Neural signatures of predictive language processing in Parkinson's disease with and without mild cognitive impairment

Cognitive deficits are common in Parkinson’s disease (PD), with some PD patients meeting criteria for mild cognitive impairment (MCI). An unaddressed question is whether linguistic prediction is preserved in PD. This ability is nowadays deemed crucial in achieving fast and efficient comprehension, and it may be negatively impacted by cognitive deterioration. To fill this gap of knowledge, we used event-related potentials (ERPs) to evaluate mechanisms of linguistic prediction in a sample of PD patients (on dopamine compensation) with and without MCI. To this end, participants read sentence contexts that were predictive or not about a sentence-final word. The final word appeared after 1 second, matching or mismatching the prediction. The introduction of the interval allowed to capture neural responses both before and after sentence-final words, reflecting semantic anticipation and processing. PD patients with normal cognition (N = 58) showed ERP responses comparable to those of matched controls. Specifically, in predictive contexts, a slow negative potential developed prior to sentence-final words, reflecting semantic anticipation. Later, expected words elicited reduced N400 responses (compared to unexpected words), indicating facilitated semantic processing. Besides, PD patients with MCI (N = 20) showed a prolongation of the N400 congruency effect (compared to matched PD patients without MCI), indicating that further cognitive decline impacts semantic processing. Finally, lower verbal fluency scores correlated with prolonged N400 congruency effects and with reduced pre-word differences in all PD patients (N = 78). This relevantly points to a role of deficits in temporal-dependent mechanisms in PD, besides prototypical frontal dysfunction, in altered semantic anticipation and semantic processing during sentence comprehension.

[1]  S. Hackley,et al.  Psychophysiological evidence for impaired reward anticipation in Parkinson’s disease , 2006, Clinical Neurophysiology.

[2]  Tamara Y. Swaab,et al.  Internal mechanisms underlying anticipatory language processing: Evidence from event-related-potentials and neural oscillations , 2017, Neuropsychologia.

[3]  Steven J. Luck,et al.  ERPLAB: an open-source toolbox for the analysis of event-related potentials , 2014, Front. Hum. Neurosci..

[4]  B. Schmand,et al.  Cognitive profile of patients with newly diagnosed Parkinson disease , 2005, Neurology.

[5]  M. Petrides,et al.  Neural Bases of Set-Shifting Deficits in Parkinson's Disease , 2004, The Journal of Neuroscience.

[6]  M. Kutas,et al.  Reading senseless sentences: brain potentials reflect semantic incongruity. , 1980, Science.

[7]  Moritz Grosse-Wentrup,et al.  Multisubject Learning for Common Spatial Patterns in Motor-Imagery BCI , 2011, Comput. Intell. Neurosci..

[8]  D. V. von Cramon,et al.  Syntactic language processing: ERP lesion data on the role of the basal ganglia , 2003, Journal of the International Neuropsychological Society.

[9]  Kara D. Federmeier,et al.  Aging in context: age-related changes in context use during language comprehension. , 2005, Psychophysiology.

[10]  Antal van den Bosch,et al.  Prediction During Natural Language Comprehension. , 2016, Cerebral cortex.

[11]  O. Monchi,et al.  Network basis of the dysexecutive and posterior cortical cognitive profiles in Parkinson's disease , 2019, Movement disorders : official journal of the Movement Disorder Society.

[12]  Fabrice Wendling,et al.  Detecting modular brain states in rest and task , 2019, Network Neuroscience.

[13]  Antoni Rodríguez-Fornells,et al.  Ahead of time: Early sentence slow cortical modulations associated to semantic prediction , 2019, NeuroImage.

[14]  Kara D. Federmeier,et al.  Contextual constraints on lexico-semantic processing in aging: Evidence from single-word event-related brain potentials , 2018, Brain Research.

[15]  Marta Kutas,et al.  Potato not Pope: human brain potentials to gender expectation and agreement in Spanish spoken sentences , 2003, Neuroscience Letters.

[16]  Ellen F. Lau,et al.  A cortical network for semantics: (de)constructing the N400 , 2008, Nature Reviews Neuroscience.

[17]  P. Silburn,et al.  A Neurophysiological Study of Semantic Processing in Parkinson’s Disease , 2016, Journal of the International Neuropsychological Society.

[18]  Kara D. Federmeier,et al.  Age-related and individual differences in the use of prediction during language comprehension , 2010, Brain and Language.

[19]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[20]  Colin M. Brown,et al.  Semantic Integration in Sentences and Discourse: Evidence from the N400 , 1999, Journal of Cognitive Neuroscience.

[21]  Brennan R. Payne,et al.  Aging, context processing, and comprehension , 2019, Psychology of Learning and Motivation.

[22]  L. Clare,et al.  Executive functions in Parkinson's disease: Systematic review and meta‐analysis , 2011, Movement disorders : official journal of the Movement Disorder Society.

[23]  D. Copland,et al.  Impaired semantic inhibition during lexical ambiguity repetition in Parkinson's disease , 2009, Cortex.

[24]  A. Rodríguez-Fornells,et al.  Electrophysiological correlates of semantic anticipation during speech comprehension , 2017, Neuropsychologia.

[25]  B. Murdoch,et al.  Semantic activation in Parkinson's disease patients on and off levodopa , 2009, Cortex.

[26]  Friedemann Pulvermüller,et al.  Behavioral / Cognitive Neural Correlates of Semantic Prediction and Resolution in Sentence Processing , 2017 .

[27]  M. Spitzer,et al.  Dopaminergic modulation of semantic network activation , 1996, Neuropsychologia.

[28]  J. Jankovic,et al.  Movement Disorder Society‐sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS‐UPDRS): Scale presentation and clinimetric testing results , 2008, Movement disorders : official journal of the Movement Disorder Society.

[29]  M. Basso,et al.  Verbal Fluency: Language or Executive Function Measure? , 2016, Applied neuropsychology. Adult.

[30]  C. Brunia,et al.  Waiting to perceive: Reward or punishment? , 2011, Clinical Neurophysiology.

[31]  Gene A. Brewer,et al.  Please Scroll down for Article the Quarterly Journal of Experimental Psychology Variation in Verbal Fluency: a Latent Variable Analysis of Clustering, Switching, and Overall Performance , 2022 .

[32]  Kara D. Federmeier,et al.  Age-related changes in the impact of contextual strength on multiple aspects of sentence comprehension. , 2012, Psychophysiology.

[33]  J. Hughes,et al.  Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[34]  Marta Kutas,et al.  CHAPTER 15 A Look around at What Lies Ahead: Prediction and Predictability in Language Processing , 2010 .

[35]  Wilson L. Taylor,et al.  “Cloze Procedure”: A New Tool for Measuring Readability , 1953 .

[36]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[37]  A. Clark Whatever next? Predictive brains, situated agents, and the future of cognitive science. , 2013, The Behavioral and brain sciences.

[38]  James L. McClelland,et al.  Modelling the N400 brain potential as change in a probabilistic representation of meaning , 2018, Nature Human Behaviour.

[39]  B. Murdoch,et al.  Dopamine and semantic activation: An investigation of masked direct and indirect priming , 2004, Journal of the International Neuropsychological Society.

[40]  Kara D. Federmeier,et al.  Multiple effects of sentential constraint on word processing , 2007, Brain Research.

[41]  F. Pulvermüller,et al.  Semantic Prediction in Brain and Mind , 2020, Trends in Cognitive Sciences.

[42]  D P Salmon,et al.  Patients with MCI and N400 or P600 abnormalities are at very high risk for conversion to dementia , 2008, Neurology.

[43]  Manuel Perea,et al.  EsPal: One-stop shopping for Spanish word properties , 2013, Behavior Research Methods.

[44]  Kara D. Federmeier,et al.  Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). , 2011, Annual review of psychology.

[45]  Brian Everitt,et al.  A systematic review and quantitative appraisal of fMRI studies of verbal fluency: Role of the left inferior frontal gyrus , 2006, Human brain mapping.

[46]  Kara D. Federmeier,et al.  A Rose by Any Other Name: Long-Term Memory Structure and Sentence Processing , 1999 .

[47]  Edward J. Golob,et al.  Event-related potentials accompanying motor preparation and stimulus expectancy in the young, young-old and oldest-old , 2005, Neurobiology of Aging.

[48]  Katherine A. DeLong,et al.  Predictability, plausibility, and two late ERP positivities during written sentence comprehension , 2014, Neuropsychologia.

[49]  M. Kutas,et al.  Altered N400 Congruity Effects in Parkinson’s Disease without Dementia , 2014 .

[50]  M. Bar Predictions in the brain : using our past to generate a future , 2011 .

[51]  Jaime Kulisevsky,et al.  Parkinson's disease‐cognitive rating scale: A new cognitive scale specific for Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

[52]  Murray Grossman,et al.  Age-Related Changes in Working Memory during Sentence Comprehension: An fMRI Study , 2002, NeuroImage.

[53]  R. Barker,et al.  Mild cognitive impairment in Parkinson disease , 2010, Neurology.

[54]  J. Gee,et al.  Grammatical and resource components of sentence processing in Parkinson’s disease , 2003, Neurology.

[55]  B. Murdoch,et al.  Decreased semantic competitive inhibition in Parkinson's disease: Evidence from an investigation of word search performance , 2010, International journal of speech-language pathology.

[56]  D. V. von Cramon,et al.  Syntactic comprehension in Parkinson's disease: investigating early automatic and late integrational processes using event-related brain potentials. , 2003, Neuropsychology.

[57]  Peter Hagoort,et al.  The Processing Nature of the N400: Evidence from Masked Priming , 1993, Journal of Cognitive Neuroscience.

[58]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[59]  Kara D. Federmeier Thinking ahead: the role and roots of prediction in language comprehension. , 2007, Psychophysiology.

[60]  J. Kulisevsky,et al.  The Free and Cued Selective Reminding Test in Parkinson's Disease Mild Cognitive Impairment: Discriminative Accuracy and Neural Correlates , 2020, Frontiers in Neurology.

[61]  Daniel Lakens,et al.  Will knowledge about more efficient study designs increase the willingness to pre-register? , 2016 .

[62]  B. Murdoch,et al.  The time course of semantic activation in Parkinson’s disease , 2004, Brain and Language.

[63]  C. Clarke,et al.  Systematic review of levodopa dose equivalency reporting in Parkinson's disease , 2010, Movement disorders : official journal of the Movement Disorder Society.

[64]  Joseph C. Griffis,et al.  Damage to white matter bottlenecks contributes to language impairments after left hemispheric stroke , 2016, NeuroImage: Clinical.

[65]  J. Kulisevsky,et al.  Mild cognitive impairment in Parkinson’s disease , 2019, Journal of Neural Transmission.

[66]  Marc D. Pell,et al.  How Parkinson's Disease Affects Non-verbal Communication and Language Processing , 2008, Lang. Linguistics Compass.

[67]  H. Michalewski,et al.  Age differences in the contingent negative variation (CNV): reduced frontal activity in the elderly. , 1980, Journal of gerontology.

[68]  J. Kulisevsky,et al.  Parkinson's disease‐cognitive rating scale: Psychometrics for mild cognitive impairment , 2013, Movement disorders : official journal of the Movement Disorder Society.

[69]  Falk Huettig,et al.  Four central questions about prediction in language processing , 2015, Brain Research.

[70]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[71]  Colin M. Brown,et al.  Anticipating upcoming words in discourse: evidence from ERPs and reading times. , 2005, Journal of experimental psychology. Learning, memory, and cognition.

[72]  Sophie Schwartz,et al.  Role of frontal versus temporal cortex in verbal fluency as revealed by voxel-based lesion symptom mapping , 2006, Journal of the International Neuropsychological Society.

[73]  A. Rodríguez-Fornells,et al.  Watching the brain during meaning acquisition. , 2007, Cerebral cortex.

[74]  M. Kutas,et al.  Brain potentials during reading reflect word expectancy and semantic association , 1984, Nature.

[75]  E. Tolosa,et al.  Clinical diagnostic criteria for dementia associated with Parkinson's disease , 2007, Movement disorders : official journal of the Movement Disorder Society.

[76]  C. Adler,et al.  MDS task force on mild cognitive impairment in Parkinson's disease: Critical review of PD‐MCI , 2011, Movement disorders : official journal of the Movement Disorder Society.

[77]  Marta Kutas,et al.  The impact of semantic memory organization and sentence context information on spoken language processing by younger and older adults: an ERP study. , 2002, Psychophysiology.

[78]  Gina R. Kuperberg,et al.  A Tale of Two Positivities and the N400: Distinct Neural Signatures Are Evoked by Confirmed and Violated Predictions at Different Levels of Representation , 2020, Journal of Cognitive Neuroscience.