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01-05-2016 | Original Paper

Age-Related Neural Oscillation Patterns During the Processing of Temporally Manipulated Speech

Authors: Katharina S. Rufener, Mathias S. Oechslin, Malte Wöstmann, Volker Dellwo, Martin Meyer

Published in: Brain Topography | Issue 3/2016

Abstract

This EEG-study aims to investigate age-related differences in the neural oscillation patterns during the processing of temporally modulated speech. Viewing from a lifespan perspective, we recorded the electroencephalogram (EEG) data of three age samples: young adults, middle-aged adults and older adults. Stimuli consisted of temporally degraded sentences in Swedish—a language unfamiliar to all participants. We found age-related differences in phonetic pattern matching when participants were presented with envelope-degraded sentences, whereas no such age-effect was observed in the processing of fine-structure-degraded sentences. Irrespective of age, during speech processing the EEG data revealed a relationship between envelope information and the theta band (4–8 Hz) activity. Additionally, an association between fine-structure information and the gamma band (30–48 Hz) activity was found. No interaction, however, was found between acoustic manipulation of stimuli and age. Importantly, our main finding was paralleled by an overall enhanced power in older adults in high frequencies (gamma: 30–48 Hz). This occurred irrespective of condition. For the most part, this result is in line with the Asymmetric Sampling in Time framework (Poeppel in Speech Commun 41:245–255, 2003), which assumes an isomorphic correspondence between frequency modulations in neurophysiological patterns and acoustic oscillations in spoken language. We conclude that speech-specific neural networks show strong stability over adulthood, despite initial processes of cortical degeneration indicated by enhanced gamma power. The results of our study therefore confirm the concept that sensory and cognitive processes undergo multidirectional trajectories within the context of healthy aging.

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Abrams DA, Nicol T, Zecker S, Kraus N (2008) Right-hemisphere auditory cortex is dominant for coding syllable patterns in speech. J Neurosci 28(15):3958–3965. doi:10.1523/JNEUROSCI.0187-08.2008 CrossRefPubMedPubMedCentral

Ahissar E, Nagarajan S, Ahissar M, Protopapas A, Mahncke H, Merzenich MM (2001) Speech comprehension is correlated with temporal response patterns recorded from auditory cortex. PNAS 98(23):13367–13372. doi:10.1073/pnas.201400998 CrossRefPubMedPubMedCentral

Baltes P, Lindenberger U (1997) Emergence of a powerful connection between sensory and cognitive functions across the adult life span: a new window to the study of cognitive aging? Psychol Aging 12(1):12–21. doi:10.1037/0882-7974.12.1.12 CrossRefPubMed

Bellis TJ, Nicol T, Kraus N (2000) Aging affects hemispheric asymmetry in the neural representation of speech sounds. J Neurosci 20(2):791–797. doi:10.1523/JNEUROSCI PubMed

Davis MH, Johnsrude IS, Hervais-Adelman A, Taylor K, McGettigan C (2005) Lexical information drives perceptual learning of distorted speech: evidence from the comprehension of noise-vocoded sentences. J Exp Psychol Gen 134(2):222–241. doi:10.1037/0096-3445.134.2.222 CrossRefPubMed

Davis SW, Dennis NA, Daselaar SM, Fleck MS, Cabeza R (2008) Que PASA? The posterior-anterior shift in aging. Cereb Cortex 18(5):1201–1209. doi:10.1093/cercor/bhm155 CrossRefPubMedPubMedCentral

Drullman R, Festen JM, Plomp R (1994) Effect of reducing slow temporal modulations on speech reception. J Acoust Soc Am 95(5 Pt 1):2670–2680CrossRefPubMed

Dudley H (1939) The automatic synthesis of speech. Proc Natl Acad Sci USA 25(7):377–383. doi:10.2307/87390 CrossRefPubMedPubMedCentral

Freunberger R, Werkle-Bergner M, Griesmayr B, Lindenberger U, Klimesch W (2011) Brain oscillatory correlates of working memory constraints. Brain Res 1375(C):93–102. doi:10.1016/j.brainres.2010.12.048 CrossRefPubMed

Giraud A-L, Poeppel D (2012) Cortical oscillations and speech processing: emerging computational principles and operations. Nat Neurosci 15(4):511–517. doi:10.1038/nn.3063 CrossRefPubMedPubMedCentral

Giraud A-L, Kleinschmidt A, Poeppel D, Lund TE, Frackowiak RSJ, Laufs H (2007) Endogenous cortical rhythms determine cerebral specialization for speech perception and production. Neuron 56(6):1127–1134. doi:10.1016/j.neuron.2007.09.038 CrossRefPubMed

Golomb JD, Peelle JE, Wingfield A (2007) Effects of stimulus variability and adult aging on adaptation to time-compressed speech. J Acoust Soc Am 121(3):1701. doi:10.1121/1.2436635 CrossRefPubMed

Gordon-Salant S (2005) Hearing loss and aging: new research findings and clinical implications. J Rehabil Res Dev 42(4s):9. doi:10.1682/JRRD.2005.01.0006 CrossRefPubMed

Greenwood DD (1990) A cochlear frequency-position function for several species—29 years later. J Acoust Soc Am 87(6):2592–2604CrossRefPubMed

Gross J, Hoogenboom N, Thut G, Schyns P, Panzeri S, Belin P, Garrod S (2013) Speech rhythms and multiplexed oscillatory sensory coding in the human brain. PLoS Biol 11(12):e1001752. doi:10.1371/journal.pbio.1001752.s005 CrossRefPubMedPubMedCentral

Hall JW III, Grose JH, Buss E, Dev MB (2002) Spondee recognition in a two-talker masker and a speech-shaped noise masker in adults and children. Ear Hear 23(2):159–165CrossRefPubMed

Hopkins K, Moore BCJ, Stone MA (2008) Effects of moderate cochlear hearing loss on the ability to benefit from temporal fine structure information in speech. J Acoust Soc Am 123(2):1140. doi:10.1121/1.2824018 CrossRefPubMedPubMedCentral

Houtgast T, Steeneken HJ (1973) The modulation transfer function in room acoustics as a predictor of speech intelligibility. J Acoust Soc Am 54(2):557CrossRef

Humes LE, Kewley-Port D, Fogerty D, Kinney D (2010) Measures of hearing threshold and temporal processing across the adult lifespan. Hear Res 264(1–2):30–40. doi:10.1016/j.heares.2009.09.010 CrossRefPubMedPubMedCentral

Humes LE, Dubno JR, Gordon-Salant S, Lister JJ, Cacace AT, Cruickshanks KJ et al (2012) Central presbycusis: a review and evaluation of the evidence. J Am Acad Audiol 23(8):635–666. doi:10.3766/jaaa.23.8.5 CrossRefPubMed

Jung TP, Makeig S, Humphries C, Lee TW, McKeown MJ, Iragui V, Sejnowski TJ (2000) Removing electroencephalographic artifacts by blind source separation. Psychophysiology 37(2):163–178CrossRefPubMed

Larsby B, Hällgren M, Lyxell B, Arlinger S (2005) Cognitive performance and perceived effort in speech processing tasks: effects of different noise backgrounds in normal-hearing and hearing-impaired subjects. Int J Audiol 44(3):131–143. doi:10.1080/14992020500057244 CrossRefPubMed

Lorenzi C, Gilbert G, Carn H, Garnier S, Moore BCJ (2006) Speech perception problems of the hearing impaired reflect inability to use temporal fine structure. Proc Natl Acad Sci USA 103(49):18866–18869. doi:10.1073/pnas.0607364103 CrossRefPubMedPubMedCentral

Luo H, Poeppel D (2012) Cortical oscillations in auditory perception and speech: evidence for two temporal windows in human auditory cortex. Front Psychol 170(3):1–10. doi:10.3389/fpsyg.2012.00170

Missonnier P, Herrmann FR, Michon A, Fazio-Costa L, Gold G, Giannakopoulos P (2010) Early disturbances of gamma band dynamics in mild cognitive impairment. J Neural Transm 117(4):489–498. doi:10.1007/s00702-010-0384-9 CrossRefPubMed

Obrist WD (1976) Problems of aging. In: Redmond A (ed) Handbook of electroencephalography and clinical neurophysiology. Elsevier, Amsterdam, pp 275–292

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

Park DC, Smith AD, Dudley WN, Lafronza VN (1989) Effects of age and a divided attention task presented during encoding and retrieval on memory. J Exp Psychol Learn Mem Cogn 15(6):1185–1191CrossRefPubMed

Park JY, Lee KS, An SK, Lee J, Kim J-J, Kim KH, Namkoong K (2012) Gamma oscillatory activity in relation to memory ability in older adults. Int J Psychophysiol 86(1):58–65. doi:10.1016/j.ijpsycho.2012.08.002 CrossRefPubMed

Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12PubMed

Peelle JE, Davis MH (2012) Neural oscillations carry speech rhythm through to comprehension. Front Psychol 3:320. doi:10.3389/fpsyg.2012.00320 CrossRefPubMedPubMedCentral

Peña M, Melloni L (2012) Brain oscillations during spoken sentence processing. J Cogn Neurosci 24(5):1149–1164. doi:10.1162/jocn_a_00144 CrossRefPubMed

Picton TW, Alain C, Woods DL, John MS, Scherg M, Valdes-Sosa P et al (1999) Intracerebral sources of human auditory-evoked potentials. Audiol Neurootol 4(2):64–79CrossRefPubMed

Poeppel D (2003) The analysis of speech in different temporal integration windows: cerebral lateralization as “asymmetric sampling in time”. Speech Commun 41(1):245–255. doi:10.1016/S0167-6393(02)00107-3 CrossRef

Reuter-Lorenz PA, Cappell KA (2008) Neurocognitive aging and the compensation hypothesis. Curr Dir Psychol Sci 17(3):177–182. doi:10.1111/j.1467-8721.2008.00570.x CrossRef

Rosen S (1992) Temporal information in speech: acoustic, auditory and linguistic aspects. Philos Trans R Soc Lond B Biol Sci 336(1278):367–373. doi:10.1098/rstb.1992.0070 CrossRefPubMed

Salthouse TA (1996) The processing-speed theory of adult age differences in cognition. Psychol Rev 103(3):403–428. doi:10.1037/0033-295X.103.3.403 CrossRefPubMed

Salthouse TA (2000) Aging and measures of processing speed. Biol Psychol 54(1–3):35–54. doi:10.1016/S0301-0511(00)00052-1 CrossRefPubMed

Sander MC, Werkle-Bergner M, Lindenberger U (2012) Amplitude modulations and inter-trial phase stability of alpha-oscillations differentially reflect working memory constraints across the lifespan. NeuroImage 59(1):646–654. doi:10.1016/j.neuroimage.2011.06.092 CrossRefPubMed

Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270(5234):303–304CrossRefPubMed

Sheft S, Ardoint M, Lorenzi C (2008) Speech identification based on temporal fine structure cues. J Acoust Soc Am 124(1):562. doi:10.1121/1.2918540 CrossRefPubMedPubMedCentral

Smith ZM, Delgutte B, Oxenham AJ (2002) Chimaeric sounds reveal dichotomies in auditory perception. Nature 416(6876):87–90. doi:10.1038/416087a CrossRefPubMedPubMedCentral

Souza PE, Boike KT (2006) Combining temporal-envelope cues across channels: effects of age and hearing loss. J Speech Lang Hear Res 49(1):138–149. doi:10.1044/1092-4388(2006/011) CrossRefPubMed

Souza PE, Kitch V (2001) The contribution of amplitude envelope cues to sentence identification in young and aged listeners. Ear Hear 22(2):112–119CrossRefPubMed

Van Tasell DJ, Greenfield DG, Logemann JJ, Nelson DA (1992) Temporal cues for consonant recognition: training, talker generalization, and use in evaluation of cochlear implants. J Acoust Soc Am 92(3):1247–1257. doi:10.1121/1.403920 CrossRefPubMed

Weiss S, Rappelsberger P (2000) Long-range EEG synchronization during word encoding correlates with successful memory performance. Brain Res Cogn Brain Res 9(3):299–312. doi:10.1016/S0926-6410(00)00011-2 CrossRefPubMed

Werkle-Bergner M, Shing YL, Müller V, Li S-C, Lindenberger U (2009) EEG gamma-band synchronization in visual coding from childhood to old age: evidence from evoked power and inter-trial phase locking. Clin Neurophysiol 120(7):1291–1302. doi:10.1016/j.clinph.2009.04.012 CrossRefPubMed

Zatorre RJ, Belin P (2001) Spectral and temporal processing in human auditory cortex. Cereb Cortex 11(10):946–953. doi:10.1093/cercor/11.10.946 CrossRefPubMed

Title: Age-Related Neural Oscillation Patterns During the Processing of Temporally Manipulated Speech
Authors: Katharina S. Rufener
Mathias S. Oechslin
Malte Wöstmann
Volker Dellwo
Martin Meyer
Publication date: 01-05-2016
Publisher: Springer US
Published in: Brain Topography / Issue 3/2016
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI: https://doi.org/10.1007/s10548-015-0464-0

ACC 2024 Congress

Springer Medicine

Age-Related Neural Oscillation Patterns During the Processing of Temporally Manipulated Speech

Abstract

ACC 2024 Congress

Springer Medicine

Abstract

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