Linguistic markers of story recall can help differentiate mild cognitive impairment from normal aging

Abstract

Mild cognitive impairment (MCI) involves a decline in episodic memory and, in many cases, language. Taler et al. (2021) developed a set of story recall materials that we expected to be sensitive to changes in language in normal aging and MCI. Here, we examined the lexical (word-level) contents of participants’ story recall responses from Taler et al. (2021). First, we compared the lexical features of story recall responses between young adults (YA; n = 22), healthy older adults (OA; n = 38), and people with MCI (n = 17) using the Linguistic Inquiry and Word Count (LIWC) program. Second, we explored the associations between these linguistic variables and story recall in each group. People with MCI produced fewer words overall, as well as higher proportions of verbs and pronouns on immediate recall compared to both YAs and OAs. OAs also produced higher proportions of auxiliary verbs than YAs. Story recall scores were positively correlated with total word count in YA and MCI groups. In YAs only, adjectives were positively correlated with recall. In OAs, recall scores were negatively correlated with proportion of verbs. Our results suggest that the LIWC program paired with our novel story recall task may help identify linguistic markers of normal aging and MCI. Some aspects of language use during story recall may also be related to episodic memory in cognitively healthy individuals and people with MCI. Our findings may have implications for the optimization of MCI screening tools to detect changes in language.

Keywords

Mild cognitive impairment / Aging / Story recall / Episodic memory

CRediT authorship contribution statement

Angela Katherine Boland: Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Writing-original draft, Writing-review & editing, Methodology. Adelaide Jensen: Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Writing-original draft, Writing-review & editing, Methodology. Patrick S. R. Davidson: Conceptualization, Methodology, Project administration, Resources, Supervision, Writing-review & editing, Investigation. Vanessa Taler: Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Writing-review & editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data availability

Data will be made available on request.

Acknowledgements

A portion of the data presented in this paper appears in the publication (Taler et al., 2021). Some of these data were also presented at La Société Québécoise pour la Recherche en Psychologie Congrès Annuel in Saint-Sauveur, Quebec, in May 2022 and at The Gerontological Society of America Annual Scientific Meeting in Indianapolis, Indiana, in November 2022. We have no conflicts of interest to disclose. We thank Dr. Christine Sheppard for her invaluable suggestions during data analysis.

Appendix A. Supplementary data

Supplementary data associated with this article can be found in the online version at doi:10.1016/j.laheal.2024.09.002.

References

[1] 2014 Alzheimer’s disease facts and figures. (2014). Alzheimer’s & Dementia, 10(2), e47-e92. https://doi.org/10.1016/j.jalz.2014.02.001

[2] Aickin M., & Gensler H. (1996). Adjusting for multiple testing when reporting research results: The Bonferroni vs Holm methods. American Journal of Public Health, 86(5), 5.

[3] Anderson N. D. (2019). State of the science on mild cognitive impairment (MCI. CNS Spectrums, 24(1), 78-87. https://doi.org/10.1017/S1092852918001347

[4] Asgari M., Kaye J., & Dodge H. (2017). Predicting mild cognitive impairment from spontaneous spoken utterances. Alzheimer’s & Dementia, 3(2), 219-228. https://doi.org/10.1016/j.trci.2017.01.006

[5] Asperholm M., Högman N., Rafi J., & Herlitz A. (2019). What did you do yesterday? A meta-analysis of sex differences in episodic memory. Psychological Bulletin, 145(8), 785-821. https://doi.org/10.1037/bul0000197

[6] Baddeley A. (2000). The episodic buffer: A new component of working memory? Trends in Cognitive Sciences, 4(11), 417-423. https://doi.org/10.1016/S1364-6613(00)01538-2

[7] Bao Z., Cao L., Han K., Li L., Hing J. W., Ooi V., Huang N., Feng L., Mahendran R., & Kua E. H. (2021). Nouns and verbs identify different subtypes of MCI. 〈https://doi.org/10.21203/rs.3.rs-1136322/v1〉.

[8] Beltrami D., Gagliardi G., Rossini Favretti R., Ghidoni E., Tamburini F., & Calzà L. (2018). Speech analysis by natural language processing techniques: A possible tool for very early detection of cognitive decline? Frontiers in Aging Neuroscience, 10, 369. https://doi.org/10.3389/fnagi.2018.00369

[9] Boyd R. L., Ashokkumar A., Seraj S., & Pennebaker J. W. (2022). The development and psychometric properties of LIWC-22 (pp. 1-47). Austin, TX: University of Texas at Austin.

[10] Buckner R. L. (2004). Memory and executive function in aging and AD: Multiple factors that cause decline and reserve factors that compensate. Neuron, 44(1), 195-208. https://doi.org/10.1016/j.neuron.2004.09.006

[11] Burke D. M., & Shafto M. A. (2004). Aging and language production. Current Directions in Psychological Science, 13(1), 21-24. https://doi.org/10.1111/j.0963-7214.2004.01301006.x

[12] Chapman S. B., Zientz J., Weiner M., Rosenberg R., Frawley W., & Burns M. H. (2002). Discourse changes in early Alzheimer disease, mild cognitive impairment, and normal aging. Alzheimer Disease & Associated Disorders, 16(3), 177.

[13] Cho S., Nevler N., Shellikeri S., Parjane N., Irwin D. J., Ryant N., Ash S., Cieri C., Liberman M., & Grossman M. (2021). Lexical and acoustic characteristics of young and older healthy adults. Journal of Speech, Language, and Hearing Research, 64( 2), 302-314. https://doi.org/10.1044/2020_JSLHR-19-00384

[14] Clayton J. A., & Tannenbaum C. (2016). Reporting sex, gender, or both in clinical research? JAMA, 316(18), 1863-1864. https://doi.org/10.1001/jama.2016.16405

[15] Dodge H., Nora M., Mattie G., Molly B., Adriana S., Oscar Y., Meysam A., & Jeffrey A. K. (2015). Social markers of mild cognitive impairment: Proportion of word counts in free conversational speech. Current Alzheimer Research, 12(6), 513-519.

[16] Duff M., & Brown-Schmidt S. (2012). The hippocampus and the flexible use and processing of language. Frontiers in Human Neuroscience, 6. 〈https://www.frontiersin.org/articles/10.3389/fnhum.2012.00069〉.

[17] Fällman K., Wressle E., Marcusson J., & Classon E. (2022). Swedish normative data and longitudinal effects of aging for older adults:The Boston Naming Test 30-item and a short version of the Token Test. Applied Neuropsychology: Adult. https://doi.org/10.1080/23279095.2022.2148106

[18] Ferretti M. T., Iulita M. F., Cavedo E., Chiesa P. A., Schumacher Dimech A., Santuccione Chadha A., Baracchi F., Girouard H., Misoch S., Giacobini E., Depypere H., & Hampel H. (2018). Sex differences in Alzheimer disease — The gateway to precision medicine. Nature Reviews Neurology, 14(8), Article 8. https://doi.org/10.1038/s41582-018-0032-9

[19] Fjell A. M., McEvoy L., Holland D., Dale A. M., & Walhovd K. B. (2014). What is normal in normal aging? Effects of aging, amyloid and Alzheimer’s disease on the cerebral cortex and the hippocampus. Progress in Neurobiology, 117, 20-40. https://doi.org/10.1016/j.pneurobio.2014.02.004

[20] Fleming V. B., & Harris J. L. (2008). Complex discourse production in mild cognitive impairment: Detecting subtle changes. Aphasiology, 22(7-8), 729-740. https://doi.org/10.1080/02687030701803762

[21] Foldi N. S. (2011). Getting the hang of it: Preferential gist over verbatim story recall and the roles of attentional capacity and the episodic buffer in Alzheimer disease. Journal of the International Neuropsychological Society, 17(1), 69-79. https://doi.org/10.1017/S1355617710001165

[22] Friedman D., de Chastelaine M., Nessler D., & Malcolm B. (2010). Changes in familiarity and recollection across the lifespan: An ERP perspective. Brain Research, 1310, 124-141. https://doi.org/10.1016/j.brainres.2009.11.016

[23] Gisev N., Bell J. S., & Chen T. F. (2013). Interrater agreement and interrater reliability: Key concepts, approaches, and applications. Research in Social and Administrative Pharmacy, 9(3), 330-338. https://doi.org/10.1016/j.sapharm.2012.04.004.

[24] Goulet M.-A., & Cousineau D. (2019). The power of replicated measures to increase statistical power. Advances in Methods and Practices in Psychological Science, 2, 199-213. https://doi.org/10.1177/2515245919849434

[25] Grady C. (2012). The cognitive neuroscience of ageing. Nature Reviews Neuroscience, 13(7), Article 7. https://doi.org/10.1038/nrn3256

[26] Hebert L. E., Weuve J., Scherr P. A., & Evans D. A. (2013). Alzheimer disease in the United States (2010-2050) estimated using the 2010 census. Neurology, 80(19), 1778-1783. https://doi.org/10.1212/WNL.0b013e31828726f5

[27] Holland D., Desikan R. S., Dale A. M., & McEvoy L. K. (2013). Higher Rates of Decline for Women and Apolipoprotein E ε4 Carriers. American Journal of Neuroradiology, 34(12), 2287-2293. https://doi.org/10.3174/ajnr.A3601

[28] JASP Team,JASP Version 0.14 [Computer software] (2023). https://jasp-stats.org/.

[29] Johnson D. K., Storandt M., & Balota D. A. (2003). Discourse analysis of logical memory recall in normal aging and in dementia of the Alzheimer type. Neuropsychology, 17(1), 82-92.

[30] Kemper S. (1986). Imitation of complex syntactic constructions by elderly adults. Applied Psycholinguistics, 7(3), 277-287. https://doi.org/10.1017/S0142716400007578

[31] Kemper S. (1992). Adults’ sentence fragments: Who, what, when, where, and why. Communication Research, 19(4), 444-458. https://doi.org/10.1177/009365092019004003

[32] Kintsch W. (1994). Text comprehension, memory, and learning. American Psychologist, 49, 294-303. https://doi.org/10.1037/0003-066X.49.4.294

[33] Kintsch W., & van Dijk T. A. (1978). Toward a model of text comprehension and production. Psychological Review, 85, 363-394. https://doi.org/10.1037/0033-295X.85.5.363

[34] Leal S. L., & Yassa M. A. (2019). Normal cognitive and brain aging. In The Oxford handbook of adult cognitive disorders (pp. 5-24). Oxford University Press. https://doi.org/10.1093/oxfordhb/9780190664121.001.0001.

[35] Lin K. A., Choudhury K. R., Rathakrishnan B. G., Marks D. M., Petrella J. R., & Doraiswamy P. M. (2015). Marked gender differences in progression of mild cognitive impairment over 8 years. Alzheimer’s & Dementia: Translational Research & Clinical Interventions, 1(2), Article 2. https://doi.org/10.1016/j.trci.2015.07.001.

[36] Lyons K., Kemper S., Labarge E., Ferraro F. R., Balota D., & Storandt M. (1994). Oral language and Alzheimer’s disease: A reduction in syntactic complexity. Aging, Neuropsychology, and Cognition, 1( 4), 271-281. https://doi.org/10.1080/13825589408256581

[37] Mielke M. M., Aggarwal N. T., Vila-Castelar C., Agarwal P., Arenaza-Urquijo E. M., Brett B., Brugulat-Serrat A., DuBose L. E., Eikelboom W. S., Flatt J., Foldi N. S., Franzen S., Gilsanz P., Li W., McManus A. J., van Lent D. M., Milani S. A., Shaaban C. E., Stites S. D., & and G. for, the D. and D. P. I. A. S. S. I. G. (2022). Consideration of sex and gender in Alzheimer’s disease and related disorders from a global perspective. Alzheimer’s & Dementia, 18(12), 2707-2724. https://doi.org/10.1002/alz.12662

[38] Nasreddine Z. S., Phillips N. A., Bédirian V., Charbonneau S., Whitehead V., Collin I., Cummings J. L., & Chertkow H. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695-699. https://doi.org/10.1111/j.1532-5415.2005.53221.x

[39] Park S., Roth N., Cosentino S., Perls T. T., Au R., Sebastiani P., & Andersen S. L. (2022). Lexical markers from paragraph recall predict cognitive status. Alzheimer’s & Dementia, 18(S7), Article S7. https://doi.org/10.1002/alz.061973

[40] Pennebaker J. W., Boyd R. L., Jordan K., & Blackburn K. (2015). The development and psychometric properties of LIWC2015. 〈https://repositories.lib.utexas.edu/handle/2152/31333〉.

[41] Petersen R. C., Caracciolo B., Brayne C., Gauthier S., Jelic V., & Fratiglioni L. (2014). Mild cognitive impairment: A concept in evolution. Journal of Internal Medicine, 275(3), 214-228. https://doi.org/10.1111/joim.12190

[42] Ploran E. J., & Wheeler M. E. (2017). Episodic memory ☆. In Reference module in neuroscience and biobehavioral psychology. Elsevier. https://doi.org/10.1016/B978-0-12-809324-5.02796-6.

[43] Reyna V. F. (2012). A new intuitionism: Meaning, memory, and development in Fuzzy-Trace Theory. Judgment and Decision Making, 7(3), 332-359.

[44] Reyna V. F., & Brainerd C. J. (1995). Fuzzy-trace theory: An interim synthesis. Learning and Individual Differences, 7(1), 1-75. https://doi.org/10.1016/1041-6080(95)90031-4

[45] Roark B., Mitchell M., Hosom J.-P., Hollingshead K., & Kaye J. (2011). Spoken language derived measures for detecting mild cognitive impairment. IEEE Transactions on Audio, Speech, and Language Processing, 19( 7), 2081-2090. https://doi.org/10.1109/TASL.2011.2112351

[46] Roark B., Hosom J., Mitchell M., & Kaye J. A. (2007). Automatically derived spoken language markers for detecting mild cognitive impairment.

[47] Ryan J. J., Kreiner D. S., Gontkovsky S. T., & Teichner G. (2023). Wechsler memory scale-fourth edition (WMS-IV) in the neuropsychological evaluation of patients diagnosed with probable Alzheimer’s disease. Applied Neuropsychology: Adult. https://doi.org/10.1080/23279095.2023.2164858

[48] Sacripante R., Girtler N., Doglione E., Nobili F., & Della Sala S. (2023). Forgetting rates of prose memory in mild cognitive impairment. Journal of Alzheimer’s Disease, 91(4), 1385-1394. https://doi.org/10.3233/JAD-220803

[49] Scheuringer A., Wittig R., & Pletzer B. (2017). Sex differences in verbal fluency: The role of strategies and instructions. Cognitive Processing, 18(4), 407-417. https://doi.org/10.1007/s10339-017-0801-1

[50] Shafto M. A., & Tyler L. K. (2014). Language in the aging brain: The network dynamics of cognitive decline and preservation. Science, 346(6209), 583-587. https://doi.org/10.1126/science.1254404

[51] Shibata D., Wakamiya S., Kinoshita A., & Aramaki E. (2016). Detecting Japanese patients with Alzheimer’s disease based on word category frequencies. In Proceedings of the clinical natural language processing workshop (ClinicalNLP) (pp. 78-85).

[52] Sokołowski A., Tyburski E., Sołtys A., & Karabanowicz E. (2020). Sex differences in verbal fluency among young adults. Advances in Cognitive Psychology, 16(2), 92-102. https://doi.org/10.5709/acp-0288-1

[53] Spieler D. H., & Griffin Z. M. (2006). The influence of age on the time course of word preparation in multiword utterances. Language and Cognitive Processes, 21(1-3), 291-321. https://doi.org/10.1080/01690960400002133

[54] Taler V., Davidson P. S. R., Sheppard C., & Gardiner J. (2021). A discourse-theoretic approach to story recall in aging and mild cognitive impairment. Aging, Neuropsychology, and Cognition, 28( 5), 762-780. https://doi.org/10.1080/13825585.2020.1821865

[55] Taler V., & Phillips N. A. (2008). Language performance in Alzheimer’s disease and mild cognitive impairment: A comparative review. Journal of Clinical and Experimental Neuropsychology, 30(5), Article 5. https://doi.org/10.1080/13803390701550128.

[56] Tausczik Y. R., & Pennebaker J. W. (2010). The psychological meaning of words: LIWC and computerized text analysis methods. Journal of Language and Social Psychology, 29(1), 24-54. https://doi.org/10.1177/0261927×09351676

[57] Uttl B. (2002). North American adult reading test: Age norms, reliability, and validity. Journal of Clinical and Experimental Neuropsychology, 24(8), 1123-1137. https://doi.org/10.1076/jcen.24.8.1123.8375

[58] Wang T., Lian C., Pan J., Yan Q., Zhu F., Ng M. L., … Yan N. (2019). Towards the speech features of mild cognitive impairment: Universal evidence from structured and unstructured connected speech of Chinese. Interspeech, 3880-3884. https://doi.org/10.21437/Interspeech.2019-2414

[59] Wechsler D. (1997). WMS-III administration and scoring manual. San Antonio, TX: The Psychological Corporation.