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A Neurophysiological Study of Semantic Processing in Parkinson’s Disease

Published online by Cambridge University Press:  05 December 2016

Anthony J. Angwin*
Affiliation:
University of Queensland, School of Health and Rehabilitation Sciences, Brisbane, Australia
Nadeeka N.W. Dissanayaka
Affiliation:
University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia Neurology Research Centre, Royal Brisbane & Women’s Hospital, Brisbane, Australia
Alison Moorcroft
Affiliation:
University of Queensland, School of Health and Rehabilitation Sciences, Brisbane, Australia
Katie L. McMahon
Affiliation:
University of Queensland, Centre for Advanced Imaging, Brisbane, Australia
Peter A. Silburn
Affiliation:
University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia Neurology Research Centre, Royal Brisbane & Women’s Hospital, Brisbane, Australia
David A. Copland
Affiliation:
University of Queensland, School of Health and Rehabilitation Sciences, Brisbane, Australia University of Queensland, UQ Centre for Clinical Research, Brisbane, Australia
*
Correspondence and reprint requests to:Anthony Angwin, University of Queensland, School of Health and Rehabilitation Sciences, Brisbane, Queensland, 4072 Australia E-mail: a.angwin@uq.edu.au

Abstract

Objectives: Cognitive-linguistic impairments in Parkinson’s disease (PD) have been well documented; however, few studies have explored the neurophysiological underpinnings of semantic deficits in PD. This study investigated semantic function in PD using event-related potentials. Methods: Eighteen people with PD and 18 healthy controls performed a semantic judgement task on written word pairs that were either congruent or incongruent. Results: The mean amplitude of the N400 for new incongruent word pairs was similar for both groups, however the onset latency was delayed in the PD group. Further analysis of the data revealed that both groups demonstrated attenuation of the N400 for repeated incongruent trials, as well as attenuation of the P600 component for repeated congruent trials. Conclusions: The presence of N400 congruity and N400 repetition effects in the PD group suggests that semantic processing is generally intact, but with a slower time course as evidenced by the delayed N400. Additional research will be required to determine whether N400 and P600 repetition effects are sensitive to further cognitive decline in PD. (JINS, 2017, 23, 78–89)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2016 

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References

REFERENCES

Aarsland, D., Andersen, K., Larsen, J.P., Lolk, A., & Kragh-Sorensen, P. (2003). Prevalence and characteristics of dementia in Parkinson disease: An 8-year prospective study. Archives of Neurology, 60, 387392.CrossRefGoogle ScholarPubMed
Angwin, A.J., Arnott, W.L., Copland, D.A., Haire, M.P.L., Murdoch, B.E., Silburn, P.A., & Chenery, H.J. (2009). Semantic activation in Parkinson’s disease patients on and off levodopa. Cortex, 45, 950959.Google Scholar
Angwin, A.J., Chenery, H.J., Copland, D.A., Murdoch, B.E., & Silburn, P.A. (2005). Summation of semantic priming and complex sentence comprehension in Parkinson’s disease. Cognitive Brain Research, 25, 7889.Google Scholar
Angwin, A.J., Chenery, H.J., Copland, D.A., Murdoch, B.E., & Silburn, P.A. (2006a). The influence of dopamine on semantic activation in Parkinson’s disease: Evidence from a multi-priming task. Neuropsychology, 20, 299306.CrossRefGoogle Scholar
Angwin, A.J., Chenery, H.J., Copland, D.A., Murdoch, B.E., & Silburn, P.A. (2006b). Self-paced reading and sentence comprehension in Parkinson’s disease. Journal of Neurolinguistics, 19, 239252.Google Scholar
Angwin, A.J., Chenery, H.J., Copland, D.A., Murdoch, B.E., & Silburn, P.A. (2007). The speed of lexical activation is altered in Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 29, 7385.Google Scholar
Arnott, W.A., Chenery, H.J., Angwin, A.J., Murdoch, B.E., Silburn, P.A., & Copland, D.A. (2010). Decreased semantic competitive inhibition in Parkinson’s disease: Evidence from an investigation of word search performance. International Journal of Speech Language Pathology, 12(5), 437445.Google Scholar
Arnott, W.L., Chenery, H.J., Murdoch, B.E., & Silburn, P.A. (2001). Semantic priming in Parkinson’s disease: Evidence for delayed spreading activation. Journal of Clinical and Experimental Neuropsychology, 23(4), 502519.CrossRefGoogle ScholarPubMed
Arnott, W.A., Copland, D.A., Chenery, H.J., Murdoch, B.E., Silburn, P.A., & Angwin, A.J. (2011). The influence of dopamine on automatic and controlled semantic activation in Parkinson’s disease. Parkinson’s disease, 2011, 157072.Google Scholar
Baayen, R.H., Piepenbrock, R., & Gulikers, L. (1995). The CELEX Lexical Database. (Release 2 [CD-ROM]. Linguistic Data Consortium, Philadelphia: University of Pennsylvania.Google Scholar
Batig, W.F., & Montague, W.E. (1969). Category norms for verbal items in 56 categories: A replication and extension of the Connecticut category norms. Journal of Experimental Psychology, 80(3), 146.CrossRefGoogle Scholar
Bocanegra, Y., Garcia, A.M., Pineda, D., Buritica, O., Villegas, A., Lopera, F., & Ibanez, A. (2015). Syntax, action verbs, action semantics, and object semantics in Parkinson’s disease: Dissociability, progression, and executive influences. Cortex, 69, 237254.Google Scholar
Brandt, J., & Benedict, R.H. (2001). Hopkins Verbal Learning Test – Revised. Lutz, FL: Psychological Assessment Resources, Inc.Google Scholar
Chiang, H.-S., Mudar, R.A., Spence, J.S., Pudhiyidath, A., Eroh, J., DeLaRosa, B., & Hart, J. (2014). Age-related changes in feature-based object memory retrieval as measured by event-related potentials. Biological Psychology, 100, 106114.Google Scholar
Chiang, H.-S., Mudar, R.A., Pudhiyidath, A., Spence, J.S., Womack, K.B., Cullum, C.M., & Hart, J. (2015). Altered neural activity during semantic object memory retrieval in amnestic mild cognitive impairment as measured by event-related potentials. Journal of Alzheimer’s disease, 46, 703717.CrossRefGoogle ScholarPubMed
Colman, K.S.F., Koerts, J., Stowe, L.A., Leenders, K.L., & Bastiaanse, R. (2011). Sentence comprehension and its association with executive functions in patients with Parkinson’s disease. Parkinson’s disease, 2011, 213983.Google Scholar
Copland, D.A. (2003). The basal ganglia and semantic engagement: Potential insights from semantic priming in individuals with subcortical vascular lesions, Parkinson’s disease, and cortical lesions. Journal of the International Neuropsychological Society, 9(7), 10411052.Google Scholar
Copland, D.A., Sefe, G., Ashley, J., Hudson, C., & Chenery, H.J. (2009). Impaired semantic inhibition during lexical ambiguity repetition in Parkinson’s disease. Cortex, 45, 943949.Google Scholar
Cotelli, M., Borroni, B., Manenti, R., Zanetti, M., Arevalo, A., Cappa, S.F., & Padovani, A. (2007). Action and object naming in Parkinson’s disease without dementia. European Journal of Neurology, 14, 632637.Google Scholar
Davis, C. (2005). N-watch: A program for deriving neighbourhood size and other psycholinguistic statistics. Behavior Research Methods, 37(1), 6570.Google Scholar
Deacon, D., Hewitt, S., Yang, C.H., & Nagata, M. (2000). Event-related potential indices of semantic priming using masked and unmasked words: Evidence that the N400 does not reflect a post-lexical process. Cognitive Brain Research, 9, 137146.Google Scholar
De Letter, M., Van Borsel, J., & Santens, P. (2012). An electrophysiological investigation of the effects of levodopa on semantic comprehension of action words in Parkinson’s disease. Journal of Neurolinguistics, 25, 95103.Google Scholar
Ferree, T.C., Luu, P., Russell, G.S., & Tucker, D.M. (2001). Scalp electrode impedance, infection risk, and EEG data quality. Clinical Neurophysiology, 112, 536544.Google Scholar
Friederici, A.D., Kotz, S.A., Werheid, K., Hein, G., & Von Cramon, D.Y. (2003). Syntactic comprehension in Parkinson’s disease: Investigating early automatic and late integrational processes using event-related potentials. Neuropsychology, 17, 133142.Google Scholar
Gratton, G., Coles, M.G.H., & Donchin, E. (1983). A new method for off-line removal of ocular artefacts. Electroencephalography and Clinical Neurophysiology, 55, 468484.CrossRefGoogle Scholar
Grossman, M., Zurif, E., Lee, C., Prather, P., Kalmanson, J., Stern, M.B., & Hurtig, H.I. (2002). Information processing speed and sentence comprehension in Parkinson’s disease. Neuropsychology, 16, 174181.Google Scholar
Henry, J.D., & Crawford, J.R. (2004). Verbal fluency deficits in Parkinson’s disease: A meta-analysis. Journal of the International Neuropsychological Society, 10, 608622.Google Scholar
Hill, H., Strube, M., Roesch-Ely, D., & Weisbrod, M. (2002). Automatic vs. controlled processes in semantic priming-differentiation by event-related potentials. International Journal of Psychophysiology, 44, 197218.Google Scholar
Hughes, A.J., Daniel, S.E., Kilford, L., & Lees, A.J. (1992). Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: A clinico-pathological study of 100 cases. Journal of Neurology, Neurosurgery, and Psychiatry, 55(3), 181184.Google Scholar
Kehagia, A.A., Barker, R.A., & Robbins, T.W. (2010). Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. Lancet Neurology, 9, 12001213.Google Scholar
Kida, Y., Tachibana, H., Takeda, M., Yoshikawa, H., & Okita, T. (2007). Recognition memory for unfamiliar faces in Parkinson’s disease: Behavioral and electrophysiologic measures. Parkinsonism and Related Disorders, 13, 157164.Google Scholar
Kotz, S.A., & Friederici, A.D. (2003). Electrophysiology of normal and pathological language processing. Journal of Neurolinguistics, 16, 4358.Google Scholar
Kotz, S.A., Frisch, S., Von Cramon, D.Y., & Friederici, A.D. (2003). Syntactic language processing: ERP lesion data on the role of the basal ganglia. Journal of the International Neuropsychological Society, 9, 10531060.CrossRefGoogle ScholarPubMed
Kulisevky, J., & Pagonabarraga, J. (2009). Cognitive impairment in Parkinson’s disease: Tools for diagnosis and assessment. Movement Disorders, 24, 11031110.Google Scholar
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, 621647.Google Scholar
Kutas, M., Iragui, V.J., Niu, Y.Q., D’Avanzo, T.J., Yang, J.C., Salmon, D.P., & Olichney, J.M. (2013). Altered N400 congruity effects in Parkinson’s disease without dementia. In G.R. Mangun (Ed.), Cognitive electrophysiology of attention: Signals of the mind. (pp. 254267). Amsterdam: Elsevier, Inc. doi: 10.1016/B978-0-12-398451-7.00020-8 Google Scholar
Lewis, F.M., Lapointe, L.L., Murdoch, B.E., & Chenery, H.J. (1998). Language impairment in Parkinson’s disease. Aphasiology, 12(3), 193206.Google Scholar
Minamoto, H., Tachibana, H., Sugita, M., & Okita, T. (2001). Recognition memory in normal aging and Parkinson’s disease: Behavioral and electrophysiologic measures. Cognitive Brain Research, 11, 2332.Google Scholar
Mudar, R.A., Chiang, H.-S., Eroh, J., Nguyen, L.T., Maguire, M.J., Spence, J.S., & Hart, J. (2016). The effects of amnestic mild cognitive impairment on go/nogo semantic categorization task performance and event-related potentials. Journal of Alzheimer’s Disease, 50, 577590.CrossRefGoogle ScholarPubMed
Mudar, R.A., Chiang, H.-S., Maguire, M.J., Spence, J.S., Eroh, J., Kraut, M.A., & Hart, J. (2015). Effects of age on cognitive control during semantic categorization. Behavioural Brain Research, 287, 285293.Google Scholar
Nelson, D.L., McEvoy, C.L., & Schreiber, T.A. (2004). The University of South Florida free association, rhyme, and word fragment norms. Behavior Research Methods, Instruments and Computers, 36, 402407.Google Scholar
Olichney, J.M., Iragui, V.J., Salmon, D.P., Riggins, B.R., Morris, S.K., & Kutas, M. (2006). Absent event-related potential (ERP) word repetition effects in mild Alzheimer’s disease. Clinical Neurophysiology, 117, 13191330.CrossRefGoogle ScholarPubMed
Olichney, J.M., Morris, S.K., Ochoa, C., Salmon, D.P., Thal, L.J., Kutas, M., & Iragui, V.J. (2002). Abnormal verbal event related potentials in mild cognitive impairment and incipient Alzheimer’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 73, 377384.CrossRefGoogle ScholarPubMed
Olichney, J.M., Pak, J., Salmon, D.P., Yang, J., Gahagan, T., Nowacki, R., & Iragui-Madoz, V.J. (2013). Abnormal P600 word repetition effects in elderly persons with preclinical Alzheimer’s disease. Cognitive Neuroscience, 4, 143151.Google Scholar
Olichney, J.M., Taylor, J.R., Gatherwright, J., Salmon, D.P., Bressler, A.J., Kutas, M., & Iragui-Madoz, V.J. (2008). Patients with MCI and N400 or P600 abnormalities are at very high risk for conversion to dementia. Neurology, 70, 17631770.Google Scholar
Olichney, J.M., Van Petten, C., Paller, K.A., Salmon, D.P., Iragui, V.J., & Kutas, M. (2000). Word repetition in amnesia: Electrophysiological measures of impaired and spared memory. Brain, 123, 19481963.Google Scholar
Pagonabarraga, J., Kulisevsky, J., Llebaria, G., Garcia-Sanchez, C., Pascual-Sedano, B., & Gironell, A. (2008). Parkinson’s disease-Cognitive Rating Scale: A new cognitive scale specific for Parkinson’s disease. Movement Disorders, 23, 9981005.CrossRefGoogle Scholar
Pedersen, K.F., Larsen, J.P., Tysnes, O., & Alves, G. (2013). Prognosis of mild cognitive impairment in early Parkinson’s disease: The Norwegian ParkWest study. JAMA Neurology, 70, 580586.Google Scholar
Peran, P., Rascol, O., Demonet, J., Celsis, P., Nespoulous, J., Dubois, B., & Cardebat, D. (2003). Deficit of verb generation in nondemented patients with Parkinson’s disease. Movement Disorders, 18(2), 150156.Google Scholar
Portin, R., Laatu, S., Revonsuo, A., & Rinne, U. (2000). Impairment of semantic knowledge in Parkinson’s disease. Archives of Neurology, 57(9), 13381343.Google Scholar
Rodriguez-Ferreiro, J., Menendez, M., Ribacoba, R., & Cuetos, F. (2009). Action naming is impaired in Parkinson’s disease patients. Neuropsychologia, 47, 32713274.Google Scholar
Shao, Z., Janse, E., Visser, K., & Meyer, A.S. (2014). What do verbal fluency tasks measure? Predictors of verbal fluency performance in older adults. Frontiers in Psychology, 5, 772.Google Scholar
Smith, E.R., Chenery, H.J., Angwin, A.J., & Copland, D.A. (2009). Hemispheric contributions to semantic activation: A divided visual field and event-related potential investigation of time course. Brain Research, 1284, 125144.CrossRefGoogle ScholarPubMed
Tachibana, H., Miyata, Y., Takeda, M., Sugita, M., & Okita, T. (1999). Event-related potentials reveal memory deficits in Parkinson’s disease. Cognitive Brain Research, 8, 165172.Google Scholar
Tomlinson, C.L., Stowe, R., Patel, S., Rick, C., Gray, R., & Clarke, C.E. (2010). Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Movement Disorders, 25, 26492653.Google Scholar
Van Petten, C., Kutas, M., Kluender, R., Mitchiner, M., & McIsaac, H. (1991). Fractionating the word repetition effect with event-related potentials. Journal of Cognitive Neuroscience, 3, 131150.Google Scholar
Van Petten, C., & Luka, B.J. (2012). Prediction during language comprehension: Benefits, costs and ERP components. International Journal of Psychophysiology, 83, 176190.Google Scholar
Ye, Z., Milenkova, M., Mohammadi, B., Kollewe, K., Schrader, C., Dengler, R., & Munte, T.F. (2012). Impaired comprehension of temporal connectives in Parkinson’s disease – A neuroimaging study. Neuropsychologia, 50, 17941800.Google Scholar