Semantic Processing of Spoken Words in Alzheimer's Disease: An
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Semantic Processing of Spoken Words in Alzheimer’s Disease: An Electrophysiological Study Antti Revonsuo, Raija Portin, Kirsi Juottonen, and Juha O. Rinne University of Turku, Finland Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/10/3/408/1758334/089892998562726.pdf by guest on 18 May 2021 Abstract ■ Patients suffering from Alzheimer’s disease (AD) have severe studies is whether word-elicited ERPs other than N400 remain difªculties in tasks requiring the use of semantic knowledge. normal in AD. In the present study our aim was to ªnd out The semantic deªcits associated with AD have been extensively whether the ERP waveforms N1, P2, N400, and Late Positive studied by using behavioral methods. Many of these studies Component (LPC) to semantically congruous and incongruous indicate that AD patients have a general deªcit in voluntary spoken words are abnormal in AD and whether such abnor- access to semantic representations but that the structure of the malities speciªcally reºect deªciencies in semantic activation representations themselves might be preserved. However, sev- in AD. Auditory ERPs from 20 scalp sites to semantically con- eral studies also provide evidence that to some extent semantic gruous and incongruous ªnal words in spoken sentences were representations in AD may in fact be degraded. Recently, a few recorded from 17 healthy elderly adults and 9 AD patients. The studies have utilized event-related brain potentials (ERPs) that early ERP waveforms N1 and P2 were relatively normal for the are sensitive to semantic factors in order to investigate the AD patients, but the N400 and LPC effects (amplitude differ- electrophysiological correlates of the semantic impairment in ence between congruous and incongruous conditions) were AD. Interest has focused on the N400 component, which is signiªcantly reduced. We interpret the present results as show- known to reºect the on-line semantic processing of linguistic ing that semantic-conceptual activation and other high-level and pictorial stimuli. The results from studies of N400 changes integration processes are defective in AD. However, a word in AD remain somewhat controversial: Some studies report congruity effect earlier than N400 (phonological mismatch normal or enlarged N400 components in AD, whereas others negativity), reºecting lexical selection processes, is at least to report diminished ones. One issue not reported in previous some extent preserved in AD. ■ a variety of behavioral tasks such as naming, generating INTRODUCTION deªnitions, real/unreal object decision, and forced- One of the principal cognitive deªcits associated with choice questions about the appearance and functional AD is the impaired performance of AD patients in a attributes of objects and animals. AD patients were se- variety of semantic tasks. The patients have difªculties in verely impaired on both verbal and visual tasks and word ªnding (poverty of content words in spontaneous disproportionately impaired on items concerned with speech, decreased ability to generate instances of a given animate objects. The authors interpret their ªndings as category, and difªculties in object naming and naming to indicative of disruption at the structural level of visual deªnition), deªcient knowledge of concept meaning representation where the visual features and spatial re- (loss or disrupted organization of attribute knowledge), lations of objects are represented and at the phonologi- and anomalies in the effects of semantic context (e.g., cal output level where object names are stored for abnormal semantic priming in lexical decision)(Chert- speech production. However, because the patients per- kow & Bub, 1990; Chertkow, Bub, & Seidenberg, 1989; formed relatively well in some tasks not requiring effort- Chertkow et al., 1994; for a review, see Nebes, 1989). It ful processing, the authors conclude that semantic is unclear whether these impairments are due to a genu- networks are partly preserved in AD and that the pa- ine disruption of semantic memory or whether they tients can access semantic knowledge to some degree in merely indicate a difªculty in effortful, voluntary access an indirect way. Laatu, Portin, Revonsuo, Tuisku, and to semantic representations (Bayles, Tomoeda, Kaszniak, Rinne (1997) investigated whether AD patients are able & Trosset, 1991; Chan et al., 1993; Hodges, Salmon, & to get voluntary access to semantic representations if the Butters, 1992; Nebes, 1994). Recent studies show that AD retrieval demands of a task are gradually eased without patients probably have a combined access and storage essentially changing the nature of the information to be deªcit. Daum, Riesch, Sartori, and Birbaumer (1996) used retrieved. In some tasks the deªcits persisted even in © 1998 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 10:3, pp. 408–420 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892998562726 by guest on 28 September 2021 passive recognition and forced-choice tasks. The authors’ congruous or incongruous with the phrase. Visual in- conclusion was that AD patients have a generalized ac- spection of the ERPs to target words showed that the cess deªcit but some indications of a storage deªcit as N400 effect (amplitude difference between ERPs to con- well. gruous and incongruous words) was smaller for the AD These observations concerning the existence of se- patients than for age-matched controls. The N400 was mantic access and storage deªcits in AD are exclusively delayed and smaller for the elderly controls compared based on behavioral measures of semantic function, with the young. However, no statistical analyses of the which do not allow observation of cognitive processes effects were presented. In the study of Schwartz, Kutas, while they occur, but only as they are inferred from Butters, Paulsen, and Salmon (1996), the experimenter overt behavior. However, ERPs provide us with a fresh uttered the name of a category, which was followed after Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/10/3/408/1758334/089892998562726.pdf by guest on 18 May 2021 methodological approach for the measurement of the about 1 sec by a visually presented target word that was on-line semantic processing of linguistic stimuli in brain- the written name of an object. Reaction times and ERPs injured patients. Especially the N400 component of the were recorded. AD patients showed large behavioral ERPs is modulated by semantic factors (Kutas & Hillyard, priming effects (faster responses to related than to un- 1980; for a review, see Hagoort & Kutas, 1994). The N400 related target words). The amplitude of the N400 effect is a negative-going wave between 300 and 600 msec (difference between ERPs to related and unrelated target poststimulus, and its scalp distribution is broad. N400 words) was, however, much smaller in the AD group and amplitude to a stimulus word is modulated by the se- peaked later than in the young and elderly control mantic expectancy (“cloze probability”) and congruity of groups. All groups showed similar patterns of ERP re- the word with the preceding semantic context. The sponses to prime words at different levels of category words most expected elicit a minimal N400, whereas the (superordinate, basic, or subordinate). According to the ones semantically incongruous and least expected elicit authors, this result indicates that the structure of seman- the largest N400 amplitudes. A standard interpretation of tic representations in AD patients is preserved at least to the N400 effect has been that it is sensitive to attention- some extent. demanding semantic integration processes, not automat- The N400 is elicited by semantically incongruous and ic aspects of lexical access (Brown & Hagoort, 1993). unexpected ªnal words in written (Kutas & Hillyard, Recent studies show that N400-like waveforms are elic- 1980) and spoken (McCallum, Farmer, & Pocock, 1984) ited from pictorial as well as linguistic stimuli (Ganis, sentences. In a recent study involving AD patients (Ham- Kutas, & Sereno, 1996; Holcomb & McPherson, 1994; berger, Friedman, Ritter, & Rosen, 1995), the ªnal words Nigam, Hoffman, & Simons, 1992; Pratarelli, 1994). These of the sentence belonged to one of four stimulus types, ªndings suggest that the N400 might largely reºect some which varied as a function of semantic relatedness to a kind of semantic search in a common modality-inde- highly expected word. The sentences and ªnal words pendent conceptual-semantic network. The issue be- were presented visually to six AD patients and to old and tween these two interpretations of N400 remains young control subjects. The N400 amplitude varied as a unresolved (Osterhout & Holcomb, 1995); assigning cog- function of semantic relatedness in young controls and nitive functions to ERPs is, in general, theoretically prob- AD patients. The elderly control subjects showed no lematic (Rugg & Coles, 1995). such orderly variation but instead showed an equally ERPs can be used to investigate the semantic process- large N400 to all kinds of unexpected ªnal words. In a ing of words in patients with linguistic or semantic simultaneous behavioral task the AD patients had difªcul- deªcits (Hagoort, Brown, & Swaab, 1996; Revonsuo & ties in distinguishing between two of the four stimulus Laine, 1996). ERPs can provide us with information about types: the best completion and its semantic associations. language processing in real time and with great temporal Thus the patients’ ERPs actually