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Structural brain aging and speech production: a surface-based brain morphometry study

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Abstract

While there has been a growing number of studies examining the neurofunctional correlates of speech production over the past decade, the neurostructural correlates of this immensely important human behaviour remain less well understood, despite the fact that previous studies have established links between brain structure and behaviour, including speech and language. In the present study, we thus examined, for the first time, the relationship between surface-based cortical thickness (CT) and three different behavioural indexes of sublexical speech production: response duration, reaction times and articulatory accuracy, in healthy young and older adults during the production of simple and complex meaningless sequences of syllables (e.g., /pa–pa-pa/ vs. /pa-ta-ka/). The results show that each behavioural speech measure was sensitive to the complexity of the sequences, as indicated by slower reaction times, longer response durations and decreased articulatory accuracy in both groups for the complex sequences. Older adults produced longer speech responses, particularly during the production of complex sequence. Unique age-independent and age-dependent relationships between brain structure and each of these behavioural measures were found in several cortical and subcortical regions known for their involvement in speech production, including the bilateral anterior insula, the left primary motor area, the rostral supramarginal gyrus, the right inferior frontal sulcus, the bilateral putamen and caudate, and in some region less typically associated with speech production, such as the posterior cingulate cortex.

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References

  • Ackermann H, Riecker A (2004) The contribution of the insula to motor aspects of speech production: a review and a hypothesis. Brain Lang 89(2):320–328. doi:10.1016/S0093-934X(03)00347-X

    Article  PubMed  Google Scholar 

  • Alario FX, Chainay H, Lehericy S, Cohen L (2006) The role of the supplementary motor area (SMA) in word production. Brain Res 1076(1):129–143

    Article  CAS  PubMed  Google Scholar 

  • Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381

    Article  CAS  PubMed  Google Scholar 

  • Alexander GE, Crutcher MD, DeLong MR (1990) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 85:119–146

    Article  CAS  PubMed  Google Scholar 

  • Anderson BJ, Eckburg PB, Relucio KI (2002) Alterations in the thickness of motor cortical subregions after motor-skill learning and exercise. Learn Mem 9(1):1–9. doi:10.1101/lm.43402

    Article  PubMed  PubMed Central  Google Scholar 

  • Andrews-Hanna JR, Snyder AZ, Vincent JL, Lustig C, Head D, Raichle ME, Buckner RL (2007) Disruption of large-scale brain systems in advanced aging. Neuron 56(5):924–935. doi:10.1016/j.neuron.2007.10.038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Averbeck BB, Chafee MV, Crowe DA, Georgopoulos AP (2002) Parallel processing of serial movements in prefrontal cortex. Proc Natl Acad Sci USA 99(20):13172–13177. doi:10.1073/pnas.162485599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Averbeck BB, Chafee MV, Crowe DA, Georgopoulos AP (2003) Neural activity in prefrontal cortex during copying geometrical shapes. I. Single cells encode shape, sequence, and metric parameters. Exp Brain Res 150(2):127–141. doi:10.1007/s00221-003-1416-6

    PubMed  Google Scholar 

  • Bengtsson SL, Ehrsson HH, Forssberg H, Ullen F (2004) Dissociating brain regions controlling the temporal and ordinal structure of learned movement sequences. Eur J Neurosci 19(9):2591–2602. doi:10.1111/j.0953-816X.2004.03269.x

    Article  PubMed  Google Scholar 

  • Bengtsson SL, Ehrsson HH, Forssberg H, Ullen F (2005) Effector-independent voluntary timing: behavioural and neuroimaging evidence. Eur J Neurosci 22(12):3255–3265. doi:10.1111/j.1460-9568.2005.04517.x

    Article  PubMed  Google Scholar 

  • Bilodeau-Mercure M, Lortie CL, Sato M, Guitton MJ, Tremblay P (2014) The neurobiology of speech perception decline in aging. Brain Struct Funct. doi:10.1007/s00429-013-0695-3

    PubMed  Google Scholar 

  • Bilodeau-Mercure M, Kirouac V, Langlois N, Ouellet C, Tremblay P (2015) Movement sequencing in normal aging: speech, oro-facial and finger movements. Age (revisions submitted)

  • Bischoff-Grethe A, Goedert KM, Willingham DT, Grafton ST (2004) Neural substrates of response-based sequence learning using fMRI. J Cogn Neurosci 16(1):127–138. doi:10.1162/089892904322755610

    Article  PubMed  Google Scholar 

  • Blackmon K, Barr WB, Kuzniecky R, Dubois J, Carlson C, Quinn BT, Blumberg M, Halgren E, Hagler DJ, Mikhly M, Devinsky O, McDonald CR, Dale AM, Thesen T (2010) Phonetically irregular word pronunciation and cortical thickness in the adult brain. Neuroimage 51(4):1453–1458. doi:10.1016/j.neuroimage.2010.03.028

    Article  PubMed  PubMed Central  Google Scholar 

  • Boersma P, Weenink D (2011) Praat: doing phonetics by computer. 5.2.10 edn

  • Bohland JW, Guenther FH (2006) An fMRI investigation of syllable sequence production. Neuroimage 32(2):821–841. doi:10.1016/j.neuroimage.2006.04.173

    Article  PubMed  Google Scholar 

  • Bohland JW, Bullock D, Guenther FH (2010) Neural representations and mechanisms for the performance of simple speech sequences. J Cogn Neurosci 22(7):1504–1529. doi:10.1162/jocn.2009.21306

    Article  PubMed  PubMed Central  Google Scholar 

  • Bookheimer SY, Zeffiro TA, Blaxton TA, Gaillard PW, Theodore WH (2000) Activation of language cortex with automatic speech tasks. Neurology 55(8):1151–1157

    Article  CAS  PubMed  Google Scholar 

  • Bramen JE, Hranilovich JA, Dahl RE, Chen J, Rosso C, Forbes EE, Dinov ID, Worthman CM, Sowell ER (2012) Sex matters during adolescence: testosterone-related cortical thickness maturation differs between boys and girls. PLoS ONE 7(3):e33850. doi:10.1371/journal.pone.0033850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brendel B, Hertrich I, Erb M, Lindner A, Riecker A, Grodd W, Ackermann H (2010) The contribution of mesiofrontal cortex to the preparation and execution of repetitive syllable productions: an fMRI study. Neuroimage 50(3):1219–1230. doi:10.1016/j.neuroimage.2010.01.039

    Article  PubMed  Google Scholar 

  • Brendel B, Erb M, Riecker A, Grodd W, Ackermann H, Ziegler W (2011) Do we have a “mental syllabary” in the brain? An FMRI study. Mot Control 15(1):34–51

    Google Scholar 

  • Brenhouse HC, Andersen SL (2011) Developmental trajectories during adolescence in males and females: a cross-species understanding of underlying brain changes. Neurosci Biobehav Rev 35(8):1687–1703. doi:10.1016/j.neubiorev.2011.04.013

    Article  PubMed  PubMed Central  Google Scholar 

  • Burggren AC, Renner B, Jones M, Donix M, Suthana NA, Martin-Harris L, Ercoli LM, Miller KJ, Siddarth P, Small GW, Bookheimer SY (2011) Thickness in entorhinal and subicular cortex predicts episodic memory decline in mild cognitive impairment. Int J Alzheimer’s Dis 2011:956053. doi:10.4061/2011/956053

    CAS  Google Scholar 

  • Bybee J (2002) Phonological evidence for exemplar storage of multiword sequences. Studies Second Lang Acquis 24:215–221

    Article  Google Scholar 

  • Bybee J, Scheibman J (1999) The effect of usage on degree of constituency: the reduction of don’t in American English. Linguistics 37:575–596

    Article  Google Scholar 

  • Calhoun KH, Gibson B, Hartley L, Minton J, Hokanson JA (1992) Age-related changes in oral sensation. Laryngoscope 102(2):109–116. doi:10.1288/00005537-199202000-00001

    Article  CAS  PubMed  Google Scholar 

  • Carriere JS, Cheyne JA, Solman GJ, Smilek D (2010) Age trends for failures of sustained attention. Psychol Aging 25(3):569–574. doi:10.1037/a0019363

    Article  PubMed  Google Scholar 

  • Caspers S, Geyer S, Schleicher A, Mohlberg H, Amunts K, Zilles K (2006) The human inferior parietal cortex: cytoarchitectonic parcellation and interindividual variability. NeuroImage 33(2):430–448

    Article  PubMed  Google Scholar 

  • Caspers S, Eickhoff SB, Geyer S, Scheperjans F, Mohlberg H, Zilles K, Amunts K (2008) The human inferior parietal lobule in stereotaxic space. Brain Struct Funct 212(6):481–495. doi:10.1007/s00429-008-0195-z

    Article  PubMed  Google Scholar 

  • Caspers S, Zilles K, Laird AR, Eickhoff SB (2010) ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 50(3):1148–1167. doi:10.1016/j.neuroimage.2009.12.112

    Article  PubMed  Google Scholar 

  • Caspers S, Eickhoff SB, Rick T, von Kapri A, Kuhlen T, Huang R, Shah NJ, Zilles K (2011) Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques. Neuroimage 58(2):362–380. doi:10.1016/j.neuroimage.2011.06.027

    Article  PubMed  Google Scholar 

  • Caspers S, Schleicher A, Bacha-Trams M, Palomero-Gallagher N, Amunts K, Zilles K (2013a) Organization of the human inferior parietal lobule based on receptor architectonics. Cereb Cortex 23:615–628

    Article  PubMed  Google Scholar 

  • Caspers S, Schleicher A, Bacha-Trams M, Palomero-Gallagher N, Amunts K, Zilles K (2013b) Organization of the human inferior parietal lobule based on receptor architectonics. Cereb Cortex 23(3):615–628. doi:10.1093/cercor/bhs048

    Article  PubMed  Google Scholar 

  • Chang LJ, Yarkoni T, Khaw MW, Sanfey AG (2013) Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb Cortex 23(3):739–749. doi:10.1093/cercor/bhs065

    Article  PubMed  Google Scholar 

  • Dale AM, Sereno MI (1993) Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci 5:162–176

    Article  CAS  PubMed  Google Scholar 

  • Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9(2):179–194. doi:10.1006/nimg.1998.0395

    Article  CAS  PubMed  Google Scholar 

  • Damoiseaux JS, Beckmann CF, Arigita EJ, Barkhof F, Scheltens P, Stam CJ, Smith SM, Rombouts SA (2008) Reduced resting-state brain activity in the “default network” in normal aging. Cereb Cortex 18(8):1856–1864. doi:10.1093/cercor/bhm207

    Article  CAS  PubMed  Google Scholar 

  • de Brabander JM, Kramers RJ, Uylings HB (1998) Layer-specific dendritic regression of pyramidal cells with ageing in the human prefrontal cortex. Eur J Neurosci 10(4):1261–1269

    Article  PubMed  Google Scholar 

  • De Leon MJ, George AE, Golomb J, Tarshish C, Convit A, Kluger A, De Santi S, McRae T, Ferris SH, Reisberg B, Ince C, Rusinek H, Bobinski M, Quinn B, Miller DC, Wisniewski HM (1997) Frequency of hippocampal formation atrophy in normal aging and Alzheimer’s disease. Neurobiol Aging 18(1):1–11

    Article  PubMed  Google Scholar 

  • Deschamps I, Baum SR, Gracco VL (2014) On the role of the supramarginal gyrus in phonological processing and verbal working memory: evidence from rTMS studies. Neuropsychologia 53:39–46. doi:10.1016/j.neuropsychologia.2013.10.015

    Article  PubMed  Google Scholar 

  • Dickerson BC, Fenstermacher E, Salat DH, Wolk DA, Maguire RP, Desikan R, Pacheco J, Quinn BT, Van der Kouwe A, Greve DN, Blacker D, Albert MS, Killiany RJ, Fischl B (2008) Detection of cortical thickness correlates of cognitive performance: reliability across MRI scan sessions, scanners, and field strengths. Neuroimage 39(1):10–18. doi:10.1016/j.neuroimage.2007.08.042

    Article  CAS  PubMed  Google Scholar 

  • Diggles Buckles V (1993) Age-related slowing. In: Netherlands S (ed) Sensorimotor impairment in the elderly, vol 75. NATO ASI Series, pp 73–87. doi:10.1007/978-94-011-1976-4_6

  • Doose G, Feyereisen P (2001) Task specificity in age-related slowing: word production versus conceptual comparison. J Gerontol Ser B Psychol Sci Soc Sci 56(2):P85–87

    Article  CAS  Google Scholar 

  • Dromey C, Boyce K, Channell R (2014) Effects of age and syntactic complexity on speech motor performance. J Speech Lang Hear Res 57(6):2142–2151. doi:10.1044/2014_JSLHR-S-13-0327

    Article  PubMed  Google Scholar 

  • Dronkers NF (1996) A new brain region for coordinating speech articulation. Nature 384(6605):159–161. doi:10.1038/384159a0

    Article  CAS  PubMed  Google Scholar 

  • Duchin SW, Mysak ED (1987) Disfluency and rate characteristics of young adult, middle-aged, and older males. J Commun Disord 20(3):245–257

    Article  CAS  PubMed  Google Scholar 

  • Engvig A, Fjell AM, Westlye LT, Moberget T, Sundseth O, Larsen VA, Walhovd KB (2010) Effects of memory training on cortical thickness in the elderly. Neuroimage 52(4):1667–1676. doi:10.1016/j.neuroimage.2010.05.041

    Article  PubMed  Google Scholar 

  • Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97(20):11050–11055. doi:10.1073/pnas.200033797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischl B, Sereno MI, Dale AM (1999a) Cortical surface-based analysis: II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 9(2):195–207

    Article  CAS  PubMed  Google Scholar 

  • Fischl B, Sereno MI, Tootell RB, Dale AM (1999b) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8(4):272–284

    Article  CAS  PubMed  Google Scholar 

  • Fischl B, Liu A, Dale AM (2001) Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 20(1):70–80

    Article  CAS  PubMed  Google Scholar 

  • Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33(3):341–355

    Article  CAS  PubMed  Google Scholar 

  • Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14(1):11–22. doi:10.1093/cercor/bhg087

    Article  PubMed  Google Scholar 

  • Fjell AM, Walhovd KB (2010) Structural brain changes in aging: courses, causes and cognitive consequences. Rev Neurosci 21(3):187–221

    Article  PubMed  Google Scholar 

  • Fjell AM, Walhovd KB, Fennema-Notestine C, McEvoy LK, Hagler DJ, Holland D, Brewer JB, Dale AM (2009a) One-year brain atrophy evident in healthy aging. J Neurosci 29(48):15223–15231. doi:10.1523/JNEUROSCI.3252-09.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fjell AM, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N, Agartz I, Salat DH, Greve DN, Fischl B, Dale AM, Walhovd KB (2009b) High consistency of regional cortical thinning in aging across multiple samples. Cereb Cortex 19(9):2001–2012. doi:10.1093/cercor/bhn232

    Article  PubMed  PubMed Central  Google Scholar 

  • Fozo MS, Watson BC (1998) Task complexity effect on vocal reaction time in aged speakers. J Voice 12(4):404–414

    Article  CAS  PubMed  Google Scholar 

  • Gamboz N, Zamarian S, Cavallero C (2010) Age-related differences in the attention network test (ANT). Exp Aging Res 36(3):287–305. doi:10.1080/0361073X.2010.484729

    Article  PubMed  Google Scholar 

  • Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG (1997) Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. Brain 120(Pt 9):1587–1602

    Article  PubMed  Google Scholar 

  • Ghosh SS, Tourville JA, Guenther FH (2008) A neuroimaging study of premotor lateralization and cerebellar involvement in the production of phonemes and syllables. J Speech Lang Hear Res 51(5):1183–1202. doi:10.1044/1092-4388(2008/07-0119)

    Article  PubMed  PubMed Central  Google Scholar 

  • Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2(10):861–863. doi:10.1038/13158

    Article  CAS  PubMed  Google Scholar 

  • Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci 101(21):8174–8179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golestani N, Paus T, Zatorre RJ (2002) Anatomical correlates of learning novel speech sounds. Neuron 35(5):997–1010

    Article  CAS  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(3):575–582. doi:10.1093/cercor/bhk001

    Article  PubMed  Google Scholar 

  • Golfinopoulos E, Tourville JA, Guenther FH (2010) The integration of large-scale neural network modeling and functional brain imaging in speech motor control. Neuroimage 52(3):862–874

    Article  CAS  PubMed  Google Scholar 

  • Grogan A, Green DW, Ali N, Crinion JT, Price CJ (2009) Structural correlates of semantic and phonemic fluency ability in first and second languages. Cereb Cortex 19(11):2690–2698. doi:10.1093/cercor/bhp023

    Article  PubMed  PubMed Central  Google Scholar 

  • Guenther FH (1995) Speech sound acquisition, coarticulation, and rate effects in a neural network model of speech production. Psychol Rev 102(3):594–621

    Article  CAS  PubMed  Google Scholar 

  • Guenther FH (2006) Cortical interactions underlying the production of speech sounds. J Commun Disord 39(5):350–365. doi:10.1016/j.jcomdis.2006.06.013

    Article  PubMed  Google Scholar 

  • Guenther FH, Hampson M, Johnson D (1998) A theoretical investigation of reference frames for the planning of speech movements. Psychol Rev 105(4):611–633

    Article  CAS  PubMed  Google Scholar 

  • Guenther FH, Ghosh SS, Tourville JA (2006) Neural modeling and imaging of the cortical interactions underlying syllable production. Brain Lang 96(3):280–301

    Article  PubMed  Google Scholar 

  • Hafkemeijer A, Altmann-Schneider I, de Craen AJ, Slagboom PE, van der Grond J, Rombouts SA (2014) Associations between age and gray matter volume in anatomical brain networks in middle-aged to older adults. Aging Cell 13(6):1068–1074. doi:10.1111/acel.12271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haller S, Radue EW, Erb M, Grodd W, Kircher T (2005) Overt sentence production in event-related fMRI. Neuropsychologia 43(5):807–814

    Article  PubMed  Google Scholar 

  • Han X, Jovicich J, Salat D, van der Kouwe A, Quinn B, Czanner S, Busa E, Pacheco J, Albert M, Killiany R, Maguire P, Rosas D, Makris N, Dale A, Dickerson B, Fischl B (2006) Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. Neuroimage 32(1):180–194. doi:10.1016/j.neuroimage.2006.02.051

    Article  PubMed  Google Scholar 

  • Henson RN, Shallice T, Dolan RJ (1999) Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. Brain 122(Pt 7):1367–1381

    Article  PubMed  Google Scholar 

  • Hickok G (2012) Computational neuroanatomy of speech production. Nat Rev Neurosci 13(2):135–145. doi:10.1038/nrn3158

    Article  CAS  PubMed  Google Scholar 

  • Hoover JE, Strick PL (1999) The organization of cerebellar and basal ganglia outputs to primary motor cortex as revealed by retrograde transneuronal transport of herpes simplex virus type 1. J Neurosci 19(4):1446–1463

    CAS  PubMed  Google Scholar 

  • Huettel SA, Mack PB, McCarthy G (2002) Perceiving patterns in random series: dynamic processing of sequence in prefrontal cortex. Nat Neurosci 5(5):485–490. doi:10.1038/nn841

    CAS  PubMed  Google Scholar 

  • Huttenlocher PR (1979) Synaptic density in human frontal cortex: developmental changes and effects of aging. Brain Res 163:195–205

    Article  CAS  PubMed  Google Scholar 

  • Jacobs B, Scheibel AB (1993) A quantitative dendritic analysis of Wernicke’s area in humans. I. Lifespan changes. J Comp Neurol 327(1):83–96. doi:10.1002/cne.903270107

    Article  CAS  PubMed  Google Scholar 

  • Jennings JM, Dagenbach D, Engle CM, Funke LJ (2007) Age-related changes and the attention network task: an examination of alerting, orienting, and executive function. Neuropsychol Dev Cogn Sect B Aging Neuropsychol Cogn 14(4):353–369. doi:10.1080/13825580600788837

    Article  Google Scholar 

  • Kennedy KM, Raz N (2005) Age, sex and regional brain volumes predict perceptual-motor skill acquisition. Cortex 41(4):560–569

    Article  PubMed  Google Scholar 

  • Kent RD (2000) Research on speech motor control and its disorders: a review and prospective. J Commun Disord 33(5):391–427 (quiz 428). pii: S0021-9924(00)00023-X

  • Kent RD, Kent JF, Rosenbek JC (1987) Maximum performance tests of speech production. J Speech Hear Disord 52(4):367–387

    Article  CAS  PubMed  Google Scholar 

  • Kuperberg GR, Broome MR, McGuire PK, David AS, Eddy M, Ozawa F, Goff D, West WC, Williams SC, van der Kouwe AJ, Salat DH, Dale AM, Fischl B (2003) Regionally localized thinning of the cerebral cortex in schizophrenia. Arch Gen Psychiatry 60(9):878–888

    Article  PubMed  Google Scholar 

  • Lashley KS (1951) The problem of serial order in behavior. In: Jeffress LA (ed) Cerebral mechanisms in behavior. Wiley, New York, pp 112–131

    Google Scholar 

  • Lewis PA, Miall RC (2002) Brain activity during non-automatic motor production of discrete multi-second intervals. NeuroReport 13(14):1731–1735

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Li C, Wu Q, Xu Z, Kurata T, Ohno S, Kanazawa S, Abe K, Wu J (2015) Decreased resting-state connections within the visuospatial attention-related network in advanced aging. Neurosci Lett 597:13–18. doi:10.1016/j.neulet.2015.03.047

    Article  CAS  PubMed  Google Scholar 

  • Lotze M, Seggewies G, Erb M, Grodd W, Birbaumer N (2000) The representation of articulation in the primary sensorimotor cortex. NeuroReport 11(13):2985–2989

    Article  CAS  PubMed  Google Scholar 

  • Lovden M, Schmiedek F, Kennedy KM, Rodrigue KM, Lindenberger U, Raz N (2013) Does variability in cognitive performance correlate with frontal brain volume? Neuroimage 64:209–215. doi:10.1016/j.neuroimage.2012.09.039

    Article  PubMed  Google Scholar 

  • Macar F, Lejeune H, Bonnet M, Ferrara A, Pouthas V, Vidal F, Maquet P (2002) Activation of the supplementary motor area and of attentional networks during temporal processing. Exp Brain Res 142(4):475–485. doi:10.1007/s00221-001-0953-0

    Article  CAS  PubMed  Google Scholar 

  • Magnaldi S, Ukmar M, Vasciaveo A, Longo R, Pozzi-Mucelli RS (1993) Contrast between white and grey matter: MRI appearance with ageing. Eur Radiol 3(6):513–519. doi:10.1007/BF00169600

    Article  Google Scholar 

  • Manoach DS, Gollub RL, Benson ES, Searl MM, Goff DC, Halpern E, Saper CB, Rauch SL (2000) Schizophrenic subjects show aberrant fMRI activation of dorsolateral prefrontal cortex and basal ganglia during working memory performance. Biol Psychiatry 48(2):99–109

    Article  CAS  PubMed  Google Scholar 

  • Mazoyer B, Zago L, Mellet E, Bricogne S, Etard O, Houde O, Crivello F, Joliot M, Petit L, Tzourio-Mazoyer N (2001) Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Res Bull 54(3):287–298

    Article  CAS  PubMed  Google Scholar 

  • Mechelli A, Crinion JT, Noppeney U, O’Doherty J, Ashburner J, Frackowiak RS, Price CJ (2004) Neurolinguistics: structural plasticity in the bilingual brain. Nature 431(7010):757. doi:10.1038/431757a

    Article  CAS  PubMed  Google Scholar 

  • Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214(5–6):655–667. doi:10.1007/s00429-010-0262-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Menon V, Anagnoson RT, Glover GH, Pfefferbaum A (2000) Basal ganglia involvement in memory-guided movement sequencing. NeuroReport 11(16):3641–3645

    Article  CAS  PubMed  Google Scholar 

  • Montembeault M, Joubert S, Doyon J, Carrier J, Gagnon JF, Monchi O, Lungu O, Belleville S, Brambati SM (2012) The impact of aging on gray matter structural covariance networks. Neuroimage 63(2):754–759. doi:10.1016/j.neuroimage.2012.06.052

    Article  PubMed  Google Scholar 

  • Morris R, Brown WS (1987) Age-related voice measures among adult women. J Voice 1(1):43

    Article  Google Scholar 

  • Moser D, Fridriksson J, Bonilha L, Healy EW, Baylis G, Baker JM, Rorden C (2009) Neural recruitment for the production of native and novel speech sounds. Neuroimage 46(2):549–557

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakamura S, Akiguchi I, Kameyama M, Mizuno N (1985) Age-related changes of pyramidal cell basal dendrites in layers III and V of human motor cortex: a quantitative Golgi study. Acta Neuropathol 65(3–4):281–284

    Article  CAS  PubMed  Google Scholar 

  • Nasreddine ZS, Chertkow H, Phillips N, Bergman H, Whitehead V (2003) Sensitivity and specificity of the Montreal cognitive assessment (MoCA) for detection of mild cognitive deficits. Can J Neurol Sci 30(30)

  • Neel AT, Palmer PM (2012) Is tongue strength an important influence on rate of articulation in diadochokinetic and reading tasks? J Speech Lang Hear Res 55(1):235–246. doi:10.1044/1092-4388(2011/10-0258)

    Article  PubMed  Google Scholar 

  • Nelson SM, Dosenbach NU, Cohen AL, Wheeler ME, Schlaggar BL, Petersen SE (2010) Role of the anterior insula in task-level control and focal attention. Brain Struct Funct 214(5–6):669–680. doi:10.1007/s00429-010-0260-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Neta M, Schlaggar BL, Petersen SE (2014) Separable responses to error, ambiguity, and reaction time in cingulo-opercular task control regions. Neuroimage 99:59–68. doi:10.1016/j.neuroimage.2014.05.053

    Article  PubMed  PubMed Central  Google Scholar 

  • Obler LK, Rykhlevskaia E, Schnyer D, Clark-Cotton MR, Spiro A 3rd, Hyun J, Kim DS, Goral M, Albert ML (2010) Bilateral brain regions associated with naming in older adults. Brain Lang 113(3):113–123. doi:10.1016/j.bandl.2010.03.001

    Article  PubMed  PubMed Central  Google Scholar 

  • Ogar J, Willock S, Baldo J, Wilkins D, Ludy C, Dronkers N (2006) Clinical and anatomical correlates of apraxia of speech. Brain Lang 97(3):343–350. doi:10.1016/j.bandl.2006.01.008

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    Article  CAS  PubMed  Google Scholar 

  • Olesen PJ, Westerberg H, Klingberg T (2004) Increased prefrontal and parietal activity after training of working memory. Nat Neurosci 7(1):75–79

    Article  CAS  PubMed  Google Scholar 

  • Peelle JE, Troiani V, Wingfield A, Grossman M (2010) Neural processing during older adults’ comprehension of spoken sentences: age differences in resource allocation and connectivity. Cereb Cortex 20(4):773–782. doi:10.1093/cercor/bhp142

    Article  PubMed  Google Scholar 

  • Peeva MG, Guenther FH, Tourville JA, Nieto-Castanon A, Anton JL, Nazarian B, Alario FX (2010) Distinct representations of phonemes, syllables, and supra-syllabic sequences in the speech production network. Neuroimage 50(2):626–638. doi:10.1016/j.neuroimage.2009.12.065

    Article  PubMed  Google Scholar 

  • Peschke C, Ziegler W, Kappes J, Baumgaertner A (2009) Auditory-motor integration during fast repetition: the neuronal correlates of shadowing. Neuroimage 47(1):392–402. doi:10.1016/j.neuroimage.2009.03.061

    Article  CAS  PubMed  Google Scholar 

  • Pessoa L, Gutierrez E, Bandettini P, Ungerleider L (2002) Neural correlates of visual working memory: fMRI amplitude predicts task performance. Neuron 35(5):975–987

    Article  CAS  PubMed  Google Scholar 

  • Petrides M (2005) Lateral prefrontal cortex: architectonic and functional organization. Philos Trans R Soc Lond B Biol Sci 360(1456):781–795. doi:10.1098/rstb.2005.1631

    Article  PubMed  PubMed Central  Google Scholar 

  • Porter JN, Collins PF, Muetzel RL, Lim KO, Luciana M (2011) Associations between cortical thickness and verbal fluency in childhood, adolescence, and young adulthood. Neuroimage 55(4):1865–1877. doi:10.1016/j.neuroimage.2011.01.018

    Article  PubMed  PubMed Central  Google Scholar 

  • Postuma RB, Dagher A (2006) Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. Cereb Cortex 16(10):1508–1521. doi:10.1093/cercor/bhj088

    Article  PubMed  Google Scholar 

  • Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98(2):676–682. doi:10.1073/pnas.98.2.676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rakic P (1988) Specification of cerebral cortical areas. Science 241(4862):170–176

    Article  CAS  PubMed  Google Scholar 

  • Riecker A, Wildgruber D, Dogil G, Grodd W, Ackermann H (2002) Hemispheric lateralization effects of rhythm implementation during syllable repetitions: an fMRI study. Neuroimage 16:169–176

    Article  PubMed  Google Scholar 

  • Riecker A, Mathiak K, Wildgruber D, Erb M, Hertrich I, Grodd W, Ackermann H (2005) fMRI reveals two distinct cerebral networks subserving speech motor control. Neurology 64:700–706

    Article  CAS  PubMed  Google Scholar 

  • Riecker A, Brendel B, Ziegler W, Erb M, Ackermann H (2008) The influence of syllable onset complexity and syllable frequency on speech motor control. Brain Lang 107(2):102–113

    Article  PubMed  Google Scholar 

  • Roehrich-Gascon D, Small SL, Tremblay P (2015) Structural correlates of spoken language abilities: a surface-based region-of interest morphometry study. Brain Lang 149:46–54

    Article  PubMed  Google Scholar 

  • Rosas HD, Liu AK, Hersch S, Glessner M, Ferrante RJ, Salat DH, van der Kouwe A, Jenkins BG, Dale AM, Fischl B (2002) Regional and progressive thinning of the cortical ribbon in Huntington’s disease. Neurology 58(5):695–701

    Article  CAS  PubMed  Google Scholar 

  • Ryan WJ, Burk KW (1974) Perceptual and acoustic correlates of aging in the speech of males. J Commun Disord 7(2):181–192

    Article  CAS  PubMed  Google Scholar 

  • Saad ZS, Reynolds RC (2012) Suma. Neuroimage 62(2):768–773. doi:10.1016/j.neuroimage.2011.09.016

    Article  PubMed  Google Scholar 

  • Sadagopan N, Smith A (2013) Age differences in speech motor performance on a novel speech task. J Speech Lang Hear Res 56(5):1552–1566. doi:10.1044/1092-4388(2013/12-0293)

    Article  PubMed  Google Scholar 

  • Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RS, Busa E, Morris JC, Dale AM, Fischl B (2004) Thinning of the cerebral cortex in aging. Cereb Cortex 14(7):721–730

    Article  PubMed  Google Scholar 

  • Salat DH, Lee SY, Van Der Kouwe A, Greve DN, Fischl B, Rosas HD (2009) Age-associated alterations in cortical gray and white matter signal intensity and gray to white matter contrast. Neuroimage 48(1):21–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satz P (1993) Brain reserve capacity on symptom onset after brain injury: a formulation and review of evidence for threshold theory. Neuropsychology 7(3):273–295

    Article  Google Scholar 

  • Scheibel ME, Lindsay RD, Tomiyasu U, Scheibel AB (1975) Progressive dendritic changes in aging human cortex. Exp Neurol 47(3):392–403

    Article  CAS  PubMed  Google Scholar 

  • Searl JP, Gabel RM, Fulks JS (2002) Speech disfluency in centenarians. J Commun Disord 35(5):383–392

    Article  PubMed  Google Scholar 

  • Sebastián-Gallés N, Soriano-Mas C, Baus C, Díaz B, Ressel V, Pallier C, Costa A, Pujol J (2012) Neuroanatomical markers of individual differences in native and non-native vowel perception. J Neurolinguist 25(3):150–162. doi:10.1016/j.jneuroling.2011.11.001

    Article  Google Scholar 

  • Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356. doi:10.1523/JNEUROSCI.5587-06.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B (2004) A hybrid approach to the skull stripping problem in MRI. Neuroimage 22(3):1060–1075

    Article  CAS  PubMed  Google Scholar 

  • Segonne F, Pacheco J, Fischl B (2007) Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 26(4):518–529

    Article  PubMed  Google Scholar 

  • Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB (2010) Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev 34(5):721–733. doi:10.1016/j.neubiorev.2009.10.005

    Article  CAS  PubMed  Google Scholar 

  • Shafto MA, Burke DM, Stamatakis EA, Tam PP, Tyler LK (2007) On the tip-of-the-tongue: neural correlates of increased word-finding failures in normal aging. J Cogn Neurosci 19(12):2060–2070. doi:10.1162/jocn.2007.19.12.2060

    Article  PubMed  PubMed Central  Google Scholar 

  • Shalom DB, Poeppel D (2008) Functional anatomic models of language: assembling the pieces. Neuroscientist 14(1):119–127. doi:10.1177/1073858407305726

    Article  PubMed  Google Scholar 

  • Shulman GL, Fiez JA, Corbetta M, Buckner RL, Miezin FM, Raichle ME, Petersen SE (1997) Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J Cogn Neurosci 9(5):648–663. doi:10.1162/jocn.1997.9.5.648

    Article  CAS  PubMed  Google Scholar 

  • Shuster LI (2009) The effect of sublexical and lexical frequency on speech production: an fMRI investigation. Brain Lang 111(1):66–72. doi:10.1016/j.bandl.2009.06.003

    Article  PubMed  Google Scholar 

  • Shuster LI, Lemieux SK (2005) An fMRI investigation of covertly and overtly produced mono- and multisyllabic words. Brain Lang 93(1):20–31

    Article  PubMed  Google Scholar 

  • Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17(1):87–97

    Article  CAS  PubMed  Google Scholar 

  • Smith BL, Wasowicz J, Preston J (1987) Temporal characteristics of the speech of normal elderly adults. J Speech Hear Res 30(4):522–529

    Article  CAS  PubMed  Google Scholar 

  • Song J, Birn RM, Boly M, Meier TB, Nair VA, Meyerand ME, Prabhakaran V (2014) Age-related reorganizational changes in modularity and functional connectivity of human brain networks. Brain Connect 4(9):662–676. doi:10.1089/brain.2014.0286

    Article  PubMed  PubMed Central  Google Scholar 

  • Soros P, Sokoloff LG, Bose A, McIntosh AR, Graham SJ, Stuss DT (2006) Clustered functional MRI of overt speech production. Neuroimage 32(1):376–387. doi:10.1016/j.neuroimage.2006.02.046

    Article  PubMed  Google Scholar 

  • Steffener J (1822) Stern Y (2012) Exploring the neural basis of cognitive reserve in aging. Biochim Biophys Acta 3:467–473. doi:10.1016/j.bbadis.2011.09.012

    Google Scholar 

  • Stern Y (2002) What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 8(3):448–460

    Article  PubMed  Google Scholar 

  • Stern Y (2003) The concept of cognitive reserve: a catalyst for research. J Clin Exp Neuropsychol 25(5):589–593. doi:10.1076/jcen.25.5.589.14571

    Article  PubMed  Google Scholar 

  • Storsve AB, Fjell AM, Tamnes CK, Westlye LT, Overbye K, Aasland HW, Walhovd KB (2014) Differential longitudinal changes in cortical thickness, surface area and volume across the adult life span: regions of accelerating and decelerating change. J Neurosci 34(25):8488–8498. doi:10.1523/JNEUROSCI.0391-14.2014

    Article  CAS  PubMed  Google Scholar 

  • Tan LH, Spinks JA, Gao JH, Liu HL, Perfetti CA, Xiong J, Stofer KA, Pu Y, Liu Y, Fox PT (2000) Brain activation in the processing of Chinese characters and words: a functional MRI study. Hum Brain Mapp 10(1):16–27

    Article  CAS  PubMed  Google Scholar 

  • Van Petten C, Plante E, Davidson PS, Kuo TY, Bajuscak L, Glisky EL (2004) Memory and executive function in older adults: relationships with temporal and prefrontal gray matter volumes and white matter hyperintensities. Neuropsychologia 42(10):1313–1335. doi:10.1016/j.neuropsychologia.2004.02.009

    Article  PubMed  Google Scholar 

  • van Velsen EF, Vernooij MW, Vrooman HA, van der Lugt A, Breteler MM, Hofman A, Niessen WJ, Ikram MA (2013) Brain cortical thickness in the general elderly population: the Rotterdam Scan Study. Neurosci Lett 550:189–194. doi:10.1016/j.neulet.2013.06.063

    Article  PubMed  CAS  Google Scholar 

  • Vingerhoets G, Van Borsel J, Tesink C, van den Noort M, Deblaere K, Seurinck R, Vandemaele P, Achten E (2003) Multilingualism: an fMRI study. Neuroimage 20(4):2181–2196

    Article  PubMed  Google Scholar 

  • Wang L, Su L, Shen H, Hu D (2012) Decoding lifespan changes of the human brain using resting-state functional connectivity MRI. PLoS ONE 7(8):e44530. doi:10.1371/journal.pone.0044530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei G, Zhang Y, Jiang T, Luo J (2011) Increased cortical thickness in sports experts: a comparison of diving players with the controls. PLoS ONE 6(2):e17112. doi:10.1371/journal.pone.0017112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilde EA, Newsome MR, Bigler ED, Pertab J, Merkley TL, Hanten G, Scheibel RS, Li X, Chu Z, Yallampalli R, Hunter JV, Levin HS (2011) Brain imaging correlates of verbal working memory in children following traumatic brain injury. Int J Psychophysiol 82(1):86–96. doi:10.1016/j.ijpsycho.2011.04.006

    Article  PubMed  PubMed Central  Google Scholar 

  • Wohlert AB (1996) Tactile perception of spatial stimuli on the lip surface by young and older adults. J Speech Hear Res 39(6):1191–1198

    Article  CAS  PubMed  Google Scholar 

  • Wohlert AB, Smith A (1998) Spatiotemporal stability of lip movements in older adult speakers. J Speech Lang Hear Res 41(1):41–50

    Article  CAS  PubMed  Google Scholar 

  • Wong PC, Warrier CM, Penhune VB, Roy AK, Sadehh A, Parrish TB, Zatorre RJ (2008) Volume of left Heschl’s Gyrus and linguistic pitch learning. Cereb Cortex 18(4):828–836. doi:10.1093/cercor/bhm115

    Article  PubMed  Google Scholar 

  • Wong PC, Ettlinger M, Sheppard JP, Gunasekera GM, Dhar S (2010) Neuroanatomical characteristics and speech perception in noise in older adults. Ear Hear 31(4):471–479. doi:10.1097/AUD.0b013e3181d709c2

    Article  PubMed  PubMed Central  Google Scholar 

  • Tremblay P, Sato M, Deschamps I (2015) The neurofunctional underpinning of sub-lexical speech production in aging. NeuroImage (submitted)

  • Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, Leirer VO (1982) Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17(1):37–49

    Article  PubMed  Google Scholar 

  • Zhang H, Sachdev PS, Wen W, Kochan NA, Crawford JD, Brodaty H, Slavin MJ, Reppermund S, Kang K, Trollor JN (2013) Grey matter correlates of three language tests in non-demented older adults. PLoS ONE 8(11):e80215. doi:10.1371/journal.pone.0080215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou SS, Fan J, Lee TM, Wang CQ, Wang K (2011) Age-related differences in attentional networks of alerting and executive control in young, middle-aged, and older Chinese adults. Brain Cogn 75(2):205–210. doi:10.1016/j.bandc.2010.12.003

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by P.T.’s research grants from the “Fonds de la Recherche du Québec Société-Culture”, the Natural Sciences and Engineering Research Council of Canada (CA), the “Fonds de Recherche du Québec—Santé” (FRQS), and by start-up funds from the “Institut Universitaire en Santé Mentale de Québec” also to P.T. Technical support was provided by the “Consortium d’imagerie en neuroscience et santé mentale de Québec” (CINQ) for protocol development and MRI data acquisition. Their support is gratefully acknowledged. We thank Mylène Bilodeau-Mercure, Anne-Marie Audet and Marc Sato for their help with MRI data acquisition and behavioural data analyses.

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  1. Centre de Recherche de l’Institut Universitaire en Santé Mentale de Québec, Quebec, QC, Canada

    Pascale Tremblay & Isabelle Deschamps

  2. Département de Réadaptation, Faculté de Médecine, Université Laval, Quebec, QC, Canada

    Pascale Tremblay & Isabelle Deschamps

  3. Département de Rehabilitation, Université Laval, Office 4462, 1050 avenue de la Médecine, Quebec, QC, G1V 0A6, Canada

    Pascale Tremblay

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  1. Pascale Tremblay
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  2. Isabelle Deschamps
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Correspondence to Pascale Tremblay.

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429_2015_1100_MOESM1_ESM.eps

Supplementary material S1. Distribution of errors for the young and older adults, separately for the simple and complex sequences, (A) as a function of position in the sequence (first vs. second half), (B) also as a function of position in the sequence, but for each of the six sequence positions, (C) as a function of the category of errors (exchanges, insertion and deletion. (C) more detailed analysis of error types with all 8 categories of errors. (EPS 4187 kb)

429_2015_1100_MOESM2_ESM.eps

Supplementary material S2. Mean cortical thickness maps for (A): the young adults, (B) the older adults and C: regions showing a significant age difference (Young > Older, in blue). Results are shown on the group average smoothed white matter folded surface in which dark gray regions represent sulci while pale gray areas represent gyri. (EPS 23344 kb)

429_2015_1100_MOESM3_ESM.eps

Supplementary material S3. Scatter plots illustrating the relationship between subcortical structures and complexity effects in response duration as a function of age (young adults: green dots; older adults, pink dots), in the left (top row) and right caudate nuclei (bottom row). (EPS 2360 kb)

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Tremblay, P., Deschamps, I. Structural brain aging and speech production: a surface-based brain morphometry study. Brain Struct Funct 221, 3275–3299 (2016). https://doi.org/10.1007/s00429-015-1100-1

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