Hostname: page-component-6b989bf9dc-mbg9n Total loading time: 0 Render date: 2024-04-13T10:05:49.431Z Has data issue: false hasContentIssue false

Semantic integration declines independently of working memory in aging

Published online by Cambridge University Press:  18 October 2019

Zude Zhu*
Affiliation:
Jiangsu Normal University, Collaborative Innovation Center for Language Ability, and Jiangsu Key Laboratory of Language and Cognitive Neuroscience
Suiping Wang
Affiliation:
Guangdong Provincial Key Laboratory of Mental Health and Cognitive Science
Nannan Xu
Affiliation:
Jiangsu Normal University
Mengya Li
Affiliation:
Jiangsu Normal University
Yiming Yang
Affiliation:
Jiangsu Normal University, Collaborative Innovation Center for Language Competence, and Jiangsu Key Laboratory of Language and Cognitive Neuroscience
*
*Corresponding author. Email: zhuzude@163.com or yangym@jsnu.edu.cn

Abstract

Semantic integration and working memory both decline with age. However, it remains unclear whether the semantic integration decline is independent of working memory decline or whether it can be solely explained by the latter factor. In this event-related potentials experiment, 43 younger adults and 43 cognitively healthy older adults read semantically congruent and incongruent sentences. After controlling for working memory, behavioral accuracy was significantly lower in the older adults than in the younger adults. In addition, the semantic integration related N400 effect (incongruent vs. congruent) for correct trials was apparent in the whole brain in the younger adults but restricted to the posterior region in the older adults. The results clarify the relationship between working memory and semantic integration, and clearly demonstrate that semantic integration decline is independent of working memory decline during aging.

Type
Original Article
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baddeley, A. (1992). Working memory. Science, 255, 556559.CrossRefGoogle ScholarPubMed
Bopp, K. L., & Verhaeghen, P. (2005). Aging and verbal memory span: A meta-analysis. Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 60, P223P233.CrossRefGoogle ScholarPubMed
Cabeza, R., & Dennis, N. A. (2012). Frontal lobes and aging: Deterioration and compensation. In Stuss, D. T. & Knight, R. T. (Eds.), Principles of frontal lobe function (2nd ed., pp. 628–652). New York: Oxford University Press.Google Scholar
Cai, Q., & Brysbaert, M. (2010). SUBTLEX-CH: Chinese word and character frequencies based on film subtitles. Plos One, 5, e10729.CrossRefGoogle ScholarPubMed
Clark, D. G., McLaughlin, P. M., Woo, E., Hwang, K., Hurtz, S., Ramirez, L., … Apostolova, L. G. (2016). Novel verbal fluency scores and structural brain imaging for prediction of cognitive outcome in mild cognitive impairment. Alzheimers & Dementia, 2, 113122.Google ScholarPubMed
DeCaro, R., Peelle, J. E., Grossman, M., & Wingfield, A. (2016). The two sides of sensory-cognitive interactions: Effects of age, hearing acuity, and working memory span on sentence comprehension. Frontiers in Psychology, 7, 236.CrossRefGoogle ScholarPubMed
Diaz, M. T., Rizio, A. A., & Zhuang, J. (2016). The neural language systems that support healthy aging: Integrating function, structure, and behavior. Linguistics and Language Compass, 10, 314334.CrossRefGoogle ScholarPubMed
Faustmann, A., Murdoch, B. E., Finnigan, S. P., & Copland, D. A. (2007). Effects of advancing age on the processing of semantic anomalies in adults: Evidence from event-related brain potentials. Experimental Aging Research, 33, 439460.CrossRefGoogle ScholarPubMed
Federmeier, K. D., Kutas, M., & Schul, R. (2010). Age-related and individual differences in the use of prediction during language comprehension. Brain and Language, 115, 149161.CrossRefGoogle ScholarPubMed
Federmeier, K. D., McLennan, D. B., De Ochoa, E., & Kutas, M. (2002). The impact of semantic memory organization and sentence context information on spoken language processing by younger and older adults: An ERP study. Psychophysiology, 39, 133146.CrossRefGoogle Scholar
Federmeier, K. D., Van Petten, C., Schwartz, T. J., & Kutas, M. (2003). Sounds, words, sentences: Age-related changes across levels of language processing. Psychology and Aging, 18, 858872.CrossRefGoogle ScholarPubMed
Fedorenko, E., & Thompson-Schill, S. L. (2014). Reworking the language network. Trends in Cognitive Sciences, 18, 120126.CrossRefGoogle ScholarPubMed
Friedman, N. P., & Miyake, A. (2005). Comparison of four scoring methods for the reading span test. Behavior Research Methods, 37, 581590.CrossRefGoogle ScholarPubMed
Gazzaley, A., Cooney, J. W., Rissman, J., & D’Esposito, M. (2005). Top-down suppression deficit underlies working memory impairment in normal aging. Nature Neuroscience, 8, 12981300.CrossRefGoogle ScholarPubMed
Gong, Y. X. (1992). Wechsler Adult Intelligence Scale—Revised in China Version. Changsha, China: Hunan Medical College.Google Scholar
Grossman, M., Cooke, A., DeVita, C., Chen, W., Moore, P., Detre, J., … Ge, J. (2002). Sentence processing strategies in healthy seniors with poor comprehension: An fMRI study. Brain and Language, 80, 296313.CrossRefGoogle Scholar
Gunter, T. C., Jackson, J. L., & Mulder, G. (1995). Language, memory, and aging: An electrophysiological exploration of the N400 during reading of memory-demanding sentences. Psychophysiology, 32, 215229.CrossRefGoogle ScholarPubMed
Hagoort, P. (2008). The fractionation of spoken language understanding by measuring electrical andmagnetic brain signals. Philosophical Transactions of the Royal Society B-Biological Sciences, 363, 10551069.CrossRefGoogle Scholar
Hagoort, P., Baggio, G., & Willems, R. M. (2009). Semantic unification. In Gazzaniga, M. S. (Ed.), The cognitive neurosciences (pp. 819836). Cambridge, MA: MIT Press.Google Scholar
Hagoort, P., Hald, L., Bastiaansen, M., & Petersson, K. M. (2004). Integration of word meaning and world knowledge in language comprehension. Science, 304, 438441.CrossRefGoogle ScholarPubMed
Hasher, L., & Zacks, R. T. (1988). Working memory, comprehension and aging: A review and a new view. In Bower, G. H. (Ed.), The psychology of learning and motivation (Vol. 22, pp. 193225). New York: Academic Press.Google Scholar
Hu, C., Wang, F., Guo, J., Song, M., Sui, J., & Peng, K. (2016). The replication crisis in psychological research. Adcances in Psychological Science, 24, 15041518.CrossRefGoogle Scholar
James, P. J., Krishnan, S., & Aydelott, J. (2014). Working memory predicts semantic comprehension in dichotic listening in older adults. Cognition, 133, 3242.CrossRefGoogle ScholarPubMed
Just, M. A., & Carpenter, P. A. (1992). A capacity theory of comprehension: Individual differences in working memory. Psychological Review, 99, 122149.CrossRefGoogle ScholarPubMed
Kemper, S., Marquis, J., & Thompson, M. (2001). Longitudinal change in language production: Effects of aging and dementia on grammatical complexity and propositional content. Psychology and Aging, 16, 600614.CrossRefGoogle ScholarPubMed
Kutas, M., & Federmeier, K. D. (2011). Thirty years and counting: finding meaning in the N400 component of the event related brain potential (ERP). Annual Review of Psychology, 62, 621.CrossRefGoogle Scholar
Kutas, M., & Hillyard, S. A. (1980). Reading senseless sentences: Brain potentials reflect semantic incongruity. Science, 207, 203205.CrossRefGoogle ScholarPubMed
Miller, J., Patterson, T., & Ulrich, R. (1998). A jackknife-based method for measuring LRP onset latency differences. Psychophysiology, 35, 99115.CrossRefGoogle ScholarPubMed
Madden, C. J., & Dijkstra, K. (2010). Contextual constraints in situation model construction: An investigation of age and reading span. Aging Neuropsychology and Cognition, 17, 1934.CrossRefGoogle ScholarPubMed
Nakano, H., Saron, C., & Swaab, T. Y. (2010). Speech and span: Working memory capacity impacts the use of animacy but not of world knowledge during spoken sentence comprehension. Journal of Cognitive Neuroscience, 22, 28862898.CrossRefGoogle Scholar
Park, D. C., & Reuter-Lorenz, P. (2009). The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173196.CrossRefGoogle ScholarPubMed
Peelle, J. E., Chandrasekaran, K., Powers, J., Smith, E. E., & Grossman, M. (2013). Age-related vulnerability in the neural systems supporting semantic processing. Frontiers in Aging Neuroscience, 5, 46.CrossRefGoogle ScholarPubMed
Peelle, J. E., Troiani, V., Wingfield, A., & Grossman, M. (2010). Neural processing during older adults’ comprehension of spoken sentences: Age differences in resource allocation and connectivity. Cerebral Cortex, 20, 773782.CrossRefGoogle ScholarPubMed
Salisbury, D. F. (2004). Semantic memory and verbal working memory correlates of N400 to subordinate homographs. Brain and Cognition, 55, 396399.CrossRefGoogle ScholarPubMed
Salthouse, T. A. (1996). The processing-speed theory of adult age differences in cognition. Psychological Review, 103, 403428.CrossRefGoogle ScholarPubMed
Sugarman, M. A., Woodard, J. L., Nielson, K. A., Seidenberg, M., Smith, J. C., Durgerian, S., & Rao, S. M. (2012). Functional magnetic resonance imaging of semantic memory as a presymptomatic biomarker of Alzheimer’s disease risk. Biochimica et Biophysica Acta (BBA)–Molecular Basis of Disease, 1822, 442456.CrossRefGoogle ScholarPubMed
Szatloczki, G., Hoffmann, I., Vincze, V., Kalman, J., & Pakaski, M. (2015). Speaking in Alzheimer’s disease, is that an early sign? Importance of changes in language abilities in Alzheimer’s disease. Frontiers in Aging Neuroscience, 7, 195.CrossRefGoogle ScholarPubMed
Tremblay, P., Dick, A. S., & Small, S. L. (2013). Functional and structural aging of the speech sensorimotor neural system: Functional magnetic resonance imaging evidence. Neurobiology of Aging, 34, 19351951.CrossRefGoogle ScholarPubMed
Wlotko, E. W., & Federmeier, K. D. (2012). Age-related changes in the impact of contextual strength on multiple aspects of sentence comprehension. Psychophysiology, 49, 770785.CrossRefGoogle ScholarPubMed
Wlotko, E. W., Lee, C. L., & Federmeier, K. D. (2010). Language of the aging brain: Event-related potential studies of comprehension in older adults. Language and Linguistics Compass, 4, 623638.CrossRefGoogle ScholarPubMed
Xu, N., Hou, X., Zhao, B., Zhu, Z., & Yang, Y. (2017). Age-related temporal-spatial dynamic ERP changes during sentence comprehension. Neuroscience Letters, 645, 7479.CrossRefGoogle ScholarPubMed
Zhang, H., & Wang, X. (1985). Raven Standard Progressive Matrices: Chinese City Revision. Beijing: Beijing Normal University Press.Google Scholar
Zhu, Z., Feng, G., Zhang, J. X., Li, G., Li, H., & Wang, S. (2013). The role of the left prefrontal cortex in sentence-level semantic integration. NeuroImage, 76, 325331.CrossRefGoogle ScholarPubMed
Zhu, Z., Hagoort, P., Zhang, J. X., Feng, G., Chen, H. C., Bastiaansen, M., & Wang, S. (2012). The anterior left inferior frontal gyrus contributes to semantic unification. NeuroImage, 60, 22302237.CrossRefGoogle ScholarPubMed
Zhu, Z., Hou, X., & Yang, Y. (2018). Reduced syntactic processing efficiency in older adults during sentence comprehension. Frontiers in Psychology, 9, 243.CrossRefGoogle ScholarPubMed
Zhu, Z., Yang, F., Li, D., Zhou, L., Liu, Y., Zhang, Y., & Chen, X. (2017). Age-related reduction of adaptive brain response during semantic integration is associated with gray matter reduction. Plos One, 12, e0189462.CrossRefGoogle ScholarPubMed
Zhu, Z., Zhang, J. X., Wang, S., Xiao, Z., Huang, J., & Chen, H.-C. (2009). Involvement of left inferior frontal gyrus in sentence-level semantic integration. NeuroImage, 47, 756763.CrossRefGoogle ScholarPubMed