EEG oscillations during word processing predict MCI conversion to Alzheimer's disease

Ali Mazaheri, Katrien Segaert, John Olichney, Jin-Chen Yang, Yu-Qiong Niu, Kimron Shapiro, Howard Bowman

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Only a subset of mild cognitive impairment (MCI) patients progress to develop a form of dementia. A prominent feature of Alzheimer's disease (AD) is a progressive decline in language. We investigated if subtle anomalies in EEG activity of MCI patients during a word comprehension task could provide insight into the likelihood of conversion to AD. We studied 25 amnestic MCI patients, a subset of whom developed AD within 3-years, and 11 elderly controls. In the task, auditory category descriptions (e.g., ‘a type of wood’) were followed by a single visual target word either semantically congruent (i.e., oak) or incongruent with the preceding category. We found that the MCI convertors group (i.e. patients that would go on to convert to AD in 3-years) had a diminished early posterior-parietal theta (3–5 Hz) activity induced by first presentation of the target word (i.e., access to lexico-syntactic properties of the word), compared to MCI non-convertors and controls. Moreover, MCI convertors exhibited oscillatory signatures for processing the semantically congruent words that were different from non-convertors and controls. MCI convertors thus showed basic anomalies for lexical and meaning processing. In addition, both MCI groups showed anomalous oscillatory signatures for the verbal learning/memory of repeated words: later alpha suppression (9–11 Hz), which followed first presentation of the target word, was attenuated for the second and third repetition in controls, but not in either MCI group. Our findings suggest that a subtle breakdown in the brain network subserving language comprehension can be foretelling of conversion to AD.

Mild cognitive impairment (MCI) is a syndrome characterized by cognitive decline that although not interfering with daily life, is greater than expected given an individual's age. Roughly 60% of the individuals diagnosed with MCI progress to develop dementia within 5 years of MCI diagnosis (Gauthier et al., 2006; Portet et al., 2006). Identifying factors that predict conversion of MCI to dementia will lead the way to early pharmacological intervention, as well as secondary prevention by controlling risk factors such as blood pressure, inactivity, diet and cholesterol levels (Brookmeyer et al., 2016; Sjogren et al., 2006; Wiesmann et al., 2015).

The most prevalent underlying cause of dementia is Alzheimer's disease (AD). A prominent feature of AD symptomatology is a progressive cognitive decline in faculties such as learning and memory, executive control, and language (Ferris and Farlow, 2013; Vestal et al., 2006). The deterioration of language abilities has been proposed to be of particular clinical relevance in terms of tracking the progression from moderate to severe stages of AD (Ferris and Farlow, 2013). The objective of the current study was to investigate if neuronal activity of MCI patients during a word comprehension task provides insight into the likelihood of conversion to AD dementia.

We examined the electroencephalogram (EEG) of MCI patients, a subset of whom developed dementia within 3 years, and healthy controls, while they performed a language comprehension task. In this task, patients and controls heard auditory phrases describing a category (e.g. `a type of wood’, `a breakfast food’), each of which was followed by the visual presentation of a single target word, which either fit (congruent, i.e. oak, pancake) or did not fit (incongruent nouns) with the preceding category statement.

The lexical processing of a target word requires the reader to access a range of different kinds of information about the word in the mental lexicon, including phonological, morphological and syntactic information, as well as the word's semantic meaning. Early changes in EEG induced by target word presentation, irrespective of whether the word is congruent or not, have been suggested to be indicative of lexical processing (Huang et al., 2014; Ledoux et al., 2007). Lexical processing can be facilitated by repeated word presentation due to implicit memory for properties of the earlier presented word. Throughout the experiment we presented target words once, twice or three times. Changes in the EEG for congruent compared to incongruent target words are indicative of semantic or meaning processing. For congruent words, properties of the target word's meaning have been pre-activated and can be integrated with the preceding phrase, facilitating meaning processing.

The data used in the current investigation was part of a previously published study (Olichney et al., 2008) using the N400 and P600 event related potentials (ERPs) to investigate memory encoding and retrieval processing deficits as predictors for conversion to AD dementia.

We focused our investigation on induced power changes in oscillatory activity generated by the onset of the target word. We examined oscillatory activity in theta (3–5 Hz), alpha (~ 10 Hz) and beta (15–20 Hz) frequency ranges given that prior studies have implicated these bands in various aspects of language processing, including lexical and semantic processing (Bastiaansen et al., 2005; Bastiaansen et al., 2008; Davidson and Indefrey, 2007; Hagoort et al., 2004; Hermes et al., 2014; Lam et al., 2016), as well as access to stored information and integration of information (Klimesch, 2012; Obleser and Weisz, 2012; Strauss et al., 2014; Weiss and Mueller, 2012). Finally, given that language comprehension involves the interaction of different brain regions across the cortex (Hagoort, 2013; Hermes et al., 2014), we also examined cross-frequency interactions of power across different brain areas during word comprehension (Mazaheri et al., 2009; Mazaheri et al., 2010; Mazaheri et al., 2014a).
Original languageEnglish
Pages (from-to)188-197
JournalNeuroImage: Clinical
Early online date9 Oct 2017
Publication statusPublished - 1 Jan 2018


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