Advertisement

Aging Clinical and Experimental Research

, Volume 27, Issue 1, pp 27–36 | Cite as

The effects of aging on the brain activation pattern during a speech perception task: an fMRI study

  • Hanani Abdul MananEmail author
  • Elizabeth A. Franz
  • Ahmad Nazlim Yusoff
  • Siti Zamratol-Mai Sarah Mukari
Original Article

Abstract

In the present study, brain activation associated with speech perception processing was examined across four groups of adult participants with age ranges between 20 and 65 years, using functional MRI (fMRI). Cognitive performance demonstrates that performance accuracy declines with age. fMRI results reveal that all four groups of participants activated the same brain areas. The same brain activation pattern was found in all activated areas (except for the right superior temporal gyrus and right middle temporal gyrus); brain activity was increased from group 1 (20–29 years) to group 2 (30–39 years). However, it decreased in group 3 (40–49 years) with further decreases in group 4 participants (50–65 years). Result also reveals that three brain areas (superior temporal gyrus, Heschl’s gyrus and cerebellum) showed changes in brain laterality in the older participants, akin to a shift from left-lateralized to right-lateralized activity. The onset of this change was different across brain areas. Based on these findings we suggest that, whereas all four groups of participants used the same areas in processing, the engagement and recruitment of those areas differ with age as the brain grows older. Findings are discussed in the context of corroborating evidence of neural changes with age.

Keywords

fMRI Speech perception processing Neural deterioration Brain laterality 

Notes

Acknowledgments

We thank Sa’don Samian from Department of Radiology, Universiti Kebangsaan Malaysia Medical Centre, for the assistance in fMRI scans. We also thank Mohammad Hairol Isa from Jabatan Kesihatan Masyarakat Universiti Kebangsaan Medical Centre, for his help on managing older participants. We also thank Noorazrul Azmie Yahya from Diagnostic Imaging and Radiotherapy Program, School of Diagnostic and Applied Health Sciences, for his ideas, and insight. This work is supported by the Research University Grant UKM GUP-SK-07-020-205.

Conflict of interest

The author certify that there is no actual or potential conflict of interest in relation to this article.

References

  1. 1.
    Grady CL, Maisog JM, Horwitz B, Ungerleider LG, Mentis MJ, Salerno JA et al (1994) Age-related changes in cortical blood flow activation during visual processing of faces and location. J Neurosci 14:1450–1462PubMedGoogle Scholar
  2. 2.
    Reuter-Lorenz PA, Cappell KA (2008) Neurocognitive aging and the compensation hypothesis. Curr Dir Psychol Sci 17(3):177–183CrossRefGoogle Scholar
  3. 3.
    Salthouse TA (2009) When does age-related cognitive decline begin? Neurobiol Aging 30:507–514PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Aine CJ, Adair JC, Knoefel JE, Hudson D, Qualls C, Kovacevic S, Woodruff CC, Cobb W, Padilla D, Lee RR, Stephen JM (2005) Temporal dynamics of age-related differences in auditory incidental verbal learning. Cogn Brain Res 24:1–18CrossRefGoogle Scholar
  5. 5.
    Cabeza R, Anderson ND, Locantore JK, McIntosh AR (2002) Aging gracefully: compensatory brain activity in high-performing older adults. NeuroImage 17:1394–1402PubMedCrossRefGoogle Scholar
  6. 6.
    Wingfield A, Grossman M (2006) Language and the aging brain: patterns of neural compensation revealed by functional brain imaging. J Neurophysiol 96:2830–2839PubMedCrossRefGoogle Scholar
  7. 7.
    Wlotko EW, Lee CL, Federmeier KD (2010) Language of the aging brain: event-related potential studies of comprehension in older adults. Lang Linguist Compass 4:623–638PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Dolcos F, Rice H, Cabeza R (2002) Hemispheric asymmetry and aging: right hemisphere decline or asymmetry reduction. Neurosci Biobehav Rev 26:819–825PubMedCrossRefGoogle Scholar
  9. 9.
    Zatorre RJ, Evans AC, Meyer E, Gjedde A (1992) Lateralization of phonetic and pitch discrimination in speech processing. Sciences 256(5058):846–849CrossRefGoogle Scholar
  10. 10.
    Butefisch CM, Kleiser R, Korber B, Muller K, Wittsack HJ, Homberg V, Seitz RJ (2005) Recruitment of contralateral motor cortex in stroke patient with recovery of hand function. Neurology 64:1067–1069PubMedCrossRefGoogle Scholar
  11. 11.
    Tyler LK, Marslen-Wilson WD, Randall B, Wright P, Devereux BJ, Zhuang J, Papoutsi M, Stamatakis EA (2011) Left inferior frontal cortex and syntax: function, structure and behavioural in patients with left hemisphere damage. Brain 134:415–431PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Gillard WD, Hertz-Pannier L, Mott SH, Bernett AS, LeBihan D, Theodore WH (2000) Functional anatomy of cognitive development: fMRI of verbal fluency in children and adults. Neurology 54:180–185CrossRefGoogle Scholar
  13. 13.
    Gillard WD, Sachs BC, Whitnah JR, Ahmad Z, Balsamo LM, Petrella JR, Braniecki SH, McKinney CM, Hunter K et al (2003) Developmental aspects of language processing: fMRI of verbal fluency in children and adults. Hum Brain Mapp 18:176–185CrossRefGoogle Scholar
  14. 14.
    Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9:97–113PubMedCrossRefGoogle Scholar
  15. 15.
    Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patient for clinician. J Psychiatry Res 12:189–198CrossRefGoogle Scholar
  16. 16.
    Turner CW, Kwon BJ, Tanaka C, Knapp J, Hubbartt LJ, Doherty KA (2008) Frequency-weighting functions for broadband speech as estimated by a correlational method. J Acoust Soc Am 104(3):1580–1585CrossRefGoogle Scholar
  17. 17.
    Hall AD, Haggard PM, Akeroyd Summerfield PR, Elliott Q, Gurney M, Bowtell RW (1999) “Sparse” temporal sampling in auditory fMRI. Human Brain Mapp 7:213–223CrossRefGoogle Scholar
  18. 18.
    Manan HA, Franz EA, Yusoff AN, Mukari SZM (2012) Hippocampal-cerebellar involvement in enhancement of performance in word-based BRT with the presence of background noise: an initial fMRI study. Psychol Neurosci 5(2):247–256. doi: 10.3922/j.psns.2012.2.16 CrossRefGoogle Scholar
  19. 19.
    Manan HA, Yusoff AN, Franz EA, Mukari SZM (2013) The effects of background noise on brain activity using speech stimuli on healthy young adults. Neurol Psychiatry Brain Res 19:207–215Google Scholar
  20. 20.
    Manan HA, Franz EA, Yusoff AN, Mukari SZM (2013) Age-related laterality shifts in auditory and attention networks with normal ageing: effects on a working memory task. Neurol Psychiatry Brain Res 19:180–191Google Scholar
  21. 21.
    Friston KJ, Holmes A, Poline JB, Price CJ, Frith CD (1996) Detecting activations in PET and fMRI: levels of inference and power. NeuroImage 40:223–235CrossRefGoogle Scholar
  22. 22.
    Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19:1233–1239PubMedCrossRefGoogle Scholar
  23. 23.
    Segheir ML (2008) Laterality index in functional MRI: methodological Issues. Magn Reson Imaging 26:594–601CrossRefGoogle Scholar
  24. 24.
    Buchsbaum BR, Hickok G, Humphries C (2001) Role of left posterior superior temporal gyrus in phonological processing for speech perception and production. Cogn Sci 25(5):663–678CrossRefGoogle Scholar
  25. 25.
    Celsis P, Boulanouar K, Doyon P, Ranjeva JP, Berry I, Nespoulous JL, Chollet F (1999) Differential fMRI responses in the left posterior superior temporal gyrus and left supramarginal gyrus to habituation and change detection in syllables and tones. NeuroImage 9(1):135–144PubMedCrossRefGoogle Scholar
  26. 26.
    Friederici AD, Ruschemeyer S, Hahne A, Fiebach CJ (2003) The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. Cereb Cortex 13(2):170–177PubMedCrossRefGoogle Scholar
  27. 27.
    Friederici AD (2011) The brain basis of language processing: from structure to function. Physiol Rev 91:1357–1392PubMedCrossRefGoogle Scholar
  28. 28.
    Scott SK, Blank CC, Rosen S, Wise RJS (2000) Identification of a pathway for intelligible speech in the left temporal lobe. Brain A J Neurol 123(12):2400–2406CrossRefGoogle Scholar
  29. 29.
    Demonet J, Chollet F, Ramsey S, Cardebat D, Nespoulous J, Wise R, Rascol A, Frackowiak R (1992) The anatomy of phonological and semantic processing in normal subjects. Brain A J Neurol 115(6):1753–1768CrossRefGoogle Scholar
  30. 30.
    Friederici AD (2002) Towards a neural basis of auditory sentence processing. Trends Cogn Sci 6(2):78–84PubMedCrossRefGoogle Scholar
  31. 31.
    Vigneau M, Beaucousin V, Herve PY, Duffau H, Crivello F, Houde O (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. NeuroImage 30(4):1414–1432PubMedCrossRefGoogle Scholar
  32. 32.
    Booth JR, Wood L, Lu D, Houk JC, Bitan T (2007) The roles of the basal ganglia and cerebellum in language processing. Brain Res 1133:136–144PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Desmond JE, Fiez JA (1998) Neuroimaging studies of the cerebellum: language, learning and memory. Trends Cogn Sci 2(9):355–362PubMedCrossRefGoogle Scholar
  34. 34.
    Just MA, Carpenter PA, Keller TA, Eddy WF, Thulborn KR (1996) Brain activation modulated by sentence comprehension. Science 274:114–116PubMedCrossRefGoogle Scholar
  35. 35.
    Frost JA, Binder JR, Springer JA, Hammeke TA, Bellgowan PSF, Rao SM, Cox RW (1998) Language processing is strongly left lateralized in both sexes. Evidence from functional MRI. Brain A J Neurol 122(2):199–208CrossRefGoogle Scholar
  36. 36.
    Mitchell KJ, Johnson MK, Raye CL, D’Esposito M (2000) fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. Cogn Brain Res 10(1):197–206CrossRefGoogle Scholar
  37. 37.
    Smith EE, Gewa A, Jonides J, Miller A, Reuter-Lorenz P, Koeppe RA (2000) The neural basis of task-switching in working memory: effects of performance and aging. Proc Natl Acad Sci USA 98:2095–2100CrossRefGoogle Scholar
  38. 38.
    Cabeza R, Dennis NA (2012) Frontal lobes and aging; deterioration and compensation. In: Stuss DT, Knight RT (eds) Principles of frontal lobe function, 2nd edn. Oxford University Press, Oxford, pp 628–652Google Scholar
  39. 39.
    Salthouse TA (2012) Does the direction and magnitude of cognitive change depend on initial level of ability? Intelligence 40:352–361PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Reuter-Lorenz PA, Sylvester CYC, Cabeza R, Nyberg L, Park D (2005) The cognitive neuroscience of working memory and aging. In: Cognitive neuroscience of aging: linking cognitive and cerebral aging. Oxford University Press, New York, pp 186–121Google Scholar
  41. 41.
    Cabeza R, Nyberg L (2000) Imaging cognition II: an empirical review of 275 PET and fMRI studies. J Cogn Neurosci 12:1–47PubMedCrossRefGoogle Scholar
  42. 42.
    Balsamo LM, Benjamin MA, Cecile BG, Jeffrey RP, Braniecki SH, Elliott TK, Gaillard DW (2002) A functional magnetic resonance imaging study of left hemisphere language dominance in children. JAMA Neurol 59(7):1168–1174Google Scholar
  43. 43.
    Sommer IEC, Ramsey NF, Kahn RS (2001) Language lateralization in schizophrenia, an fMRI study. Schizophrenia Res 52:57–67CrossRefGoogle Scholar
  44. 44.
    Cabeza R (2001) Cognitive neuroscience of aging: contributions of functional neuroimaging. Scand J Psychol 42:277–286PubMedCrossRefGoogle Scholar
  45. 45.
    Cabeza R, Nyberg L, Park D (2005) Cognitive neuroscience of aging: linking cognitive and cerebral aging. Oxford University Press, New YorkGoogle Scholar
  46. 46.
    Kemper S (2000) Over- and under-accommodations to aging. In: Charness N, Parks DC, Sabel BA (eds) Communication, technology, and aging. Springer, DoylestownGoogle Scholar
  47. 47.
    Kemper S, Sumner A (2001) The structure of verbal abilities in young and older adults. Psychol Aging 16:312–322PubMedCrossRefGoogle Scholar
  48. 48.
    Kemper S, Thompson M, Marquis J (2001) Longitudinal change in language production: effects of aging and dementia on grammatical complexity and propositional content. Psychol Aging 16:600–614PubMedCrossRefGoogle Scholar
  49. 49.
    Kemper S, Herman RE, Lian CHT (2003) The costs of doing two things at once for young and older adults: talking while walking, finger tapping, and ignoring speech or noise. Psychol Aging 18:181–192PubMedCrossRefGoogle Scholar
  50. 50.
    Kemper S, Herman RE, Nartowicz J (2005) Different effects of dual task demands on the speech of young and older adults. Aging Neuropsychol Cogn 12:340–358CrossRefGoogle Scholar
  51. 51.
    Kemper S, McDowd J, Pohl P, Herman R, Jackson S (2006) Revealing language deficits following stroke: the cost of doing two things at once. Aging Neuropsychol Cogn 13:115–139CrossRefGoogle Scholar
  52. 52.
    Banich MT (1998) The missing link: the role of interhemispheric interaction in attentional processing. Brain Cogn 36:128–157PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Hanani Abdul Manan
    • 1
    Email author
  • Elizabeth A. Franz
    • 2
  • Ahmad Nazlim Yusoff
    • 1
  • Siti Zamratol-Mai Sarah Mukari
    • 3
  1. 1.Diagnostic Imaging and Radiotherapy Program, School of Diagnostic and Applied Health Sciences, Faculty of Health SciencesUniversiti Kebangsaan MalaysiaKuala LumpurMalaysia
  2. 2.Department of Psychology and fMRIotagoUniversity of OtagoDunedinNew Zealand
  3. 3.Audiology Program, School of Rehabilitation Sciences, Faculty of Health SciencesUniversiti Kebangsaan MalaysiaKuala LumpurMalaysia

Personalised recommendations