DOI: 10.1093/brain/awg243 Advanced Access publication August 5, 2003 Brain (2003), 126, 2419±2430 Idiom comprehension in Alzheimer's disease: the role of the central executive Costanza Papagno,1 Federica Lucchelli,2 Silvia Muggia1 and Silvia Rizzo3 di Psicologia, UniversitaÁ di Milano-Bicocca, di Neurologia, Azienda Ospedaliera Ospedale Niguarda Ca' Granda, Milano, 3Dipartimento di Psicologia, UniversitaÁ di Palermo, Palermo, Italy 1Dipartimento 2Divisione Summary Idiom comprehension of 15 patients with mild probable Alzheimer's disease was examined by means of a sentence-to-picture matching task. Patients had to choose between two pictures, one representing the ®gurative and the other the literal interpretation. They were also submitted to a literal sentence comprehension test and to a pencil-and-paper dual task. Whereas literal comprehension was normal in seven subjects and mildly impaired in the others, idiom comprehension was very poor in all of them and correlated with the performance on the dual task. When the idiom test was repeated using an unrelated situation as an alternative to the picture representing the ®gurative meaning, performance signi®cantly improved. It was hypothesized that the response in the sentence-to-picture matching task in the case of idioms requires sentence processing followed by the suppression of the literal interpretation. Alzheimer's Correspondence to: Costanza Papagno, Dipartimento di Psicologia, UniversitaÁ di Milano-Bicocca, Piazza dell'Ateneo Nuovo 1, Edi®cio U6, 20126 Milano, Italy E-mail: [email protected] disease patients proved to be unable to inhibit the literal meaning, although they had not lost the idiomatic meaning. In a second experiment, 15 Alzheimer's disease patients with a comparable level of cognitive impairment were submitted to the same idiom comprehension test, and to a test of verbal explanation of the idioms. The results showed signi®cantly better performance in the oral task than in the sentence-to-picture matching task. In oral explanation, however, Alzheimer's disease patients also produced some literal interpretation whenever this represented a possible situation in the real world. We suggest that, during idiom interpretation, the literal meaning needs to be suppressed in order to activate the ®gurative meaning, and we stress the fact that both linguistic and extralinguistic factors must be taken into account to explain idiom interpretation. Keywords: idiom; central executive; suppression; Alzheimer's disease Abbreviations: MODA = Milan Overall Dementia Assessment Introduction An aspect of linguistic communication is the use of ®gurative expressions, the meaning of which differs from the literal meaning of their component words; examples of these expressions are proverbs, hyperbole, metaphors and idioms. Two aspects concerning ®gurative language have been studied in detail: linguists have addressed problems related to the mechanisms involved in the interpretation of ®gurative language, and neuropsychologists have been concerned with its neural correlates. These expressions, however, do not constitute a homogeneous group, and idioms, metaphors, proverbs etc. have different characteristics. Idioms are among the most common forms of ®gurative language. They are typically described as frozen phrases whose meanings are stipulated directly in a mental lexicon, and the speaker's meaning cannot be derived from an analysis of the words' typical meanings. Many idioms, however, are more complex Brain 126 ã Guarantors of Brain 2003; all rights reserved and dynamic (Glucksberg et al., 1993). They range from expressions that are almost like long words (e.g. `by and large') to expressions that are like metaphors (e.g. `skate on thin ice'). In between there is the majority of idioms, in particular verbal idioms, that are processed syntactically and semantically, and accordingly can undergo syntactic and semantic variations. Neuropsychological studies on ®gurative language comprehension in brain-damaged patients concern mainly metaphors. There is, however, some information available on idioms, suggesting that patients with left hemisphere damage outperform right-brain-damaged patients in ®gurative sentence comprehension (Foldi et al., 1983; Van Lancker and Kempler, 1987; Kempler and Van Lancker, 1993; Burgess and Chiarello, 1996), even though psycholinguistic models all stress the importance of lexical knowledge (Swinney and 2420 Costanza Papagno et al. Table 1 Clinical and demographic data of the Alzheimer's disease patients: Experiment 1 Patient Age (years) Education (years) Gender MODA (normal values >89.1) Verbal ¯uency Visuoperceptual tests Stroop test 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 75 83 76 68 73 58 87 55 75 76 69 71 75 59 76 12 8 8 8 5 17 8 5 12 6 8 5 5 5 17 F F F M F F F F F F F F F M M 63.9 89.1 73.9 80.2 82.3 81.7 67.3 79.0 78.1 76.0 88.9 85.6 76.2 72.4 83.7 0 4 1 1 2 2 0 2 4 1 4 2 4 2 1 2 3 4 3 4 2 1 4 2 1 2 3 0 3 2 0 4 1 1 0 Equivalent scores are reported for verbal ¯uency, the Stroop test and visuoperceptual abilities (range 0± 4, where 0 corresponds to a score within the lowest 5% of the normal population, 4 is equal to/better than the median of normal population and 1, 2 and 3 are intermediate between 0 and 4 on a quasiinterval scale). Visuoperceptual abilities were tested in some patients with the Street test and in others with the Line Orientation Judgement test. M = male; F = female. Cutler, 1979; Tabossi and Zardon, 1995) and increasing evidence indicates the involvement of syntactic processing (Peterson et al., 2001) in the comprehension of idioms. There are, in our opinion, many limitations in previous neuropsychological studies on idioms. First, even if the literal and non-literal sentences were matched in structure, items were not chosen on the basis of their intrinsic linguistic features, and idioms, proverbs and courtesy phrases were considered together as `familiar language' (Van Lancker and Kempler, 1987; Kempler et al., 1999). The severity of aphasia and the modalities of assessment are not always described; the time of testing with respect to the time of onset of aphasia was variable and it is not clear whether patients underwent language rehabilitation; other neuropsychological de®cits are not reported; and the number of stimuli was limited. Moreover, in one of these studies (Van Lancker and Kempler, 1987), the performance of aphasic patients cannot be considered normal since their score was ~72% correct for idioms, compared with the controls' performance of 97.3%. The same aphasic subjects scored 90% correct on word comprehension. Papagno and colleagues (Papagno et al., 2002) and Papagno and Tabossi (2002) produced data which do not support the right hemisphere hypothesis. In both studies, a sentence-to-picture matching task was used for idiomatic and literal sentences. A homogeneous class of expressions was selected. These were non-ambiguous, opaque idioms; the meaning could not be directly derived from the ®gure involved and the literal interpretation was implausible because it had no meaning (for example, the idiom `venire alle mani' literally means `to come to the hands') (Nunberg et al., 1994). In the ®rst study, repetitive transcranial magnetic stimulation was used to evaluate the neural correlates of idiom comprehension. It was found that only left hemisphere stimulation increased reaction times and reduced accuracy in a task in which participants had to choose between a literal and a ®gurative representation of the idiomatic sentence. In the second study (Papagno and Tabossi, 2002), ten aphasic left-brain-damaged subjects were submitted to the same tests. They showed a performance in idiom comprehension that was signi®cantly impaired compared with that of a matched group of normal controls, even when aphasic de®cits were mild. These dif®culties seem to be due, to a large extent, to the fact that patients, unlike unimpaired listeners, rely on a literal-®rst strategy in the interpretation of idioms, and access a ®gurative interpretation only when the linguistic analysis fails to yield acceptable results (Bobrow and Bell, 1973). As far as patients with Alzheimer's disease are concerned, it has been suggested that their behaviour is similar to that of right-brain-damaged patients (Winner and Gardner, 1977). It is not clear which expressions were used, how severe their dementia was and how it was tested. Kempler and colleagues examined 29 patients with probable Alzheimer's disease ranging from mild (Mini-Mental State Examination score 28) to severe (Mini-Mental State Examination score 2); they were given tests of words, idioms, proverbs (overall, ten stimuli) and novel phrase comprehension (Kempler et al., 1988). In the ®gurative language comprehension task, no alternative corresponding to the literal interpretation was available, but only a referential representation of one word in the stimulus (concrete response). The results showed that Alzheimer's disease patients had dif®culty interpreting abstract meanings: when faced with alternative interpretations of familiar phrases, they chose concrete responses, suggesting that they were using lexical (single-word), referential meaning to Idiom comprehension in Alzheimer's 2421 Fig. 1 example of the idiom comprehension (sentence-to-picture matching) task. (A) The alternative corresponds to the literal interpretation. (B) The alternative corresponds to a sentence including a word contained in the idiom. This ®gure can be viewed in colour as supplementary data at Brain Online. interpret the phrases (Kempler et al., 1988). Familiar phrases are considered as psychological `chunks' similar to words, perceived and understood as wholes, without analysis of constituent parts taking place at all. Although we disagree with this interpretation and suggest that idioms undergo processes very similar to those involved in the comprehension of literal expressions, in particular a full syntactic analysis (C.Papagno, P.Tabossi, M.R.Colombo, P.Zannetti, unpublished results; Peterson et al., 2001), we accept that idiom comprehension can be impaired for other reasons, apart from lexical±semantic and syntactic de®cits. In a recent study on Alzheimer's disease patients, it was shown that the decline of ®gurative language (assessed by means of an oral explanation task of metaphors and idioms) is not an early symptom of dementia, can be preserved longer compared with propositional language, and can occur independently of the impairment of propositional language (Papagno, 2001). Idioms were both ambiguous and non-ambiguous, decomposable and non-decomposable, frozen and unfrozen. Performance on the idiom comprehension test was contrasted with performance on the Token Test. There were, however, very few patients with an impairment of ®gurative language but normal propositional language. It was suggested that an idiom needs to be present as a whole in the subject's semantic store, and then it must be correctly accessed and retrieved. Semantic memory and executive functions, therefore, seem to 2422 Costanza Papagno et al. which corresponds to a mild degree of cognitive impairment, were included in the study. Other criteria of inclusion were (i) the absence of previous neurological diseases, (ii) the absence of lesion on the CT scan, and (iii) a minimum of 3 years of education. Demographic and clinical data for the 15 Alzheimer's disease patients are reported in Table 1. They all gave informed consent to participate in the study. Procedure Fig. 2 Example of the literal sentence comprehension task. be involved. Consistent results were found by Papagno and Vallar (2001), investigating the ability of a patient with Down syndrome to appreciate non-literal and literal aspects of language. Whereas the latter was largely preserved, the former was defective. Some executive aspects of working memory were also impaired. What could be taken for certain in this patient was that impaired appreciation of metaphor and idioms could not be interpreted in terms of syntactic and lexical±semantic aspects of language comprehension, but might involve executive functions. Patients with Alzheimer's disease have impaired executive functions, even in the early stage (Baddeley et al., 1997). Therefore, we decided to explore idiom comprehension in this group of subjects, given that Alzheimer's disease patients with no de®cit in propositional language comprehension but impaired ®gurative language comprehension have been found (Papagno, 2001). In these cases (impaired idiom comprehension, normal literal comprehension), dif®culties in idiom comprehension cannot be attributed to lexical±semantic and syntactic de®cits. In particular, we examined the relation between idiomatic and literal language in Alzheimer's disease patients and the role of executive functions in idiom comprehension. Experiment 1 Subjects Fifteen patients (12 women and three men, mean age 71.73, SD 8.86; years of education 8.6, SD 4.12) with probable Alzheimer's disease were selected on the basis of their clinical history, their CT or MRI ®ndings and their performance on the Milan Overall Dementia Assessment (MODA; Brazzelli et al., 1994). Only patients with a score >63/100, Forty unambiguous verbal idioms were selected (see Appendix). They were rated as familiar by a group of 45 healthy subjects from different parts of Italy (31 women and 14 men, age 22±65 years), who had to judge whether each idiom was unknown (score 0), known but not sure about the meaning (score 1), familiar, with a well-known meaning (score 2), or highly familiar (score 3). Idioms were unambiguous: either they were ill-formed from a syntactical point of view (some Italian idioms contain a syntactic violation) or their literal interpretation was unlikely, because it made no sense (as in the example above, `venire alle mani') or the situation was implausible in the real world (e.g. `spremersi le meningi', which means `to squeeze one's own meninges'). In a ®rst version, for each idiom, two line drawings were created, one representing the idiomatic interpretation and the other representing as well as possible the literal interpretation (Fig. 1A). In a second version, the test was administered again with two alternatives, but the picture representing the literal interpretation was replaced by one representing an unrelated situation, which was de®ned by a sentence containing one word of the idiomatic expression (for example, when the idiomatic expression was `to have a green thumb', the alternative was a man hurting his thumb) (Fig. 1B). Each patient performed both versions. Tests Patients performed three tasks. The order of presentation was counterbalanced across participants. Idiom comprehension This was a sentence-to-picture matching task: the examiner read a sentence corresponding to an idiom to the patient, who chose between two pictures. Patients' performance on this task was compared with the performance of a group of 15 elderly healthy participants, matched for age and educational level. Literal sentence comprehension (Parisi and Pizzamiglio, 1970) This test included 80 items. The patient was shown a pair of pictures while one sentence was read to him. One of the Idiom comprehension in Alzheimer's 2423 Table 2 Results of tests in the Alzheimer's disease patients: Experiment 1 Patient 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Dual task (normal value 91.99 6 11.10) Literal sentences Idioms Literal/®gurative Figurative/unrelated 0.37 (±1.24) 0.82 (0.68) 0.89 (0.98) 0.48 (0.76) 0.99 (1.41) 0.86 (0.85) 0.79 (0.55) 0.125 (±2.28) 0.68 (0±08) 0.72 (0.25) 0.65 (±0.04) 0.55 (±0.46) 0.81 (0.64) 0.76 (0.42) 0.40 (±1.11) 60/80 (0.68) 74/80 (0.90) 76/80 (1.1852) 75/80 (1.0463) 69/80 (0.213) 59/80 (±1.1759) 66/80 (±0.203) 51/80 (±2.2871) 72/80 (0.6296) 62/80 (±0.7593) 74/80 (0.907) 71/80 (0.4907) 66/80 (±0.2037) 64/80 (±0.4815) 73/80 (0.7685) 15/40 (±0.71) 29/40 (±1.044) 34/40 (1.671) 18/40 (±0.334) 24/40 (0.417) 34/40 (1.671) 19/40 (±0.208) 9/40 (±1.4622) 18/40 (±0.3342) 15/40 (±0.71) 17/40 (±0.4595) 16/40 (±0.5849) 30/40 (1.1697) 22/40 (0.1671) 10/40 (±1.3368) 18/40 (±2.9057) 34/40 (0.1664) 38/40 (0.9344) 37/40 (0.7424) 32/40 (±0.2176) 37/40 (0.7424) 33/40 (±0.0256) 29/40 (±0.7936) 31/40 (±0.4096) 35/40 (0.3584) 39/40 (1.1265) 38/40 (0.9344) 34/40 (0.1664) 32/40 (±0.2176) 30/40 (±0.6016) Figures in parentheses are Z scores. pictures was correctly described by the sentence; the other corresponded to a sentence that was identical except for a detail (i.e. `the boy draws' versus `the boy will draw'). The sentences were matched, as far as possible, in length and complexity to idiomatic sentences. As no control subject scored <70 on this task in the original study and in a subsequent one (Vallar et al., 1988), the score of 70 was taken as the cut-off point (Fig. 2). Pencil-and-paper dual task (Baddeley et al., 1997) After being tested for a baseline span (the maximum length at which the patient recalled three lists without errors), patients were presented with lists of digits at their own span for a period of 2 min. Patients were then required to cross out, in a speci®c sequence, boxes (1 cm square) which had been linked to form a path laid out on an A4-size sheet of white paper over a 2-min interval. Finally, the two tasks were combined (digit span and tracking) for 2 min. A score combining the performance on the two tasks was given (control mean = 91.99 6 11.10). This test was chosen because it proved to be particularly sensitive to early dysexecutive changes in Alzheimer's disease patients. Results The results for the 15 patients in the three tests are shown in Table 2. The mean number of correct responses in idiom comprehension when a literal foil was used was 20.67 (SD 7.97), whereas for the 15 healthy participants the mean number of correct responses was 34.53 (4.37). The t-test showed that the difference between Alzheimer's disease and control subjects was highly signi®cant [t(14) = ±5.963, P < 0.0001]. Sentence comprehension proved to be preserved in seven patients and mildly impaired in the others, with the exception of Patients 6 and 8, whose impairment was moderate. Performance on idiom comprehension was correlated with that on the dual-task (rS = 0.89, P < 0.001), whereas there was no correlation between the former and the degree of cognitive decline, as assessed by the MODA (rS = ±0.26, P = 0.92) or sentence comprehension (rS = 0.24, P = 0.37). Finally, sentence comprehension was not correlated either 2424 Costanza Papagno et al. Table 3 Clinical and demographic data for the Alzheimer's disease patients: Experiment 2 Patient Age (years) Education (years) Gender MODA (normal values >89.1) Verbal ¯uency Visuoperceptual tests 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 76 79 84 82 85 79 78 78 67 69 56 76 65 77 82 5 17 3 3 5 5 12 5 13 5 8 8 13 11 6 M F F F F M M F F F M M F F F 80.6 77.8 82.7 85.4 77.9 85.6 85.6 86.4 79.9 82.2 78.7 83.9 79.8 86.5 74.3 4 1 4 1 0 4 4 4 4 3 1 1 0 3 1 4 3 4 2 1 4 4 4 3 4 4 1 0 2 1 Stroop test 0 For explanation see footnote of Table 1. with dual-task performance (rS = 0.16, P = 0.54) or with cognitive decline (rS = 0.41, P = 0.13). We submitted 20 normal subjects to a rating task to check the plausibility of the pictures representing the literal interpretations. The subjects were asked to rate how well the picture corresponding to the literal interpretation of the idiom matched the sentence read by the examiner. A score ranging from 0 to 7 was assigned, where 0 meant `not at all' and 7 `perfectly'. A correlation analysis indicated that the more implausible an idiomatic sentence is as a linguistic description of the literal picture, the more likely it is that, upon presentation of that sentence, the patient will select the idiomatic picture (rS = ±0.32, P < 0.05). In contrast, there was no effect of familiarity in this task (rS = 0.02, P = 0.87). When the test was re-administered in the second version (one picture representing the idiomatic interpretation and the other representing an unrelated situation including a word contained in the idiom), performance signi®cantly improved (mean of correct responses 33.13, SD 5.20) [t(14) = ±6.38, P < 0.0001], showing that patients had a good knowledge of the meaning of the idiom, despite their poor performance in the previous task. Every item that was selected correctly when the alternative was the literal interpretation was also chosen correctly when the alternative was the unrelated situation, demonstrating a consistent response of the patient, who was not performing at chance. Discussion Patients chose the literal interpretation when the corresponding picture was highly plausible but chose the idiomatic interpretation when the alternative represented an unrelated situation, even when the distractor corresponded to a sentence including a word contained in the idiom. This means that Alzheimer's disease patients know the meaning of the idiom, but the literal interpretation, which is also activated, strongly interferes with it; it also means that patients are not picking the literal interpretation on the basis of a single word in the idiom. It seems as if patients are unable to suppress the literal interpretation when there is an overt representation of it. We suggest that the activation of the literal interpretation is stronger or perhaps quicker than the activation of the idiomatic meaning, as hypothesized by Bobrow and Bell (1973), in contrast with the conclusion drawn with normal subjects (Gibbs, 1980). The interference produced by the literal interpretation is similar to that observed in the Stroop test: the choice of the literal representation can be due to the greater automaticity of the inhibition of the response with respect to that actually requested (MacLeod, 1991). It has been demonstrated that Alzheimer's disease patients produce signi®cantly larger interference effects with the Stroop ColorWord Test than comparable normal people (Bondi et al., 2002) To further investigate this possibility (interference of the literal interpretation), we selected another group of Alzheimer's disease patients, comparable with respect to their degree of cognitive impairment, and we submitted them to a second experiment. The hypothesis was that when a verbal explanation is required, people are not `offered' an external literal interpretation but generate their own response internally. Indeed, the representation of the literal meaning could reinforce the literal interpretation, which seems to take place. If the idiomatic meaning were unknown, a greater number of unrelated responses would be expected, the literal ones being produced only in the case of a highly plausible meaning. Experiment 2 Subjects Fifteen Alzheimer's disease patients, ®ve men and 10 women (mean age 75.53 years, SD 7.98, range 56±85; years of education 7.93, SD 4.26, range 3±17), entered the study. They Idiom comprehension in Alzheimer's 2425 Table 4 Results of the tests in Alzheimer's disease patients: Experiment 2 Patient 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Dual task (normal value 91.99 6 11.10) Idioms String-to-picture Oral explanation 0.69 (±0.49) 0.88 (0.59) 0.74 (±0.207) 0.39 (±2.248) 0.79 (0.08) 0.73 (±0.2651) 0.90 (0.7145) 0.82 (0.2536) 0.73 (±0.2651) 0.80 (0.1386) 0.96 (1.0605) 0.87 (0.5418) 0.91(0.7723) 0.43 (±1.9942) 1 (1.2911) 6/40 22/40 24/40 9/40 11/40 10/40 16/40 14/40 27/40 13/40 37/40 27/40 22/40 25/40 28/40 21/40 25/40 25/40 26/40 14/40 32/40 29/40 33/40 33/40 19/40 26/40 28/40 33/40 25/40 31/40 (±1.5) (0.29) (0.52) (±1.2) (±1) (±1.1) (±0.4) (±0.6) (0.86) (±0.7) (1.99) (0.86) (0.29) (0.63) (0.97) (±1) (±0.3) (±0.3) (±0.1) (±2.3) (0.96) (0.42) (1.14) (1.14) (±1.4) (±0.1) (0.24) (1.14) (±0.3) (0.78) Values in parentheses are Z scores were comparable to the patients of the previous group in severity of disease [t(14)= ±1.353, P = 0.19], mean age [t(14)= ±1.225, P = 0.24] and education [t(14) = 0.406, P = 0.69]. The same criteria of inclusion were followed. Demographic and clinical data of the patients are reported in Table 3. All patients gave informed consent to participation in the study. Procedure In this experiment patients were subjected to the dual task, to the idiom comprehension test in the sentence-to-picture matching modality, and to a test of oral explanation of idioms. In this last task, the same idioms were presented verbally to the patient, who was asked to explain their meanings (after being instructed that he/she was expected to give a ®gurative interpretation of the sentence). The oral explanation was accepted when at least two out of three independent judges considered it adequate. The order of tasks was counterbalanced across subjects. We assumed that when Alzheimer's disease patients have simply to explain the meaning of an idiom, they attain a better performance than when they have to operate a choice between two alternatives, where the concrete representation interferes with the retrieval of the abstract interpretation. In other words, the lexical knowledge of idioms is preserved, but patients are not able to reject the literal meaning when this is offered to them. Results The results for the 15 patients in the three tests are shown in Table 4. Their performance was signi®cantly worse than that of 15 healthy participants, matched for age and educational level, both in the sentence-to-picture matching task [t(14) = ±5.377, P < 0.0001] and in the oral task [t(14) = ±6.994, P < 0.0001]. However, the performance of the Alzheimer's disease patients was signi®cantly better in the oral explanation task (mean number of correct responses 26.27, SD 5.57) compared with their performance in the sentence-to-picture matching task (mean number of correct responses 19.4, SD 8.84) [t(14) = ±3.17, P < 0. 01]. Whereas for 35.5% of the total answers the patients gave a correct response in both tasks, 31.2% of answers were correct in the oral task and wrong in the sentence-to-picture matching task. Responses were wrong in both tasks in 20.5%, and only 12.8% of responses were correct in the sentence-to-picture and wrong in the oral task. As in the previous experiment, the performance on idiom comprehension in the sentence-to-picture matching task correlated with that on the dual task (rS = 0.54, P < 0.05), while there was no correlation between the former and the degree of cognitive decline (rS = ±0.29, P = 0.28). Also, performance in the oral task did not correlate with cognitive decline (rS = 0.22, P = 0.41) or dual-task performance (rS = 0.27, P = 0.30). The number of correct responses correlated signi®cantly with literal picture plausibility in the sentence-to-picture matching task (rS = ±0.35, P = 0.02). The number of correct responses in the oral task correlated signi®cantly with familiarity (rS = 0. 42, P < 0.01). We also checked sentence plausibility, because some oral responses corresponded to the literal interpretation (25%). Ten normal controls were asked to rate how well an idiomatic string would also evoke a literal interpretation. For example: the sentence `to go to the cool' means in Italian `to be put in jail', but one could accept the possibility that someone is moving towards a cool place, while the sentence `to squeeze his/her own meninges' does not allow any literal explanation. Controls had to give a rating of 0 (no acceptable literal meaning), 1 (mild literal meaning) or 2 (absolutely acceptable literal meaning). A correlation analysis showed that Alzheimer's disease patients produced the literal interpret- 2426 Costanza Papagno et al. ation whenever the sentence offered this possibility: this means that, whenever plausible, the literal meaning overpasses the ®gurative one (rS = 0.63, P < 0.0001). The remaining errors in the oral task were mainly partial or wrong interpretation (57%), no response (17%) and opposite meaning (1%). Discussion The performance of Alzheimer's disease patients was signi®cantly better in the oral task than in the sentence-topicture matching task. In this last task performance correlated with the plausibility of the pictures, whereas in the oral task performance correlated with familiarity. A correlation was also found between the literal errors produced in the oral task and the degree of plausibility of the sentence, suggesting that, at least out of context, the literal interpretation precedes the ®gurative one for patients with Alzheimer's disease, inhibiting further analysis whenever the result of sentence processing is plausible. General discussion Two experiments were conducted with Alzheimer's disease patients. In Experiment 1, an analysis of the relationship between idiomatic and literal language was performed. Idiomatic comprehension was tested in two conditions, both using a sentence-to-picture matching task paradigm: a picture representing the idiomatic meaning was contrasted, in one condition, with a picture representing the literal meaning, whereas in the other condition it was contrasted with a picture representing an unrelated situation, including a word contained in the idiom. There was no correlation between idiomatic and literal language comprehension, as already found in a previous study (Papagno, 2001). However, participants had better idiomatic comprehension than is re¯ected in the ®rst condition (idiomatic versus literal interpretation): indeed, their performance signi®cantly improved with the unrelated alternative. In Experiment 2, idiom comprehension was assessed in two modalities: patients performed a sentence-to-picture matching task (two alternatives: correct ®gurative meaning versus literal representation) and an oral task in which they produced a verbal explanation of the idioms. This latter task was signi®cantly better performed than the former, but patients still produced a literal interpretation whenever the literal meaning of the sentence was plausible. In both experiments, performance on idiomatic expressions correlated with performance on the dual task. The conclusions of this study are straightforward. First, our data con®rm those of a previous study (Papagno, 2001), in which ®gurative language comprehension was dissociated from literal language comprehension, but also suggest that the modality of testing is very important, as already outlined by Tompkins and colleagues (Tompkins et al., 1992). In Papagno's (2001) paper, idioms were both ambiguous and non-ambiguous and varied in transparency, leading to more literal interpretations in the oral modality. In the present study, idioms were chosen in order to be non-ambiguous, and the literal interpretation in the oral task is therefore restricted to the few plausible ones. Kempler and colleagues used ten stimuli, which they called `familiar phrases', generically referring to overlearned expressions, including proverbs, idioms and social interaction formulae, some of the items being full sentences and others being phrases (Kempler et al., 1988). We have already discussed the fact that even restricted categories of idioms can be divided into subgroups with different features, and therefore it is dangerous to consider them together. There is another point to discuss: Kempler and colleagues stated that the oral type of testing often presents problems because responses can be judged to be poor, as Alzheimer's disease patients may choose the wrong word or may not respond to the question asked, or the response may be uninterpretable (Kempler et al., 1988). For this reason these authors required a picture pointing response, suggesting that de®cient performance can be interpreted more clearly with this type of response. Our patients, however, had only mild cognitive impairment and, more importantly, they had no remarkable language de®cits. Moreover, we accepted all responses, that showed that the core abstract meaning of the idiom was preserved. On the other hand, we have found that a sentence-to-picture matching task can produce other problems. Another point deserves further discussion. In the previous study by Papagno (2001), out of 39 Alzheimer's disease patients, only two were found with an impairment of metaphor and idiom comprehension and preserved literal comprehension, while six showed the opposite pattern. This could be due to the fact that poor literal comprehension is not suf®cient or necessary to reduce ®gurative interpretation. Idiomatic language can be impaired not only because of lexical±semantic and syntactic de®cits, as observed in aphasic patients (Papagno and Tabossi, 2002), but can be produced by different mechanisms. One possibility is inadequate suppression, as seen in the Stroop task. Brega and Healy (1999) showed that sentence processing can be obligatory when the component words are highly relevant to the task. In their experiment, participants showed longer reaction times and more errors in naming the colours in which words were printed when the words were included in a sentence and were colour words or colour-related words. By analogy, one can assume that idioms are processed syntactically and semantically and that this produces the interfering effect. Gernsbacher and Robertson (1999) had already described the crucial role that suppression plays in many aspects of language comprehension. They de®ne suppression as a general, cognitive mechanism, the purpose of which is to attenuate the interference caused by the activation of extraneous, unnecessary or inappropriate information. Sometimes this super¯uous activation arises from the external environment, as when we conduct a conversation in a noisy place. At other times this super¯uous information is activated internally, as when we have to deal with the Idiom comprehension in Alzheimer's competing meanings of a word or phrase. In the case of idiomatic expressions, the literal and ®gurative interpretations can be activated in parallel, so that a mechanism for attenuating the activation of the inappropriate interpretation is needed. However, it has been proposed that there are some asymmetries in what gets activated and what gets suppressed. Giora and Fein (1999) suggested that hearing familiar idioms should lead to both idiomatic and literal interpretations becoming activated, because both interpretations are salient out of context. In contrast, less familiar idioms are more likely to activate a literal interpretation, out of context. According to their view, the literal interpretation of an idiom is functional for idiom interpretation. Therefore they predict that, with familiar idioms, deriving the literal interpretation does indeed involve suppressing the idiomatic interpretation; however, they propose that deriving the idiomatic interpretation requires the literal interpretation to be retained. Our data do not support this hypothesis, given that familiar idioms need suppression of the literal interpretation in order to derive the idiomatic meaning. It seems as if familiar idioms, out of context, are also more likely to activate the literal meaning, so that suppression is necessary. We suggest that suppression is mediated by the central executive. In the case of an absolutely implausible expression or an expression that contains a syntactic violation (Papagno and Tabossi, 2002), the literal meaning is less salient and can be easily rejected even when the central executive is damaged, but when the literal interpretation is acceptable or is overtly suggested, suppression is necessary. As the central executive is damaged in Alzheimer's disease patients, as already observed in previous studies (Baddeley et al., 1991, 1997), inhibition of the literal meaning does not take place ef®ciently and the ®gurative meaning does not get suf®cient activation. 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The comprehension of metaphor in braindamaged patients. Brain 1977; 100: 717±29. Received January 30, 2003. Revised March 26, 2003. Second revision May 22, 2003. Accepted May 26, 2003 Idiom comprehension in Alzheimer's Appendix Where possible the equivalent English idiom is given, otherwise an explanation of the ®gurative meaning is given. Table 5 List of idioms 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 avere il pollice verde andare al fresco avere la puzza sotto il naso dare del ®lo da torcere essere in forma andare in bestia fare ®asco essere al settimo cielo mandare a monte essere di facili costumi prendere ®schi per ®aschi montarsi la testa dare i numeri farsene un baffo avere i minuti contati stare alle costole avere il cuore in mano vendere cara la pelle venire alle mani mordere il freno parlare al muro essere sul viale del tramonto spremersi le meningi essere di manica larga far cadere le braccia non vedere l'ora perdere la faccia stare in campana avere poco sale in zucca tendere le orecchie essere uno stinco di santo avere le mani in pasta prendere in castagna lasciarci le penne far venire il latte alle ginocchia essere a piede libero tenere banco essere sulla cattiva strada restare con un palmo di naso mettersi le gambe in spalla NS NS SV SV NS SV SV NS I NS SV NS NS NS I SV NS NS NS NS SV I NS I SV SV NS NS SV SV NS NS SV SV NS NS NS IF (0±3) PP (0±7) SP (0±2) 2.4 2.3 2.5 2.6 2.7 2.5 2.3 2.5 2.3 2.3 2.3 2.7 2.6 2.4 2.5 2.3 2.1 1.9 2.4 1.4 2.7 1.9 2.4 2.2 2.3 2.8 2.4 2.1 2.3 2.2 2.3 1.8 2 2.1 1.9 2.1 1.9 2.4 2 1.5 4.3 2.3 4.8 3.3 1.3 2.2 1.9 2.8 3.2 1.0 1.7 2.8 3.9 1.8 1.4 2.2 5.5 3.1 0.8 3.3 4.4 3.7 1.9 2.9 3.0 3.7 3.4 2.3 2.0 3.3 1.1 2.4 2.4 2.2 1.9 2.6 2.4 2.0 1.6 3.4 0.2 1.4 0.4 0.1 0 0 0 0.1 0.3 0 0 0.1 1.1 0 0.3 0 0.3 0.7 0.1 0.2 0.6 0.7 0 0.1 0.4 1 0 0 0 0.6 0 0.5 0 0.2 0 0 0.4 0.7 0 0.1 IF = idiom familiarity; PP = literal picture plausibility; SP = literal meaning plausibility; SV = syntactic violation; NS = lack of sense; I = real-world implausibility of the sentence. The ®rst three idioms could have a plausible literal interpretation and were excluded from further studies. 2429 2430 Costanza Papagno et al. Table 6 Idiom translation Idiom Literal meaning Figurative meaning 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 To be good at gardening To go in the cool to have a bad smell under the nose to give some thread to twist to be in shape to go in beast to make ¯ask to be at the seventh sky to send to mountain to be of easy customs to take whistles for ¯asks to mount the head to give the numbers to make a moustache of it to have the minutes counted to stay at the ribs to have the heart in hand to sell the skin at a high price to come to the hands to bite the brake to talk to the wall to be on the sunset boulevard to squeeze one's meninges to be of large sleeve to make the arms fall to not see the hour to lose the face to stay in bell to have few salt in pumpkin to stretch the ears to be the shin-bone of a saint to have the hands in dough to take in chestnut to leave the feathers to make the milk come to the knees to be at free foot to hold bench to be on the bad path to remain with a span of nose to put the legs on shoulder to have a green thumb to go to jail to be snooty to make things hard for someone to be very well to become very angry to fail badly to be in the seventh heaven to make something fail to be of easy virtue to misunderstand to become swollen-headed to talk nonsense not to give a damn to have very little time to dog someone's heels to be very generous to ®ght hard to come to blows to champ at the bit to talk to a brick wall to be on the wane to rack one's brains to be indulgent to have one's heart sink to one's boots to look forward to lose face to be very careful to have nonsense in one's head to prick up one's ears to be an angel to have one's ®nger in the pie to catch someone out to lose life to be particularly boring to be on bail to be the person who talks a lot in a group of people paying attention to one to make bad things to be badly disappointed to ¯ee
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