetry in twins. Cereb Cortex 12(7):749–755. https://doi.org/10.1093/cercor/12.7.749

doi: 10.1093/cercor/12.7.749 pubmed: 12050086

Eckert MA, Leonard CM, Richards TL, Aylward EH, Thomson J, Berninger VW (2003) Anatomical correlates of dyslexia: frontal and cerebellar findings. Brain 126(2):482–494. https://doi.org/10.1093/brain/awg026

doi: 10.1093/brain/awg026 pubmed: 12538414

Eckert MA, Kamdar NV, Chang CE, Beckmann CF, Greicius MD, Menon V (2008) A cross-modal system linking primary auditory and visual cortices: evidence from intrinsic fMRI connectivity analysis. Hum Brain Mapp 29(7):848–857. https://doi.org/10.1002/hbm.20560

doi: 10.1002/hbm.20560 pubmed: 18412133 pmcid: 2605422

Eckert MA, Vaden KI Jr., Dyslexia Data Consortium (2019) A deformation-based approach for characterizing brain asymmetries at different spatial scales of resolution. J Neurosci Meth 322:1–9. https://doi.org/10.1016/j.jneumeth.2019.04.007

doi: 10.1016/j.jneumeth.2019.04.007

Eckert MA, Vaden KI Jr., Iuricich F, Dyslexia Data Consortium (2022) Cortical asymmetries at different spatial hierarchies relate to phonological processing ability. PLoS Biol 20(4):e3001591. https://doi.org/10.1371/journal.pbio.3001591

doi: 10.1371/journal.pbio.3001591 pubmed: 35381012 pmcid: 8982829

Falchier A, Clavagnier S, Barone P, Kennedy H (2002) Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci 22(13):5749–5759. https://doi.org/10.1523/JNEUROSCI.22-13-05749.2002

doi: 10.1523/JNEUROSCI.22-13-05749.2002 pubmed: 12097528 pmcid: 6758216

Gaser C, Dahnke R, Thompson PM, Kurth F, Luders E, Alzheimer’s Disease Neuroimaging Initiative (2022) CAT–A computational anatomy toolbox for the analysis of structural MRI data. biorxiv:2022.2006. 2011.495736

Golestani N, Zatorre RJ (2004) Learning new sounds of speech: reallocation of neural substrates. NeuroImage 21(2):494–506. https://doi.org/10.1016/j.neuroimage.2003.09.071

doi: 10.1016/j.neuroimage.2003.09.071 pubmed: 14980552

Golestani N, Molko N, Dehaene S, LeBihan D, Pallier C (2007) Brain structure predicts the learning of foreign speech sounds. Cereb Cortex 17(3):575–582. https://doi.org/10.1093/cercor/bhk001

doi: 10.1093/cercor/bhk001 pubmed: 16603709

Golestani N, Price CJ, Scott SK (2011) Born with an ear for dialects? Structural plasticity in the expert phonetician brain. J Neurosci 31(11):4213–4220. https://doi.org/10.1523/JNEUROSCI.3891-10.2011

doi: 10.1523/JNEUROSCI.3891-10.2011 pubmed: 21411662 pmcid: 3108888

Green R, Hutsler J, Loftus W, Tramo M, Thomas C, Silberfarb A, Nordgren R, Nordgren R, Gazzaniga M (1999) The caudal infrasylvian surface in dyslexia: Novel magnetic resonance imaging–based findings. Neurology 53(5):974–974. https://doi.org/10.1212/wnl.53.5.974

doi: 10.1212/wnl.53.5.974 pubmed: 10496255

Hackett TA, Preuss TM, Kaas JH (2001) Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. J Comp Neurol 441(3):197–222. https://doi.org/10.1002/cne.1407

doi: 10.1002/cne.1407 pubmed: 11745645

Hämäläinen J, Leppänen P, Guttorm T, Lyytinen H (2007) N1 and P2 components of auditory event-related potentials in children with and without reading disabilities. Clin Neurophysiol 118(10):2263–2275. https://doi.org/10.1016/j.clinph.2007.07.007

doi: 10.1016/j.clinph.2007.07.007 pubmed: 17714985

Hertrich I, Dietrich S, Ackermann H (2011) Cross-modal interactions during perception of audiovisual speech and nonspeech signals: an fMRI study. J Cog Neurosci 23(1):221–237. https://doi.org/10.1162/jocn.2010.21421

doi: 10.1162/jocn.2010.21421

Leonard CM, Eckert MA (2008) Asymmetry and dyslexia. Dev Neuropsychol 33(6):663–681. https://doi.org/10.1080/87565640802418597

doi: 10.1080/87565640802418597 pubmed: 19005910 pmcid: 2586924

Leonard CM, Voeller KK, Lombardino LJ, Morris MK, Hynd GW, Alexander AW, Andersen HG, Garofalakis M, Honeyman JC, Mao J (1993) Anomalous cerebral structure in dyslexia revealed with magnetic resonance imaging. Arch Neurol 50(5):461–469. https://doi.org/10.1001/archneur.1993.00540050013008

doi: 10.1001/archneur.1993.00540050013008 pubmed: 8489401

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(5):397–406. https://doi.org/10.1093/cercor/8.5.397

doi: 10.1093/cercor/8.5.397 pubmed: 9722083

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(2):148–157. https://doi.org/10.1093/cercor/11.2.148

doi: 10.1093/cercor/11.2.148 pubmed: 11208669

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 Dis 35(6):501–531. https://doi.org/10.1016/s0021-9924(02)00120-x

doi: 10.1016/s0021-9924(02)00120-x

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(2):729–743. https://doi.org/10.1007/s00429-013-0680-x

doi: 10.1007/s00429-013-0680-x pubmed: 24310352

McGettigan C, Warren JE, Eisner F, Marshall CR, Shanmugalingam P, Scott SK (2011) Neural correlates of sublexical processing in phonological working memory. J Cog Neurosci 23(4):961–977. https://doi.org/10.1162/jocn.2010.21491

doi: 10.1162/jocn.2010.21491

Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113. https://doi.org/10.1016/0028-3932(71)90067-4

doi: 10.1016/0028-3932(71)90067-4 pubmed: 5146491

Penhune V, Zatorre R, MacDonald J, Evans A (1996) Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex 6(5):661–672. https://doi.org/10.1093/cercor/6.5.661

doi: 10.1093/cercor/6.5.661 pubmed: 8921202

Pundir AS, Singh UA, Ahuja N, Makhija S, Dikshit PC, Radotra B, Kumar P, Shankar SK, Mahadevan A, Roy TS, Iyengar S (2016) Growth and refinement of excitatory synapses in the human auditory cortex. Brain Struct Funct 221(7):3641–3674. https://doi.org/10.1007/s00429-015-1124-6

doi: 10.1007/s00429-015-1124-6 pubmed: 26438332

R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

Rademacher J, Caviness VS Jr., Steinmetz H, Galaburda AM (1993) Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. Cereb Cortex 3(4):313–329. https://doi.org/10.1093/cercor/3.4.313

doi: 10.1093/cercor/3.4.313 pubmed: 8400809

Rubin DB (1996) Multiple imputation after 18 + years. J Am Stat Assoc 91(434):473–489. https://doi.org/10.1080/01621459.1996.10476908

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(9):1241–1247. https://doi.org/10.1038/nn1530

doi: 10.1038/nn1530 pubmed: 16116442

Sheehan KA, McArthur GM, Bishop DV (2005) Is discrimination training necessary to cause changes in the P2 auditory event-related brain potential to speech sounds? Cog Brain Res 25(2):547–553. https://doi.org/10.1016/j.cogbrainres.2005.08.007

doi: 10.1016/j.cogbrainres.2005.08.007

Sigalovsky IS, Fischl B, Melcher JR (2006) Mapping an intrinsic MR property of gray matter in auditory cortex of living humans: a possible marker for primary cortex and hemispheric differences. NeuroImage 32(4):1524–1537. https://doi.org/10.1016/j.neuroimage.2006.05.023

doi: 10.1016/j.neuroimage.2006.05.023 pubmed: 16806989

Tong Y, Melara RD, Rao A (2009) P2 enhancement from auditory discrimination training is associated with improved reaction times. Brain Res 1297:80–88. https://doi.org/10.1016/j.brainres.2009.07.089

doi: 10.1016/j.brainres.2009.07.089 pubmed: 19651109

Tremblay K, Kraus N, McGee T, Ponton C, Otis B (2001) Central auditory plasticity: changes in the N1-P2 complex after speech-sound training. Ear Hear 22(2):79–90. https://doi.org/10.1097/00003446-200104000-00001

doi: 10.1097/00003446-200104000-00001 pubmed: 11324846

Vaden KI, Gebregziabher M, Kuchinsky SE, Eckert MA (2012) Multiple imputation of missing fMRI data in whole brain analysis. NeuroImage 60(3):1843–1855. https://doi.org/10.1016/j.neuroimage.2012.01.123

doi: 10.1016/j.neuroimage.2012.01.123 pubmed: 22500925

Vaden KI, Kuchinsky SE, Cute SL, Ahlstrom JB, Dubno JR, Eckert MA (2013) The cingulo-opercular network provides word-recognition benefit. J Neurosci 33(48):18979–18986. https://doi.org/10.1523/jneurosci.1417-13.2013

doi: 10.1523/jneurosci.1417-13.2013 pubmed: 24285902 pmcid: 3841458

Vaden KI Jr, Gebregziabher M, Eckert MA, Consortium DD (2020) Fully synthetic neuroimaging data for replication and exploration. NeuroImage 223:117284. https://doi.org/10.1016/j.neuroimage.2020.117284

doi: 10.1016/j.neuroimage.2020.117284 pubmed: 32828925

Vaden KI, Teubner-Rhodes S, Ahlstrom JB, Dubno JR, Eckert MA (2022) Evidence for cortical adjustments to perceptual decision criteria during word recognition in noise. NeuroImage 253:119042. https://doi.org/10.1016/j.neuroimage.2022.119042

doi: 10.1016/j.neuroimage.2022.119042 pubmed: 35259524

Van Atteveldt N, Formisano E, Goebel R, Blomert L (2004) Integration of letters and speech sounds in the human brain. Neuron 43(2):271–282. https://doi.org/10.1016/j.neuron.2004.06.025

doi: 10.1016/j.neuron.2004.06.025 pubmed: 15260962

Wechsler D (1999) Wechsler Abbreviated Scale of Intelligence. APA Psyc Tests. https://doi.org/10.1037/t15170-000

doi: 10.1037/t15170-000

Wechsler D (2004) The Wechsler intelligence scale for children-revised, 4th edn. Pearson Assessment, New York. https://doi.org/10.1037/t15174-000

Woodcock RW (1973) Woodcock Reading Mastery tests. APA PsycTests. https://doi.org/10.1037/t15178-000

doi: 10.1037/t15178-000

Woodcock RW, McGrew K, Mather N (2001) Woodcock-Johnson tests of cognitive abilities and tests of achievement, 3 edn. Rolling Meadows, Riverside, IL. https://doi.org/10.1002/9780470479216.corpsy1042

doi: 10.1002/9780470479216.corpsy1042

Xie L, Pluta JB, Das SR, Wisse LEM, Wang H, Mancuso L, Kliot D, Avants BB, Ding SL, Manjon JV, Wolk DA, Yushkevich PA (2017) Multi-template analysis of human perirhinal cortex in brain MRI: explicitly accounting for anatomical variability. NeuroImage 144(Pt A):183–202. https://doi.org/10.1016/j.neuroimage.2016.09.070

doi: 10.1016/j.neuroimage.2016.09.070 pubmed: 27702610

Ye Z, Rüsseler J, Gerth I, Münte TF (2017) Audiovisual speech integration in the superior temporal region is dysfunctional in dyslexia. Neuroscience 356:1–10. https://doi.org/10.1016/j.neuroscience.2017.05.017

doi: 10.1016/j.neuroscience.2017.05.017 pubmed: 28527953