A possible contributory mechanism for impaired idiom perception in schizophrenia

Author’s Accepted Manuscript A possible contributory mechanism for impaired idiom perception in schizophrenia Tal Sela, Michal Lavidor, Rachel L.C. Mitchell

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S0165-1781(15)00478-3 http://dx.doi.org/10.1016/j.psychres.2015.07.021 PSY9073

To appear in: Psychiatry Research Received date: 26 June 2014 Revised date: 11 June 2015 Accepted date: 11 July 2015 Cite this article as: Tal Sela, Michal Lavidor and Rachel L.C. Mitchell, A possible contributory mechanism for impaired idiom perception in schizophrenia, Psychiatry Research, http://dx.doi.org/10.1016/j.psychres.2015.07.021 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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A possible contributory mechanism for impaired idiom perception in schizophrenia. Tal Selaa, Michal Lavidora and Rachel L. C. Mitchellb a

Department of Psychology, Bar Ilan University, Israel.

b

Centre for Affective Disorders, Institute of Psychiatry, KCL, London. UK. * Corresponding Author: Dr. Rachel Mitchell, Centre for Affective Disorders (PO Box 72), Department of

Psychological Medicine, Institute of Psychiatry, King’s College London, 16 De Crespigny Park, Denmark Hill. LONDON. SE5 8AF. Email: [email protected]. Tel: +44 (0)20 7848 0805. Fax: +44 (0)20 7848 0298 Abstract In this review, we focus on the ability of people with schizophrenia to correctly perceive the meaning of idioms; figurative language expressions in which intended meaning is not derived from the meaning of constituent words. We collate evidence on how idiom perception is impaired, ascertain the clinical relevance of this impairment, and consider possible psychological and neural mechanisms behind the impairment. In reviewing extant literature, we searched the PubMed database, from 1975-2014, focussing on articles that directly concerned schizophrenia and idioms, with follow up searches to explore the viability of possible underlying mechanisms. We learn that there is clear evidence of impairment, with a tendency to err towards literal interpretations unless the figurative meaning is salient, and despite contextual cues to figurative interpretations. Given the importance of idioms in everyday language, the potential impact is significant. Clinically, impaired idiom perception primarily relates to positive symptoms of schizophrenia, but also to negative symptoms. The origins of the impairment remain speculation, with impaired executive function, impaired semantic functions, and impaired context processing all proposed to explain the phenomenon.

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We conclude that a possible contributory mechanism at the neural level is an impaired dorsolateral prefrontal cortex system for cognitive control over semantic processing.

Keywords: idioms, schizophrenia, figurative language, cognitive control

Word Count: 7,153 1. Introduction Schizophrenia is an insidious and pervasive spectrum of disorders that is one of the top ten medical disorders causing disability in the world today (World Health Organisation, 1990). It affects one in a hundred people worldwide (Jablensky et al., 1992), and in the UK, its estimated total cost per annum is 6.7 billion GBP (Mangalore and Knapp, 2007). Although our understanding of the illness has advanced in recent years, schizophrenia continues to challenge those who live and work with it. Impaired cognition is connected to poor functional outcome for patients, and of the cognitive deficits observed, language abnormalities are among the most salient (Boudewyn et al., 2012). In this review, we focus on the difficulties people with schizophrenia have interpreting a particularly large class of figurative linguistic expressions known as idioms (Rapp et al., 2012). Further research on idiomatic language impairment may hold important clues as to the bases of language impairment in schizophrenia, because it has the potential to provide important insights into their thought patterns (Thoma and Daum, 2006; Mashal et al., 2008). Impaired perception of figurative language could also play an important role in the social isolation experienced by people with schizophrenia (Gavilán and García-Albea, 2011).

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With the overall aim of shedding light on the significance of impaired idiom perception in schizophrenia and its possible causes and consequences, we set the scene by introducing figurative language functions and describing the characteristics of idioms. We then review the direct literature on impaired idiom perception in schizophrenia and go on to consider the clinical relevance of this impairment and current suggestions for the underlying mechanisms of this impairment. We finish by describing how faulty dorsolateral prefrontal cortex cognitive control could be responsible for the deficit, with the suggestion that it might be worth probing in future research.

2. Figurative Language Functions Literal language refers to phrases that can be taken at face value to mean exactly what they say, but the meaning of figurative language cannot be derived by analysing its constituent words and their semantic and syntactic properties. Such phrases are commonly used to add colour and interest, or to awaken the imagination, and often incorporates exaggerations or alterations to make a particular point (Proverbio et al., 2009). Figurative phrases also allow speakers to express abstract concepts in a concise manner (Zempleni et al., 2007). To comprehend a figurative phrase as intended, in-depth interpretation is required (Regel et al., 2010). This process can be challenging, since it involves recognising literal meaning, understanding a speaker's intentions, and integrating word meaning with context (Kana et al., 2012). However, the ability to use figurative communication effectively may promote personal and professional success (Thoma and Daum, 2006), and the ability to engage in socially meaningful exchanges and resolve interpersonal conflicts (Im-Bolter et al., 2013).

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Classically, idioms are defined as phrases for which the intended meaning is not derived from the meaning of its individual constituent words, for example, ‘life’s too short’. The composition of life, is, too, and short does not produce “you should not waste time doing or worrying about things that are not important. The psycholinguistic characteristics of idioms form a heterogeneous class and include several features such as predictability, compositionality and ambiguity – see Box 1 (Nunberg et al., 1994; Titone and Connine, 1994b, 1999). By exploring these specific characteristics, it is possible to learn about the way in which the relations between an idiom's words and meanings are mapped. Different theoretical accounts have sought to explain the nature of the mapping process between an idiom’s words and construction of its figurative meaning – see Box 1. For example, idioms have been described as configurations of words in which a key part needs to be processed to prompt recognition of the idiomatic nature of the string (Cacciari and Tabossi, 1988). There are some suggestions that unitary representations of familiar idioms may be directly retrieved (Swinney and Cutler, 1979a), however, other phrases like ‘kick the bucket’ are ambiguous as to whether they carry literal or idiomatic meaning in certain contexts, and may need to be analysed compositionally to understand their meaning (Libben and Titone, 2008a). Thus individual idioms vary widely in difficulty, with more familiar and transparent expressions being easier to understand than those less familiar and more opaque (Nippold, 1998). Idiomatic phrases often occur in spoken and written communications such as the jokes, riddles and anecdotes people exchange during social situations though (Tabossi et al., 2009), and it has been suggested that people in fact have a strong propensity to “speak idiomatically unless there is a good reason not to do so” (Searle, 1975). Given their frequency, it is important that people comprehend them effectively, and understanding how

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people deal with idiomatic expressions should be a crucial part of any theory of language processing.

3. How is the Perception of Idioms Impaired in Schizophrenia? Of the family of language functions comprising figurative language, the performance of patients with schizophrenia on tasks using these as stimuli falls below that of healthy adults for numerous categories, including for the perception of metaphors, proverbs, and irony (Mitchell and Crow, 2005; Mo et al., 2008; Elvevag et al., 2011; Rapp et al., 2014). Yet despite their importance, there remains curiously little direct research on how idiom perception is impaired in schizophrenia. This paradox becomes even more surprising when one considers the wide-ranging back-drop of linguistic impairment in schizophrenia, including impairments of both the semantic processing that is needed to understand the meaning of idioms (Caillies and Declercq, 2011; Rommers et al., 2013), along with the appreciation of pragmatic language useage to understand that their use is not for literal purposes (Rinaldi, 2000; Regel et al., 2010; Le Sourn-Bissaoui et al., 2012). Further, in the case of schizophrenia, there exists a clear relationship between these linguistic impairments and cardinal symptoms of psychosis such as thought disorder (Kumar and Debruille, 2004; Covington et al., 2005). As a consequence, in patients with diagnoses of schizophrenia, interpersonal functioning can be severely compromised by these communicative impairments (Mitchell and Crow, 2005). The known neuroanatomical correlates of schizophrenia also seem to fit well with the potential for impairments of figurative language perception, through disrupted activity of cortico-subcortical circuitry during the processing of verbal material (Li et al., 2009; Han and Wible, 2010), reduced cerebral asymmetry (Oertel-Knochel et al., 2012) and impaired interhemispheric communication transfer due to callosal abnormities

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(Strelnikov, 2010). As to whether impaired understanding of figurative language impairments in schizophrenia could ever be used for diagnostic purposes, very little research has addressed the important question of whether impaired comprehension is specific for schizophrenia or a more general feature of psychiatric disorders (Thoma and Daum, 2006). Indeed, impaired perception of idioms presents in a number of psychiatric and neurological disorders, including autism (Whyte et al., 2013; Whyte et al., 2014), Alzheimer’s disease (Rassiga et al., 2009; Rapp and Wild, 2011), mild cognitive impairment (Cardoso et al., 2014), and Parkinson’s disease (Papagno et al., 2013). However, as seen in the study of Iakimova et al. below, there is evidence of differences in the pattern of impairments of idiom perception shown in schizophrenia and depression (Iakimova et al., 2006). For this review, relevant original studies of idiom perception in schizophrenia were identified through a PubMed search, using the terms (schizophrenia OR schizophrenic OR psychosis OR psychoses OR psychotic) AND (idiom OR idioms OR idiomatic), and are summarised for the reader in Table 1. At the outset, the difficulty is unlikely to be caused by a problem acquiring knowledge of idiom meaning, since much of that knowledge is acquired prior to the late adolescence risk period for the neurodevelopmental brain mechanisms associated with schizophrenia (Nippold and Taylor, 2002; Powell, 2010). As part of a wider investigation of receptive and expressive language functions, Tavano et al. (2008) assessed idiom perception by presenting 20 idioms and simply asking people with schizophrenia to explain their meaning. Two points were awarded if the full meaning was explained, one point if the answer was only partially correct, and zero points if the answer was literal, deviant or if no answer was given. As expected, people with schizophrenia showed significant deficits when attempting to explain the meaning of the idioms, and since their score negatively correlated with syntactic comprehension, it was suggested that when patients made less

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syntactic errors, they also tended to provide more appropriate explanations of the idioms (Tavano et al., 2008). An alternative methodology has been to use Multiple Choice Questionnaire format tests like that used by Iakimova et al. in their 2006 article, who argued that such tests prevent intrusive factors inherent to verbalisation which are not necessarily related to figurative interpretation (e.g. difficulty expressing ideas). In this study, they sought to test the existence of a literality and concreteness bias that might influence access to the meaning of ambiguous idioms in people with schizophrenia. Both people with depression and people with schizophrenia sometimes chose concrete responses. However, the people with schizophrenia chose literal idiom interpretations more often than both healthy controls and people with depression. This pattern occurred despite incorporating additional response options to counter over-estimation of the literality bias when only literal and figurative response options are specified, and despite the figurative bias for idioms induced by only including figurative expressions (Iakimova et al., 2006). Semantic decision type tasks have also been used e.g. in the 2010 study by Iakimova et al. In this task, participants judge whether a target word is semantically related to the preceding idiom (Iakimova et al., 2010). In this later study, Iakimova et al. probed whether the perception of idioms with two meanings (literal and figurative) is guided by the salience (familiarity, conventionality, and frequency of use), or by the literality/figurativeness of idioms. The authors predicted that difficulty in figurative comprehension in people with schizophrenia would be marked when figurative meaning was not salient, but preserved when salient. Whilst the performance of people with schizophrenia was universally less accurate and slower than that of the healthy controls, there were also interesting interactions between participant group and the relatedness, salience and figurativeness of the target word. In accordance with Giora’s graded salience theory (Giora, 1997), the salience effect was observed for patients just as it was for the healthy controls.

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However, patients with schizophrenia did not show the figurative bias of healthy controls in which for idioms of equal figurative and literal salience, they access the figurative meaning more accurately than the literal meaning (Iakimova et al., 2010). These two studies focussed exclusively on perceiving ambiguous idioms. Ambiguous idioms have a well-formed literal counterpart, whereas unambiguous idioms do not. In the study by Schettino et al., the authors reasoned that idiom perception by people with schizophrenia should be impaired, particularly for ambiguous idioms which require inhibition of a plausible literal meaning (Schettino et al., 2010). Idiom perception was tested with a sentence-to-picture matching task in which participants are presented with a written sentence (idiomatic or literal), followed by a picture, and have to decide whether the picture represents the meaning of the sentence or not. Whilst performance by the people with schizophrenia was impaired for both ambiguous and unambiguous idioms, their performance was particularly poor for the ambiguous idioms (Schettino et al., 2010). For many language functions, contextual clues can be of great benefit in understanding the correct meaning of expressions (Pulvermuller et al., 2009; Van Petten and Luka, 2012). Elsewhere, other methodology has therefore focussed on unambiguous idioms without a literal counterpart, the reasoning being that the presence of an idiom with a plausible literal meaning in a sentence might lead patients to expect the potential literal meaning whether or not that was in fact the appropriate meaning to derive. In one study this prompted the use of a sentence verification task in which participants were asked to decide whether a target word is a sensible continuation of a previous sentence fragment (Pesciarelli et al., 2014). In particular, this study aimed to determine the relevant impact of an overreliance on the semantic memory-based language processing at the expense of combinatorial analysis that establishes meaning compositionally. This was achieved by

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manipulating the predictability of final words in a sentence, to design literal and idiomatic sentences whose final words were expected to a comparably high degree. Whilst healthy controls and the patients with schizophrenia were expected to be equally facilitated in anticipating what came next in literal and idiomatic sentences, patients were expected to be more facilitated by idiomatic than literal predictability, because of the bound prefabricated structure of idioms. They theorised that since idiomatic meanings should be directly retrieved from semantic memory, patients’ over-reliance on a semantic memory-based stream of analysis may actually turn into a processing resource rather than a limitation. Their results revealed that patients’ reaction times to idiomatic sentences were slower than those of the healthy controls, but this difference was not statistically significant. The authors interpretation stressed that this pattern of results could not be taken to imply that patients comprehended idioms as per normal. Rather they felt that the results showed that for their clinically stable patients, the state of residual schizophrenia did not contribute to slower processing of sensible idioms above and beyond the cognitive deficits that also characterised their patients (Pesciarelli et al., 2014). One way to study the value of contextual clues rather than exclude them is to use the N400 component of event-related potentials. Normally, a large N400 is elicited when the terminal word in a sentence is incongruous with the expected meaning of an expression (Debruille, 2007). This N400 was the measure used by Strandburg et al. in their study of idiom perception in schizophrenia (Strandburg et al., 1997). Specifically, they focused on N400 activity in response to idiomatic word pairs that had a stronger contextual link due to familiarity and frequent use. Thus they presented literal and idiomatic meaningful two-word phrases and nonsensical phrases to participants and asked them to indicate whether each phrase was meaningful or not. Importantly, the idioms selected had no literal interpretation (e.g. ‘fat chance’). Behaviourally, the people with schizophrenia showed lower performance

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accuracy and longer reaction times. The ERP correlate of these behavioural data was a larger than normal N400 to both idiomatic and literal phrases, whereas healthy controls showed a smaller N400 response to idiomatic phrases than to the literal ones. Thus the authors concluded that the influence of the linguistic context provided by the first word of two-word idiomatic and literal phrases is reduced in schizophrenia (Strandburg et al., 1997). In their study of impaired idiom perception in schizophrenia, Titone et al. aimed to distinguish how the use of contextual clues breaks down in people with this diagnosis (Titone et al., 2002). They reasoned that people with schizophrenia fail to take advantage of these clues because they cannot decode or encode contextual clues, or because they are not able to inhibit activation of the contextually irrelevant dominant meaning. Thus they presented participants with prime stimuli consisting of literally plausible or implausible idioms within neutral sentences (e.g. ‘the man kicked the bucket’), and asked them to make lexical decisions about idiom-related or literally-related target words (word/non-word). The people with schizophrenia showed reduced priming for literally plausible idioms, but intact priming for literally implausible idioms relative to healthy controls. Both patients and controls showed evidence of literal word priming. From these results, Titone et al. rejected the view that people with schizophrenia have a global deficit using contextual clues, and instead favoured the view that the problem reflected a difficulty inhibiting the literal interpretations of idioms when available. In the next section of this review we focus more on the mechanistic explanations for impaired idiom perception in people with schizophrenia, and how these mechanisms are grounded in the symptoms of schizophrenia.

4. Symptomatological Correlates and Suggested Underlying Mechanisms Of the studies of impaired idiom perception mentioned above, neither Strandburg et al., Tavano et al., nor Titone et al. examined the relationship with symptoms of

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schizophrenia. Iakimova et al. noticed in their original study that some patients with schizophrenia never chose a concrete response. Intrigued by this result, they decided to compare the clinical characteristics of patients who never chose a concrete response, with those patients who had chosen one. This incidental analysis showed that the patients who never chose a concrete response had weaker positive symptoms than those who had sometimes chosen a concrete response. Although they commented that this speculative finding demonstrated cognitive and clinical heterogeneity as has been demonstrated for other figurative language functions, the authors did not expand further (Iakimova et al., 2006). Nevertheless, this finding hints that the incorrect selection of concrete responses may somehow be associated with overall positive symptomatology. In their later study, they uncovered a more complex pattern of results (Iakimova et al., 2010). When figurative meaning was salient, performance negatively correlated with thought disorder and abstraction. When not salient, performance was again negatively correlated with abstraction. Finally, when figurative and literal meanings were equally salient, performance correlated with thought disorder. The interpretation put forward by the authors was that people with schizophrenia who have prominent thought disorder might show impaired perception of salient figurative meaning because of an impairment in their semantic memory system (Iakimova et al., 2010), although the details of this interpretation were not worked out in detail. This interpretation was based on the premise of Giora that perception of salient figurative meaning is accessed directly from the lexicon without the need for controlled processing (Giora, 1997, 2003). The relationship with difficulty in abstract thinking is perhaps a little more obvious given that figurative language is particularly sensitive to abstract thinking in patients who suffer from impaired abstraction and language abilities (Yang et al., 2010). In one of the other studies of idiom perception in schizophrenia, the effects of severity of thought disorder were of limited nature and mostly existed only at trend

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level (Pesciarelli et al., 2014). However, the trends suggested that as conceptual disorganisation and difficulty in abstract thinking increased, patients’ reaction times slowed down, thereby reflecting the semantic processing impairment. Relationships between idiom perception and negative symptoms of schizophrenia were the key result in Schettino et al’s study (Schettino et al., 2010). In particular, they noted a correlation between general idiom perception and conceptual disorganisation, and between the perception of ambiguous idioms and negative symptoms as a whole. In trying to explain these results, they cited the link between executive functions and negative symptoms (Orellana and Slachevsky, 2013), and suggested that negative symptoms can be considered ‘cognitive behaviours’ expressing deficits of executive control (Frith, 1992). In the Pesciarelli et al. study, longer reaction times in their task also correlated positively with severity of negative symptoms, which they too interpreted as reflecting a deficit in executive function (Pesciarelli et al., 2014). This explanation now leads us to our discussion of the cognitive mechanisms suggested to underlie impaired idiom perception in schizophrenia. From the extant literature on idiom perception in schizophrenia, three main explanations emerge, namely impaired executive function, impaired semantic functions, and impaired context processing. Note that these explanations are not mutually exclusive, and sometimes they are combined. Tavano et al proposed a global deficiency in pragmatic inferencing skills from the profile of impairment of their patients across figurative language tasks, but this is perhaps more of a descriptive statement than an explanation (Tavano et al., 2008). The studies by Iakimova et al, Schettino et al, and Titone et al all suggest that impaired executive functions may at least partially be responsible for impaired idiom perception in people with schizophrenia (Titone et al., 2002; Iakimova et al., 2010; Schettino et al., 2010), just as it has for their metaphor and proverb comprehension (Langdon et al., 2002; Brune and Bodenstein,

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2005; Mo et al., 2008). Whilst Iakimova et al did not examine the relationship with executive functions per se, they observed a relationship between impaired perception of idioms when the figurative meaning was not salient, and verbal IQ. In speculating on the reason for this relationship, the authors invoked Giora et al’s graded salience hypothesis (Giora, 2003), citing the tenet that when figurative meanings are not salient, their comprehension requires higher-level cognitions such as the suppression of salient literal meanings. Since it is wellknown that executive functions are also impaired in schizophrenia (Fioravanti et al., 2012), the authors reasoned that the perception of idioms with non-salient figurative meaning may be particularly difficult for them. Titone et al. also alluded to impaired inhibition of literal meaning being a possible cause of impaired idiom perception in people with schizophrenia (Titone et al., 2002). Schettino et al. took a more direct approach, and administered three executive function tasks alongside their idiom perception task, namely the Wisconsin Card Sorting Task (WCST), the Tower of London Task, and the Digit Sequencing Task, to tap into set shifting, planning, and working memory respectively (Schettino et al., 2010). The authors make a similar point to that raised by Iakimova et al. above, that unless an idiom is almost always used in the figurative sense, people with schizophrenia find it difficult to inhibit its literal meaning. The results demonstrated that performance on the WCST and Digit Sequencing Tasks by people with schizophrenia was predictive of their performance on the idiom perception task (Schettino et al., 2010). That the former relationship was significant for perceiving ambiguous idioms and the latter for unambiguous idioms suggests that future studies may need to be more specific, since the results seems to indicate that different executive functions are necessary for the perception of different types of idiom, a finding supported by studies of idiom perception in other patient groups (Papagno et al., 2003;

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Rassiga et al., 2009). Pesciarelli et al. were able to demonstrate that once the contribution of cognitive impairment (ascertained with an IQ test, a syntactic comprehension test, and phonemic and semantic fluency tests) was statistically accounted for, patients’ response times to sensible idiomatic continuations of sentence fragments did not in fact differ from those of healthy controls (Pesciarelli et al., 2014). Thus they concluded that these cognitive variables did indeed play a role in shaping the idiom perception performance of patients. Impaired semantic processing provides a second account of how idiom perception is impaired in people with schizophrenia. Mention of impaired semantic processing was made in Iakimova et al’s 2005 paper (Iakimova et al., 2006), where it was used to explain the observation that patients were less influenced by the global contextual characteristics of the idiom task that normally led to rejection of the literal meaning and selection of the figurative meaning (see next paragraph on context). Thus they speculated that abnormal semantic processing generally led to a failure to reject literal meaning in people with schizophrenia. In their later study, however, they more specifically proposed that an impaired semantic memory system underlies idiom perception when the figurative meaning is salient and cannot be accessed directly from the lexicon without the need for non-linguistic processing (Iakimova et al., 2010). Elsewhere, it was speculated that idiom perception might be relatively spared in patients when idioms are familiar and literally implausible, and predictable, because of patients’ over-reliance on the semantic memory-based stream of analysis due to the fact that idioms are retrieved directly from semantic memory (Pesciarelli et al., 2014). Of the three explanations used to account for impaired idiom perception in schizophrenia, impaired semantic processing is perhaps the least well worked out, and as noted in this section, many other interactive factors could be involved.

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The final explanation given in studies of impaired idiom perception in schizophrenia is the idea that it represents a breakdown of the processing of, or integration of, contextual information that assists in disambiguating idiom meaning. This has been the most prevalent explanation so far (Strandburg et al., 1997; Titone et al., 2002; Iakimova et al., 2006; Iakimova et al., 2010), and it has similarly been used to explain impaired comprehension of other figurative language functions such as metaphors (Iakimova et al., 2005) and proverbs (Gavilán and García-Albea, 2011). Cohen and Servan-Schreiber (1992) were the first to argue forcibly for deficient context processing in schizophrenia, by proposing that a core deficit underlying impaired linguistic and cognitive functions in schizophrenia is "the inability to construct and maintain an internal representation of context for the control of action" (p 52) (Cohen and Servanschreiber, 1992). This definition suggests that there may be some overlap between the context integration and executive dysfunction explanations. Since then, it has remained a prevalent feature of mechanisms hypothesised to underlie cognitive dysfunction in schizophrenia (Hemsley, 2005), and as with executive dysfunction, is thought to reflect impaired dorsolateral prefrontal cortex function (Melcher et al., 2008). However, as we shall see in the next paragraph, with respect to idioms, context integration necessitates not just intact executive functioning, but correct interpretation of the contextual cues themselves. At the task level, contextual characteristics of a task can influence the perception of idioms such that when a task contains only idioms or a high percentage of idioms, a bias towards figurative interpretations is induced even when figurative and literal meanings are equally salient. However, people with schizophrenia do not show this figurativeness bias (Iakimova et al., 2006; Iakimova et al., 2010), and in one study that exclusively presented idioms, patients with schizophrenia still interpreted idioms literally 20% of the time (Iakimova et al., 2006). With a lexical-decision or priming task, people with schizophrenia

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show less accurate and slower recognition of target words i.e. less priming, specifically for idioms that are literally plausible. Thus with that particular type of idiom, they are less able to benefit from contextual cues and inhibit activation of the contextually irrelevant dominant meaning (Titone et al., 2002). In the Strandburg et al study, context processing reflected the need to hold in mind the semantic constraints of the first word in a two-word phrase for use in interpreting the second word (Strandburg et al., 1997). Failure to make use of contextual information in idiom perception does not seem to be global across all situations though. There is some suggestion that intact context processing may be particularly important when the figurative meaning of idioms is not salient (Iakimova et al., 2010), or when it has a literally plausible interpretation (Titone et al., 2002). However, given that the impaired context integration explanation of impaired idiom perception in schizophrenia has primarily been driven by findings from other figurative language functions such as metaphors (Iakimova et al., 2005) and proverbs (Gavilán and García-Albea, 2011), further elaboration of the applicability of this explanation to idioms is required. Furthermore, at this point in time, it is difficult to see how the context deficit explanation can be anything more than an interpretive predisposition given that it is arguably difficult to conceive what concrete entity ‘context’ is exactly, or how it can be definitively tested in an experimental context. What one researcher classifies as being ‘context’, may vary greatly to why another researcher identifies their experimental manipulation as ‘context’. ‘Context’ may potentially reflect the experimental settings that can vary within idiom perception paradigms, but that is not the same thing as constituting a mediatory mechanism.

5. A Faulty Dorsolateral Prefrontal Cognitive Control Mechanism?

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As reviewed in the previous section, the problem with the mechanisms put forward to explain impaired idiom perception in schizophrenia so far, is that apart from the investigation of relationship with executive function by Schettino et al. (2010), much of the hypothesising has been speculative. Here, we put forward for testing, a specific candidate neurocognitive mechanism that is currently unexplored, but which may hold great promise for explaining why idiom perception is impaired in schizophrenia. Our intention is to provide a testable conceptual framework with corollary predictions whose utility can be evaluated by future researchers.

5.1. The Role of Cognitive Control in Language Cognitive control is a construct which incorporates higher order processes that enable the formation, maintenance, and updating of behavioural goal representations (Miller and Cohen, 2001), as well as top-down biasing of other mechanisms that enhance or inhibit information processing (Banich et al., 2000; Savine and Braver, 2010). In language the comprehension of a message relies on a complex interplay between previously processed information, information currently being processed, and importantly, predictions arising from the combination of these two sources of information (Roehm et al., 2007). Bulk evidence highlights the presence of predictive forward-looking mechanisms in language (Vespignani et al., 2010), but the form and role of these anticipatory mechanisms when they break down in schizophrenia has not yet been established. Faulty cognitive control mechanisms in schizophrenia may play a significant role in the language processing deficits observed. One particularly important question concerns how cognitive control operations influence semantic processing. Specifically, how might goals bias information retrieval from semantic memory, and contribute to selection processes when there are competing semantic meanings (Sela et

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al., 2012). In schizophrenia, the ability to implement cognitive control is known to be dysfunctional (Luck et al., 2012). It is also highly prevalent and is thought to affect 45-95% of patients (Velligan and Bow-Thomas, 1999), and may adversely influence their social, professional, and personal levels of achievement (Green, 1996; Penn et al., 2002). Many other cognitive deficits in schizophrenia have been accounted for by the idea that people with schizophrenia have a degraded ability to construct and maintain internal representations (Cohen and Servanschreiber, 1992; Lesh et al., 2011). At present, the neurocognitive mechanisms responsible for the impaired ability to implement cognitive control and make predictive inferences from linguistic context, are poorly understood in schizophrenia (Titone et al., 2000). Yet, identifying a specific deficit in implementing cognitive control mechanisms, and understanding its relationship to clinical symptoms, could lead to new potential approaches for treating related social skills (McClure et al., 2008).

5.2. Cognitive Control in Idiom Perception Idiom comprehension is not a universal process, and can depend on the particular type of idiom in question (Titone and Connine, 1994a; Tabossi et al., 2005; Caillies and Declercq, 2011). Thus their processing can sometimes necessitate top-down cognitive control over language, particularly semantic processing, since they entail variation in predictability and semantic relatedness (Caillies and Declercq, 2011; Sela et al., 2012). For example, ‘Steve was the first to let the cat out of the bag at the office’ is a highly predictable idiom, whereas ‘the bankruptcy came out of the blue for the store's owner’ is a less predictable idiom. Here, predictability refers to the degree to which forward looking processing is required when the linguistic fragment contains a multiword expression (i.e., an idiom) whose canonical structure

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and meaning is stored in semantic memory (Vespignani et al., 2010). According to the ‘Configuration Hypothesis’, it is the predictability of an idiom that affects access to its figurative and literal meaning (Cacciari and Tabossi, 1988). Here idioms are represented as configurations of words, not lexical units (Titone and Connine, 1994a). With predictable idioms, only the idiomatic meaning is activated by the time the last word of an idiomatic string is encountered. With unpredictable idioms, only the literal meaning of the last word is available until sometime later when both idiomatic and literal meanings are activated (Caillies and Declercq, 2011). Thus individual components of an idiom are analysed as normal linguistic items i.e. the default mode is literal processing (Holsinger and Kaiser, 2012), until they are faced with sufficient cues to trigger recognition of a string as being idiomatic i.e. until a key part (the ‘idiomatic key’) is processed that prompts recognition of the idiomatic nature of the string and activation of its figurative meaning (Cacciari and Tabossi, 1988; Titone and Connine, 1994a; Lauro et al., 2008; Holsinger and Kaiser, 2012; Sela et al., 2012). Currently, there is no universally accepted explanation of impaired idiom perception in schizophrenia (Iakimova et al., 2005). Therefore the speculations and testable model that follow first necessitate acceptance of the underlying theoretical basis, namely the ‘Configuration Hypothesis, and the subsequent fine-coarse semantic coding theory’ (Jung-Beeman, 2005). The Configuration Hypothesis is a well-developed theory that explains how idiom perception is normally mediated, but it is unknown whether it retains any utility for schizophrenia. By examining the effects of predictability on idiom perception, we can examine what happens to the cognitive control network that normally helps evaluate the predictive value of idioms to constrain processing and direct semantic related decision-making processes. A focus on predictability may therefore provide fruitful clues to understanding the neurocognitive processes underlying impaired figurative comprehension in schizophrenia (Iakimova et al., 2010). Potential

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difficulties in figurative comprehension in schizophrenia may be particularly marked when the figurative meaning is not predictable. Although the perception of highly predictable idioms may still show signs of impairment, it may be relatively preserved when compared to perception of idioms with low predictability. Whether this faulty cognitive control mechanism reflects a cognitive deficit in probabilistic evaluation of the predictive properties of the string (Waltz et al., 2011), or a deficit inhibiting the plausible literal meaning of some idioms (Schettino et al., 2010), remains unknown (see Figure 1). In the next section, we consider a possible functional neuroanatomical means by which impaired cognitive control of language processing might be expressed in schizophrenia.

5.3. The Role of Dorsolateral Prefrontal Cortex We wish to promote the possibility that a faulty cognitive control mechanism in the brain may play a significant contribution to the language processing deficits that impact on schizophrenia. In the brain, the locus of the cognitive control mechanism that facilitates language perception for idioms, lies within dorsolateral prefrontal cortex (dlPFC) (Rizzo et al., 2007; Lauro et al., 2008), and converging observations suggest that patients with PFC lesions produce more literal interpretations than patients with non-frontal lesions (Papagno, 2008). Further, in studies performed on patients with Alzheimer’s disease or Down’s syndrome, the bias towards producing literal interpretations correlates with performance on tasks assessing executive functions (Fogliata et al., 2007). Linguistic analysis of a sentence produces two possible interpretations, the literal and the figurative for idioms. A response must be chosen from these alternatives, and the selection and monitoring of internally generated responses are performed by the central executive, in the PFC (Fleming and Dolan, 2012; Nee et al., 2012). PFC dysfunction is frequently reported in schizophrenia, and

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functional neuroimaging data suggest that this represents the engagement of a faulty generalpurpose cognitive control network (Minzenberg et al., 2009). Further, major symptoms of schizophrenia involve profound PFC dysfunction, including cognitive deficits, thought disorder, delusions and hallucinations (Arnsten, 2011). Thus the dlPFC that plays a central role in semantic processing through cognitive control, is key in the neuropathology of schizophrenia (Kircher et al., 2007). Many studies have shown dysfunction of this particular region during language processing in schizophrenia (Mitchell and Crow, 2005). Activation of dlPFC during a neuroimaging idiom perception study relative to healthy young adults would perhaps be the obvious initial test of the localisation of idiom perception impairment in this brain region. As the need for cognitive control is increased, e.g. judging the relatedness of unpredictable idioms and target words in a semantic decision task vs. predictable idioms and target words, using region of interest analyses one might expect a smaller increase in dlPFC activity between the neural response to these two types of idiom in patients with schizophrenia vs. healthy adults. Relative lack of dlPFC activation during idiom perception should also correlate with the extent of executive dysfunction at the behavioural level. If cognitive control plays a significant role in impaired idiom perception in people with schizophrenia, one might predict less dlPFC activation than healthy controls during the figurative bias failure (the failure to access figurative meaning of idioms (Iakimova et al., 2010)) when judging the relatedness of figuratively vs. literally related idioms and target words. If the dlPFC is specifically involved in the semantic processing element of idiom perception, one would expect dlPFC activation to be similar in healthy controls and people with schizophrenia during the ‘reading phase’ of a semantic decision task, but significantly less than that of healthy controls during the actual ‘semantic decision phase’. In contrast, if dlPFC activation were not equal during the reading phase, i.e. if it was lower in people with schizophrenia than in healthy controls, this pattern of results would point to a specific

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problem with predictive evaluation of idiom meaning. However, if reduced dlPFC activity in people with schizophrenia was indiscriminately observed across all conditions regardless of relatedness or predictability, a general non-specific cognitive deficit would have to be concluded instead. A general reduction in middle/superior temporal gyri activation might indicate a non-specific semantic processing deficit, whereas a general reduction in left inferior frontal cortex activation could indicate a non-specific semantic retrieval deficit (Reilly et al., 2011). Across the cerebral hemispheres, left and right dlPFC normally have a differential role in idiom perception, and in this respect, the fact that inter-hemispheric connectivity disturbances play a major role in schizophrenia is particularly significant (Ribolsi et al., 2011; Bleich-Cohen et al., 2012). Jung-Beeman’s ‘fine-coarse semantic coding theory’ proposes that both hemispheres are engaged in semantic activation, integration, and selection (JungBeeman, 2005), but that they differ in the level of granularity at which they encode semantic information (Kasparian, 2013)(see Figure 1). Due to certain differences between them (JungBeeman, 2005), the right hemisphere has a processing advantage for tasks that require more distantly-related, wide- spread, semantic activation (i.e., coarse semantic coding), e.g. for making long-term predictive inferences, understanding figurative language as in idioms (Beeman, 1993). Thus the right hemisphere coarsely codes semantic input, so that a word activates many semantic features, but each only weakly, so that only vague interpretations can be made. In contrast, the left hemisphere has a predisposition for analytic tasks that require activation of more closely related, focused and literal semantic activation (i.e., fine semantic coding)(Jung-Beeman, 2005; Bohrn et al., 2012; Rapp et al., 2012; Sela et al., 2012; Subramaniam et al., 2012). The left hemisphere thus finely codes semantic input, so that a word activates few semantic features, but all so strongly that they are accessible to consciousness and selected for further processing (Beeman, 1993). Put succinctly, ‘the right

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hemisphere proposes, and the left hemisphere disposes’ (Taylor, 1988). Thus it is thought that the right hemisphere has a crucial role in figurative language processing (Kircher et al., 2007; Lauro et al., 2008). Much of the relevant work on differential involvement of left and right dlPFC in idiom processing has been performed with neurostimulation methods, particularly transcranial direct current stimulation (tDCS). However, support can also be found in neuroimaging evidence. For example, idiomatic interpretation of idioms and the literal interpretations of literal sentences has been shown to involve left hemisphere brain regions, whereas processing the literal interpretation of idioms was associated with increased activity in right hemisphere regions Thus the right hemisphere was indeed more sensitive than the left to distant semantic relations, and the left hemisphere was indeed more suitable for selecting a single interpretation and inhibition of irrelevant interpretations (Mashal et al., 2008). Elsewhere, there is further support from neuroimaging for frontal regions in the left hemisphere being associated with the processing of unambiguous idioms where there is little literal plausibility, but the processing of ambiguous idioms was not associated with any subthreshold regions of activity, in either hemisphere (Zempleni et al., 2007). However, unlike correlational methods such as functional magnetic resonance imaging, tDCS can provide causal evidence that a brain region is involved in a behaviour of interest (Filmer et al., 2014). Using tDCS we have subsequently demonstrated that in accordance with Beeman’s theory, for idioms left dlPFC stimulation enhances activation of top-down control over semantic processing, which improves performance when predictable idioms are followed by their most expected semantic meanings (e.g., figurative targets), reflecting activation of close semantic relationships. In contrast, stimulation of the right lateralised PFC network improved activation of top-down control over semantic processing in the right hemisphere, resulting in improved performance when unpredictable idioms are followed by

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their most expected semantic meanings (e.g., literal targets), reflecting activation of both close and distant semantic relationships (Sela et al., 2012). Inhibition of left and right dlPFC activity with tDCS might normally be expected to impair the perception of predictable and unpredictable idioms respectively. However, given the prominent impairments of lateralisation of brain function observed in schizophrenia (Ribolsi et al., 2009; OertelKnochel and Linden, 2011), one would not expect as clear a difference in performance accuracy according to idiom type in patients with schizophrenia following inhibition of left and right dlPFC activity. If one were to use tDCS to stimulate rather than inhibit dlPFC control systems and observe effects on idiom perception at the behavioural level, one would not expect the right dlPFC control system to improve perception of unpredictable idioms, nor the left dlPFC control system to improve perception of unpredictable idioms in people with schizophrenia.

6. Conclusions Idioms are a large class of figurative language expressions which together with their widespread use, should make them an important target of studies of language skills in people with schizophrenia. Future research is needed because the mechanism of impairment and its clinical significance remain speculative. It may also feed forward into some of the social impairments associated with schizophrenia. Indeed, understanding idioms is a challenging process, and not surprisingly perhaps, people with schizophrenia are prone to interpreting them incorrectly, often choosing the unintended literal meaning, particularly for less familiar and opaque idioms. Neither are people with schizophrenia able to use contextual clues appropriately to resolve the correct interpretation of idioms. At the clinical level, evidence has linked both positive and negative symptoms of the disorder to impaired idiom perception,

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but the stronger relationship seems to be with positive symptoms such as thought disorder. Further investigation is required though, to map out the mechanistic relationship between the impairment and the related symptoms. At the cognitive level, impairments in executive function, semantic processing and context integration have been proposed as possible antecedents of impaired idiom perception. However, these are not necessarily independent explanations, and context integration needs to be constrained by tighter definitions. Whilst one explanation on its own may not be sufficient to explain all aspects of the impairment observed in schizophrenia, in this climate of an uncertain candidate mechanism we put forward the contribution of impaired cognitive control for further testing. Cognitive control is an under-recognised yet integral aspect of semantic processing, widely known to be impaired in schizophrenia. Examining the effect of inherent variations in predictability on idiom perception could be especially informative for identifying why its constraints on semantic processing in healthy people do not function as well in people with schizophrenia. Indeed, such work could have more widespread implications for our more general knowledge of semantic processing in schizophrenia. The most obvious neuroanatomical focus of impaired cognitive control over language processing is the dorsolateral prefrontal cortex, a region whose functioning is widely known to be impaired relative to psychiatrically healthy people. Recent evidence from both fMRI and neurostimulation studies of idiom perception in people without schizophrenia provide testable hypotheses, including a differential role of right vs left dlPFC based on coarse vs. fine semantic coding.

Acknowledgements

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This work was supported by the I-CORE Program of the Planning and Budgeting Committee and The Israel Science Foundation (grant No. 51/11). References

Box 1. Key Concepts in Idiom Research: Theories & Definitions Main theories: Different classes of theories have been proposed to explain how idioms are represented and processed during comprehension. In general these accounts differ in several aspects: (a) the psycholinguistic dimension/s they emphasise as important; (b) the way that idiomatic meaning is represented in semantic memory; and (c) whether literal processing is believed to be mandatory for idiom comprehension. (1) Classic Non-compositional view – Literal first: Idiomatic meanings are retrieved when the literal interpretation of the string is contextually defective (Idiom-List Hypothesis; (Bobrow and Bell, 1973). Or, idioms are represented as long words, and retrieval of figurative meaning is initiated following presentation of the first word of an idiom (Lexical Representation Model; (Swinney and Cutler, 1979b). (2) Compositional view – Knowledge of an idiom’s internal semantic structure is necessary for understanding its idiomatic meaning, i.e., the interaction between an idiom’s literal and figurative meanings is mandatory in order to construct the meaning (Idiom Decomposition Hypothesis; (Gibbs et al., 1989); (Nunberg, 1978). (3) Hybrid approach - Idioms have unitary representations that may be directly retrieved when idioms are familiar or predictable, but they may also be compositionally analysed during comprehension, especially in the case of unfamiliar or unpredictable idioms (The

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Configurational Hypothesis, (Cacciari and Tabossi, 1988); The Hybrid Model, (Titone and Connine, 1999).

Main factors which influence idiom comprehension: Familiarity - The subjective frequency a person has with an idiom in its written or spoken form, regardless of their knowledge of the actual meaning of the phrase (Titone and Connine, 1999; Libben and Titone, 2008b). Predictability - The extent to which an idiom is completed idiomatically when the final word is omitted (Cacciari and Tabossi, 1988). Ambiguity or Literality - The extent to which an idiom has an alternative reasonable literal meaning. For example, some idioms, such as 'bite the bullet', have a well-formed literal meaning, whereas other idioms, such as 'break her word', only have a meaningful idiomatic interpretation. Compositionally - The extent to which the words of the idiom independently contribute to its figurative interpretation. There are two main classifications: Normally and Abnormally decomposable idioms. The first refer to idioms in which a part of the idiom is used literally (e.g., the 'question' in the expression 'pop the question'). The latter are expressions in which the referents of an idiom’s parts can be identified metaphorically (e.g., 'maker' in 'meet your maker', which metaphorically refers to a divine being).

Table 1. Direct Studies of Idiom Perception in Schizophrenia.

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Study

Task

Key Results

28

Suggested Mechanisms

Iakimova et al.

MCQ: Choose

Despite contextual

Anomalies processing

(2006)a

appropriate meaning

constraints, patients

semantic context.

of idiom from literal,

opted for literal

figurative, concrete or responses more often unrelated words

than controls

Iakimova et al.

Semantic decision

Controls understood

Functional

(2010)a

task: Relation of

figurative meaning

impairment in

target word to global

idioms of equal

semantic memory.

meaning of idiom

figurative and literal

Impaired suppression

salience better than

of literally salient

literal meaning, but

meaning

not patients Pesciarelli et al. (2014)a

Sentence continuation verification task: Is a target word a sensible continuation of the previous sentence fragment.

Patients slower in responding to literal and idiomatic sentences, but effects disappeared when cognitive deficits accounted for.

Schettino et al.

Sentence to picture

Patients impaired for

Residual schizophrenia does not contribute to slower processing of sensible idioms above and beyond cognitive deficits associated with schizophrenia. Impaired suppression

(2010)a

matching task: Did

both literal and

of literal meaning due

picture represent

idiomatic sentences.

to dysexecutive

meaning of idiomatic

Performance lower

deficits.

and literal sentences

for ambiguous than unambiguous idioms

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Strandburg et al.

Idiomatic recognition

Patients showed more Anomalies processing

(1997)

task: Judge whether

errors and longer

two-word phrases

RTs. ERP correlate:

(literal, idiomatic,

larger N400 to

nonsense) are

idioms and literals vs.

meaningful or not

controls

Lexical decision task:

Reduced priming for

Impaired suppression

Judge word vs. non-

literally plausible

of literal meaning due

word for

idioms but intact

to dysexecutive

idiomatically and

priming for literally

deficits.

linguistically-related

implausible idioms

Titone et al. (2002)

semantic context

target words Tavano et al. (2008)

Idiom explanation

Performance

Impaired pragmatic

task: Explain

impaired relative to

inferencing skills.

meaning verbally

controls

Also likely involves syntactic abilities.

a

Studies which demonstrated a link with symptoms of schizophrenia.Figure Captions

Figure 1. A Faulty Dorsolateral Prefrontal Cognitive Control Mechanism for Semantic Processing. The main sub-processes involved in the semantic processing necessary for understanding idioms, alongside the brain regions that underlie those processes.

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Stage 1: Configural Analysis – activation of fine semantic coding in the left hemisphere begins, alongside activation of coarse semantic coding in the right hemisphere. In parallel, dorsolateral prefrontal cortex (dlPFC) receives input on semantic representations from middle/superior temporal gyrus regions (MTG/STG). Stage 2: Anticipatory Control in dlPFC (probabilistic evaluation of the configuration) – How predictable is the string? Has the idiomatic key been activated? (2.1) If the idiom is predictable, e.g., the idiomatic key has been triggered, processing will be constrained to the left hemisphere, with top-down facilitation of the fine semantic field followed by direct retrieval of the idiomatic meaning, supported by the left IFG. (2.2) If the idiom is unpredictable, processing will be expanded into the right hemisphere. Two processes may take place: (a) response inhibition, supported by the right IFG; (b) facilitation of coarse semantic field in the right hemisphere.

We request that this figure is to be reproduced in color on the Web (free of charge) and in black-and-white in print.

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Psychiatric Research A possible contributory mechanism for impaired idiom perception in schizophrenia. Highlights The meaning of idioms is not derived from the meaning of their constituent words. People with schizophrenia often (mis)interpret idioms literally. Impaired idiom perception has clinical significance in schizophrenia. Current explanations are problematic, ill-defined and unconstrained. Impaired cognitive control may underlie impaired idiom perception in schizophrenia.