ORIGINAL RESEARCH published: 14 June 2019 doi: 10.3389/fnhum.2019.00205 Semantic Processing in Bilingual Aphasia: Evidence of Language Dependency Marco Calabria 1* , Nicholas Grunden 1,2 , Mariona Serra 1 , Carmen García-Sánchez 2 and Albert Costa 1,3 1 Center for Brain and Cognition, Pompeu Fabra University, Barcelona, Spain, 2 Hospital de la Santa Creu i Sant Pau, Barcelona, Spain, 3 Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain Individuals with aphasia frequently show lexical retrieval deficits due to increased interference of semantically related competitors, a phenomenon that can be observed in tasks such as naming pictures grouped by semantic category. These deficits are explained in terms of impaired semantic control, a set of abilities that are to some extent dependent upon executive control (EC). However, the extent to which semantic control abilities can be affected in a second and non-dominant language has not been extensively explored. Additionally, findings in healthy individuals are inconclusive regarding the degree to which semantic processing is shared between languages. In this study, we explored the effect of brain damage on semantic processing by comparing the performance of bilingual individuals with aphasia on tasks involving semantic control during word production and comprehension. Furthermore, we explored whether semantic deficits are related to domain-general EC deficits. First, we investigated the naming performance of Catalan–Spanish bilinguals with fluent aphasia and age- Edited by: matched healthy controls on a semantically blocked cyclic naming task in each of Beatriz Martín-Luengo, National Research University Higher their two languages (Catalan and Spanish). This task measured semantic interference School of Economics, Russia in terms of the difference in naming latencies between pictures grouped by the same Reviewed by: semantic category or different categories. Second, we explored whether lexical deficits Yasmeen Faroqi-Shah, extend to comprehension by testing participants in a word-picture matching task during University of Maryland, College Park, United States a mixed language condition. Third, we used a conflict monitoring task to explore the Claudia Peñaloza, presence of EC deficits in patients with aphasia. We found two main results. First, in both Boston University, United States language tasks, bilingual patients’ performances were more affected than those of *Correspondence: Marco Calabria healthy controls when they performed the task in their non-dominant language. Second, calabria.marc@gmail.com there was a significant correlation between the speed of processing on the EC task and the magnitude of the semantic interference effect exclusively in the non-dominant Received: 28 January 2019 Accepted: 29 May 2019 language. Taken together, these results suggest that lexical retrieval may be selectively Published: 14 June 2019 impaired in bilinguals within those conditions where semantic competition is higher, Citation: i.e.,- in their non-dominant language; this could possibly be explained by an excessive Calabria M, Grunden N, Serra M, amount of inhibition placed upon this language. Moreover, lexico-semantic impairments García-Sánchez C and Costa A (2019) Semantic Processing seem to be at least somewhat related to conflict monitoring deficits, suggesting a certain in Bilingual Aphasia: Evidence degree of overlap between EC and semantic control. of Language Dependency. Front. Hum. Neurosci. 13:205. Keywords: bilingual aphasia, semantic control, cycling naming, language dependency, executive control, doi: 10.3389/fnhum.2019.00205 language control Frontiers in Human Neuroscience | www.frontiersin.org 1 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia INTRODUCTION been extensively used to investigate semantic interference both in healthy individuals (Damian and Bowers, 2003; Belke et al., 2005; Lexical retrieval deficits in aphasia have many different potential Damian and Als, 2005; Navarrete et al., 2012; Belke, 2017) and sources of impairment including dysfunction in semantic in monolingual patients with aphasia (McCarthy and Kartsounis, selection, lexical selection, and/or phonological processing (Laine 2000; Wilshire and McCarthy, 2002; Schnur et al., 2006; Biegler and Martin, 2006). Some more recent views, specifically those et al., 2008; Harvey and Schnur, 2015) as a measurement of that take into account connectionist models, have broadly defined semantic competition during lexical selection. two main levels of retrieval: the first stage comprised of meaning and grammar and the second of phonological structure and content (Schwartz, 2014). In the present study, we aim to Semantic Processing in Healthy investigate the role of semantic control, defined as one of the Bilinguals: Language-Dependent mechanisms within the semantic network, in lexical retrieval or Independent? deficits within patients with bilingual aphasia. The results of a series of behavioral and neuroimaging studies Semantic control can be defined as a set of processes that agree with the hypothesis that there are similar principles of enable an individual to modulate retrieval of information based semantic representation across languages. For instance, studies on the contextual cognitive demand (Lambon Ralph et al., 2017) that used semantic cross-language priming found that, with and can be distinguished from semantic representation within highly proficient bilinguals, the magnitude of word priming the semantic cognition network (Jefferies, 2013; Lambon Ralph between semantically related words is similar irrespective of the et al., 2017). To some extent, this idea coincides with the concept language direction (e.g., Zeelenberg and Pecher, 2003; Perea et al., of ‘access deficits’ in semantic aphasia as opposed to the ‘storage 2008; Travis et al., 2017). Furthermore, when bilinguals have to deficits’ in semantic dementia (for a review, see Mirman and Britt, name pictures in a semantically demanding task, they show a 2004). Of particular interest within the context of post-stroke similar magnitude of semantic interference in both L1 and L2, aphasia is the control element of this semantic framework, since suggesting that semantic control abilities are independent of the semantic memory is usually spared (Jefferies and Lambon Ralph, language being utilized (Runnqvist et al., 2012). 2006; Jefferies et al., 2008; Rogers et al., 2015). Despite that some qualitative differences between languages Findings from neuroimaging studies have distinguished a have been found, the main results of relevant studies support semantic control network that includes the left prefrontal and the hypothesis of a shared conceptual/semantic system across temporo-parietal cortices, as opposed to the anterior temporal languages (Francis, 1999, 2005), as proposed in some models lobes, serving as crucial elements for conceptual representations of bilingual production and comprehension (BIA+ model: (Noonan et al., 2010, 2013). Interestingly, the neural model of Dijkstra and van Heuven, 2003; ICM: Green, 1986; RHM: semantic cognition proposed by Lambon Ralph et al. (2017) Kroll and Stewart, 1994). shows an overlap with the bilingual language control network in A second line of research has investigated the underlying which prefrontal areas are engaged in conflict resolution and the neural network of semantic processing in bilinguals on a posterior areas (inferior parietal lobules) in language selection variety of semantic tasks. Some studies concur that bilinguals (Abutalebi and Green, 2016; Calabria et al., 2018). Most studies show similar activation while they are processing semantic agree that a second language (L2) is mainly acquired through the representations in their L1 and L2, identifying a language- same neural devices responsible for the first language (L1) and invariant semantic network that includes the inferior temporal that the brain systems associated with the linguistic processing lobe (Grogan et al., 2009), superior temporal lobes (Chee et al., are shared between the two languages (e.g., Perani and Abutalebi, 2001; Pillai et al., 2003), frontal (Illes et al., 1999; Chee et al., 2005; Abutalebi and Green, 2007). Broadly speaking, we did 2001) or a more widely distributed set of language areas (Correia not expect there to be a difference in semantic control abilities et al., 2014; Van de Putte et al., 2017). One exception is a study for L1 and L2. However, some differences have been reported conducted by Klein et al. (2006) that found activation in the between the two languages when bilinguals have to process putamen when subjects performed L1-L2 translation but not semantic incongruence. In their review, Moreno et al. (2008) the inverse direction that coincided with an otherwise complete concluded that semantic processing in L2 is delayed, as measured overlap of activation for the two languages during a word by a delayed peak latency of the event-related potential (N400) generation task. associated with semantic violation, thus suggesting differences Finally, some evidence of the possible language-dependency in semantic integration between the bilinguals’ two languages. of semantic processing comes from sentence processing in Similarly, some bilingual models of speech production claimed bilinguals. Specifically, the event-related potential component that lexico-semantic representation might function differently for (N400) that indexes semantic violation has been found to be a bilingual’s two languages (Kroll and Stewart, 1994; Gollan et al., consistently delayed in its peak latency for L2 relative to L1 (for a 2008; Kroll et al., 2015; for a review see Branzi et al., 2018). review see Moreno et al., 2008). In the present study, we wanted to test the hypothesis of Therefore, although most studies agree that bilinguals show language-independency of semantic control by investigating the shared semantic networks for L1 and L2, some research revealed performance of bilingual patients with aphasia on semantic the presence of language-dependent processes, possibly related control tasks in their two languages (Catalan and Spanish). To do to the type of task used to assess semantic representation or so, we used the semantic blocked cycling naming task that has control. These results are in line with what some other models Frontiers in Human Neuroscience | www.frontiersin.org 2 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia of bilingual speech production have proposed. For instance, the interfere with the activation level of their two languages (Green, Revised Hierarchical Model (RHM) by Kroll and Stewart (1994) 1986). Therefore, the degree of within- and between-language assumes that the L1 lexicon is larger than that of L2 and that generalization depends on the interplay of these two mechanisms, the connections between L1 concepts are stronger than those namely how inhibitory control works to allow semantic activation between L2, which are thought to be attached to the L1 lexicon. to increase in one language and/or in both. Similarly, the ICM model by Green (1986) would predict different Interestingly, the idea that EC plays a role during semantic degrees of inhibitory control in each language that, once applied processing is similar to what was proposed by Lambon Ralph at the schema level, would modulate lexical selection according et al. (2017) for monolinguals. These authors claim that, along the dominance of the two languages. with an amodal ‘hub’ which functions by integrating different sources of information (Patterson et al., 2007), there are EC mechanisms that supervise how activation spreads throughout Semantic Deficits in Bilingual Speakers the semantic representation network. That is, there exists a With Brain Damage combination of two systems: one representational (temporo- Research that has investigated semantic deficits in bilingual parietal) and one for control (frontally distributed), with the patients with neurodegenerative disorders has shown similar latter being more closely related to semantic control deficits in impairments across languages, suggesting that semantic monolingual patients with aphasia (Harvey and Schnur, 2015). processing is language-independent (Mendez et al., 1999; Therefore, following the idea of the CSC model, we aimed Hernández et al., 2008, 2010). In the first study by Hernández to investigate whether semantic control may be differentially et al. (2008), patient JPG had similar category-specific deficits in affected in the two languages of bilinguals post-stroke. To do both languages (Spanish and Catalan) with worse performance so, we employed a blocked naming task that allowed us to in naming verbs than nouns. In a further study, Hernández manipulate the amount of interference during word retrieval et al. (2010) found that the semantic memory deficits of JFF for semantically-related competitors. This type of paradigm (a Catalan–Spanish bilingual patient) had a similar influence has been extensively used in studies with monolingual patients on his performance while he performed word translation in with aphasia to test the root causes of word retrieval deficits both language directions. In both studies, only some qualitative (e.g., Wilshire and McCarthy, 2002; Biegler et al., 2008; Schnur differences of errors between languages were reported, but the et al., 2009; Scott and Wilshire, 2010; Harvey and Schnur, main result supports a shared conceptual representation across 2015). According to some authors, this task can also help test languages (Francis, 1999, 2005). whether word retrieval deficits can be explained in terms of Also, studies performed on bilingual patients with aphasia an increased excitation or an excessive inhibition applied to have found that the representational level of knowledge is semantic competitors, resulting in the target words being less shared between languages. For example, Siyambalapitiya et al. available during lexical selection (Schnur et al., 2006). (2013) found that their patient (SN) not only showed intact Moreover, to specifically test the relationship between semantic priming in both languages, but also in the cross- semantic control processes and EC, we tested patients on a language condition (from English to Spanish), supporting a conflict monitoring task. The inclusion of this task was motivated language-independent nature of bilingual semantic memory. by a new body of research with bilingual aphasic patients that Other research within bilingual aphasia has uncovered a more highlights the cross-talk between deficits in language control and complex picture that would support the notion that, in post- in domain-general EC (Dash and Kar, 2014; Gray and Kiran, stroke aphasia, patients’ deficits arose from dysfunction in the 2015; Faroqi-Shah et al., 2016; for a review on this issue see control part of the semantic system instead of representational Calabria et al., 2018). system of knowledge as in dementia patients [see the controlled semantic cognition (CSC) model by Lambon Ralph et al., The Present Study 2017]. Some of this data comes from the study of cross- To investigate semantic control during speech production language generalization using semantic-based training (for a in patients, we employed a semantic blocked cyclic naming more extended discussion on cross-language issues in aphasia task. In this paradigm, participants were required to name see Faroqi-Shah et al., 2010; Khachatryan et al., 2016). For pictures in two conditions: (a) homogeneous, where pictures instance, Kiran and Roberts (2010) found that the only one belonged to the same semantic category (e.g., only animals), and of the four patients they tested after semantic-based naming (b) heterogeneous, where pictures belonged to different semantic treatment improved in the untrained language, suggesting that categories (e.g., animals, furniture, tools, etc.). The latencies in providing semantic information to improve lexical retrieval has the naming of elements in the heterogeneous condition become little to no cross-language transfer. Kiran et al. (2013b) in a faster over repetitions (cycles) whereas those in the homogeneous further study found a similar result of limited cross-language generally remain constant after the second cycle (e.g., Damian generalization for semantic representations. Interestingly, they and Bowers, 2003; Belke et al., 2005; Damian and Als, 2005; proposed that the degree of cross-language transfer might be Navarrete et al., 2012; Crowther and Martin, 2014; Belke, 2017). explained by the integrity of two independent mechanisms: the The difference in naming latencies between these two conditions first being a generalized mechanism involved in the spreading is an index of semantic interference that is increased in patients of activation brought about via treatment and the second being with aphasia compared to healthy individuals (e.g., Schnur inhibitory control which, in the case of bilingual speakers, would et al., 2006, 2009; Biegler et al., 2008; Scott and Wilshire, 2010) Frontiers in Human Neuroscience | www.frontiersin.org 3 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia due to hyper-activation or excessive inhibition of semantic To summarize, the current study was undertaken to explore competitors brought on by their language impairments. This two issues in the context of semantic control and bilingualism: agrees with the view that lexical selection is a competitive process (for a recent review see Nozari and Hepner, 2018). The (1) Are semantic control processes language-dependent automatic activation of semantically related items spreads to and differentially affected by brain damage in a their corresponding lexical representations and the target word bilingual’s two languages? competes for selection (for non-competitive models see Costa (2) Are semantic control processes dependent on general- et al., 1999; Mahon et al., 2007). domain EC mechanisms such as conflict monitoring The general hypothesis about semantic control in bilingualism and resolution? was that if semantic control was language-independent, we expected to see a similar increase of semantic interference in both languages in patients with aphasia compared to healthy MATERIALS AND METHODS controls. Indeed, according to the models that have proposed that lexical selection in bilinguals is qualitatively similar to that Participants of monolinguals, we should expect language-independency of A total of 11 Catalan–Spanish patients with bilingual aphasia semantic control (Costa et al., 1999; Caramazza and Costa, 2000; were recruited from the Speech Therapy Unit of Hospital de la La Heij, 2005; Finkbeiner et al., 2006). Santa Creu i Sant Pau in Barcelona. All patients were speakers On the other hand, if semantic control was language- of both Catalan and Spanish prior to stroke, exhibited adequate dependent, we expected to see higher interference in one hearing and vision, demonstrated stable health status and were language compared to the other. Presumably, more semantic in the chronic stage for language disorders (more than 1 year impairment would occur in the non-dominant language if it were post-injury). The etiology was brain tumor for one patient (Pt2) related to EC deficits (e.g., Abutalebi and Green, 2007, 2016) and cerebrovascular (either ischemic or hemorrhagic stroke) or had weaker connections between lexical and semantic units for all other patients. All patients had lesions localized in the (e.g., Kroll and Stewart, 1994). left hemisphere. In order to assess the integrity of semantic representations, we A group of 13 healthy individuals also participated in the study employed a bilingual word-picture matching task. Participants as controls; their demographic and linguistic characteristics were were required to match a picture presented on the screen with one matched to those of patients with aphasia. of two word options (semantically related, same category). The main reasoning behind the inclusion of this task was to measure Language Assessment the accuracy of patients as compared to healthy controls on the To define the type and the degree of language impairment, the task and thus to exclude the possibility of any representational Spanish version of the Western Aphasia Battery (Kertesz and deficits in semantic memory. We adopted a bilingual version Pascual-Leone García, 1990) was administered by Dr. García of the matching task because this type of paradigm allowed us Sánchez, a clinical neuropsychologist with expertise in aphasia to test both languages in the same task and because we have from the same hospital. The WAB is a comprehensive test of already seen previous evidence that it serves as a robust task language functions with a relatively short test administration time for testing comprehension in bilinguals (Macizo et al., 2010; (30–60 min) and includes four language subtests which assess Mosca and de Bot, 2017). spontaneous speech, comprehension, repetition, and naming Additionally, we investigated the integrity of EC with a to calculate an Aphasia Quotient (AQ). Patients were only conflict monitoring task in patients and healthy controls. This tested in Spanish since a Catalan version of the WAB is not task has been used previously in studies with bilingual patients currently available. with the aim to investigate the relationship between language According to WAB assessment, one patient was classified as control and EC deficits (Green et al., 2010; Gray and Kiran, having conduction aphasia, two with Wernicke’s aphasia and 2015). We correlated patients’ performance on this EC task with eight classified as presenting anomic aphasia. The degree of the semantic blocked cyclic naming task, with the degree of language impairment ranged from mild to moderate (55.6 to the correlation indicating to what extent the two domains of 84.5 out of 100) and the mean values for each subtest were: control overlap. The available literature on this issue reports 14.1/20 (±2.6) for Fluency, 8.2/10 (±1.2) for Comprehension; mixed findings and the number of studies performed with 7.4/10 (±1.7) for Repetition, and 7.4/10 (±1.1) for Naming (see bilingual patients after stroke in which the two domains have Table 1 for details). been compared is very slim (for a review see Calabria et al., Patients’ language abilities were also tested using part C 2018), resulting in a need for further research on this issue. of the Bilingual Aphasia Test (BAT, Paradis and Libben, Therefore, an overlap of deficits in both domains would suggest 1987) which assesses cross-language abilities over four subtests: that domain-general EC is also involved in language selection. Word Recognition, Word Translation, Sentence Translation, and That is, the hyper-activation or -inhibition upon the semantic Grammatical Judgment. In Word Recognition, patients were competitor during lexical selection would be intimately related asked to select the correct translation for each word from a list to non-linguistic EC processes (inhibitory control and/or conflict of 10 possible choices (5 words per language; max. score = 10). resolution), as predicted by the ‘executive selection account’ In the Word Translation task, patients needed to verbally supply (Wilshire and McCarthy, 2002). the translation of a word spoken by the examiner (10 words Frontiers in Human Neuroscience | www.frontiersin.org 4 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia LogToken per language; max. score = 20). Increasing in difficulty, subjects LogType/ NDL 0,92 0,88 0,88 0,87 0,89 0,91 0,83 0,80 0,77 0,89 0,88 then were asked in the Sentence Translation task to provide a translation of a sentence that could be repeated a maximum LogToken of three times by the examiner (scoring based on correct LogType/ translations of 3 sections of each sentence for 6 sentences in each 0,92 0,87 0,85 0,86 0,83 0,91 0,86 0,80 0,79 0,95 0,87 DL language; max. score = 36). Finally, in Grammatical Judgment, patients were asked to determine whether a sentence spoken by DL vs. NDL the examiner was grammatically correct and, if incorrect, how to p-values BAT-C- 0.405 0.407 0.675 0.675 0.533 0.817 0.830 0.828 0.106 0.834 0.007 fix it (scoring based on correct judgment of grammatical structure and accurate correction of grammatical mistakes if applicable for 8 sentences per language; max. score = 28). These subtests of Aphasia Quotient (AQ). Range of severity of the scores: 0–25: Very severe; 26–50: Severe; 51–75: Moderate: > 76: Mild. DL: dominant language; NDL: non-dominant language. BAT -C NDL the BAT-C were administered by a bilingual neuropsychologist, (max. 48) completing all four tasks in one direction of translation followed 24 19 18 26 24 12 30 17 36 28 9 by the same four tasks in the other direction (i.e., Catalan to Spanish in all tasks followed by Spanish to Catalan). BAT-C DL Furthermore, to have an additional measure of language (max. 48) impairment in their two languages, we asked patients to describe 29 24 21 29 28 14 30 16 17 46 26 two complex picture scenes: the Cookie Theft Picture (Goodglass and Kaplan, 1972) and the scene description from the WAB. They CAST CAST CAST CAST CAST CAST CAST CAST NDL CAT CAT CAT were instructed to use Catalan to describe the scene in one session and Spanish in the other, with this order counterbalanced across CAST CAST CAST CAT CAT CAT CAT CAT CAT CAT CAT DL subjects. If some features of the pictures were neglected, the experimenter pointed to them and asked the patient to mention (max. 10) Naming them. Speech was recorded and subsequently analyzed off-line. 8.10 8.60 6.50 6.30 8.90 7.30 8.90 5.80 5.70 8.10 6.90 We collected one recording for each language, each lasting 3 min. After transcribing the descriptions in each language, the Repetition total number of words (tokens) and the number of different (max. 10) 8.10 6.40 8.20 7.00 6.20 8.60 9.70 7.10 3.20 9.60 7.30 words (type) were calculated. In order to reduce the impact of sample size, we calculated the individual token-type ratio for each TABLE 1 | Individual scores of patients for the Western Aphasia Battery and Bilingual Aphasia Test (Part C). language by using the following transformation logtype /logtoken Comprehension (Kong, 2016). (max. 10) 8.50 9.25 7.30 8.40 6.75 9.55 9.50 6.90 6.25 10.00 7.90 Language Profile Language history and dominance were determined by means of a questionnaire administered to the participants and an (max. 20) interview with them. Pre-morbid language proficiency in the Fluency 12.00 18.00 10.00 15.00 16.00 14.00 15.00 10.00 13.00 18.00 14.00 two languages (Catalan and Spanish) was self-rated by each participant on a four-point scale of their abilities of speaking, comprehension, writing and reading (1 = poor, 2 = regular, Mild to moderate Mild to moderate 3 = good, 4 = perfect). As can be appreciated in Table 2, Moderate Moderate Moderate Moderate Moderate Moderate Severity Mild Mild Mild both patients and healthy controls were highly proficient in all four linguistic domains (see also Appendix I for individual data). Moreover, participants were considered early bilinguals as, on average, they were first regularly exposed to their (max. 100) quotient∗ Aphasia 71.00 84.50 64.00 73.40 75.70 79.90 88.20 57.60 56.30 92.40 72.20 non-dominant language at 6 years of age, thus not differing significantly from the exposure to their dominant language. Finally, language usage was rated based on ten questions in Months which participants were required to report with what frequency onset post- 131 122 108 119 73 46 49 21 84 66 14 they spoke each of the two languages across different periods of their lives. The final score was transformed into a percentage CONDUCTION Aphasia type (from 0 meaning using only Spanish to 100% meaning using WERNICKE WERNICKE ANOMIC ANOMIC ANOMIC ANOMIC ANOMIC ANOMIC ANOMIC ANOMIC only Catalan, around 50% translating to balanced use of the two languages). Both patients and healthy controls reported equal amounts of Catalan and Spanish usage and thus would be considered balanced bilinguals. Patients The bilinguals that participated in this study acquired their Pt10 Pt11 Pt1 Pt2 Pt3 Pt4 Pt5 Pt6 Pt7 Pt8 Pt9 two languages at the same time and it is difficult to say which Frontiers in Human Neuroscience | www.frontiersin.org 5 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia TABLE 2 | Socio-demographic and linguistic characteristics of the samples. whereas, for others, this pattern was reversed. Sets of 16 different pictures for each language were presented four times (cycles) Patients with Healthy in 4 Homogenous as well as 4 Heterogeneous blocks, with aphasia controls a total number of 128 naming trials per participant. Eight (n = 11) (n = 13) different lists consisting of 128 stimuli each were created for each language, avoiding the repetition of the same set of pictures M SD M SD p-values between languages. Age (years) 58.2 6.4 55.4 4.1 0.29 Each trial included the following elements: a fixation point Education (years) 13.6 1.7 14.4 1.2 0.18 presented for 750 ms followed by the picture to be named Age of regular dominant 2.1 0.7 2.2 0.3 0.52 which appeared for up to 2000 ms or until response was language use provided. After each block, participants were allowed to rest. Age of regular non-dominant 4.6 1.6 4.8 1.2 0.75 In order to reduce the number of errors due to possible name language use disagreement/confusion, participants were presented with the set Language proficiency (1–4) of pictures before the experimental task and were asked to name Dominant language them in the required language. Participants were tested in two Speaking 4.0 0.0 3.9 0.3 0.35 languages (Catalan and Spanish) and, when possible, over two Comprehension 4.0 0.0 4.0 0.0 – different sessions staggered week apart. The order of language Reading 3.7 0.6 4.0 0.0 0.21 testing was counterbalanced across participants. Writing 3.7 0.6 3.9 0.3 0.21 The dependent variables were naming latencies (RTs), which Non-dominant language 3.9 0.3 4.0 0.0 0.30 were analyzed off-line with Checkvocal (Protopapas, 2007), Speaking and accuracy. Errors were classified as follows: ‘No response,’ Comprehension 3.9 0.3 4.0 0.0 0.30 when the patient was unable to name the object; ‘semantic,’ Reading 3.9 0.4 3.8 0.4 0.51 when they produced an incorrect word semantically related Writing 3.7 0.6 4.0 0.0 0.16 to the target; ‘cross-language intrusion,’ when they produced % Language use 54.5 15.3 45.1 20.8 0.22 the correct word but in the incorrect language; ‘phonological paraphasia,’ when they deleted, substituted or added phonemes to the correct word describing the picture; and ‘unrelated,’ when would be their L1 or L2. Therefore, we used the terms ‘dominant’ they produced a word with no relation, semantic or otherwise, to and ‘non-dominant’ instead of L1 and L2 to refer to their the target word. languages. The use of ‘dominant’ refers to the language that they prefer to use (or they feel more comfortable speaking), even if Bilingual Word-Picture Matching Task they reported that their ‘non-dominant’ language was at the same Stimuli were made up of 60 pictures from different semantic level of proficiency and frequency of usage as their dominant. categories selected from Snodgrass and Vanderwart (1980) According to this definition, 3 patients and 3 healthy controls database. A list of 240 words was also selected consisting of two were classified as Spanish-dominant bilinguals while the rest were types of stimuli: (a) 120 as target words corresponding to the classified as Catalan-dominant bilinguals. picture presented (60 in Catalan and 60 in Spanish); (b) 120 as distractor words semantically related to target words (60 in Materials and Procedure Catalan and 60 in Spanish). Distractor and target words were The experimental software used for the administration of all of the same semantic category. Each picture was presented with tasks was DMDX (Forster and Forster, 2003). All the participants a pair of words, one being the target and the other being the performed three experimental tasks: the semantic blocked cyclic distractor. The pictures and the words were presented in a mixed naming task, the bilingual word-picture matching task, and the language condition (Catalan and Spanish), but within each trial flanker task. Before starting the experimental procedure, the the two words were from the same language. There were two patients signed an informed consent approved by the ‘Parc de types of trials: repeat trials in which participants had to match Salut MAR’ Research Ethics Committee under the reference the picture to a target word in the same language as the target number: 2018/8029/I. of the previous trial, and switch trials in which participants were required to do the matching within the opposite language Semantic Blocked Cyclic Naming Task compared to the previous trial. There were a total of 120 trials Stimuli consisted of 32 pictures total with 8 exemplars from presented in the following manner: 43 Spanish repeat trials, 43 4 semantic categories (animals, vegetables, kitchen tools, and Catalan repeat trials, 17 Spanish switch trials and 17 Catalan furniture) selected from the Snodgrass and Vanderwart (1980) switch trials; the task was thus comprised of 28% switch trials database (see Appendix II for the details of the stimulus). and 72% repeat trials. Every trial started with a fixation point Participants were required to name 8 blocks of pictures: 4 blocks (a black cross) in the center of the screen displayed for 500 ms, containing semantically related items (Homogenous) and 4 followed by a picture and two words below for a maximum of blocks containing semantically unrelated items (Heterogeneous). 2500 ms. Participants were required to match the target word For some participants, two Homogenous blocks were followed with the picture presented on the screen by pressing one of by four Heterogeneous and then two Homogenous blocks two keys on the keyboard. The two keys used for the response Frontiers in Human Neuroscience | www.frontiersin.org 6 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia corresponded to the word appearing on the same side of the Reaction Times (RTs) computer as the key (i.e., “z” corresponding to the word on The analysis with healthy controls showed that main effects the left side of the screen). Dependent variables were defined as of Condition [F(1,12) = 1307, p = 0.004, η2p = 0.52] and RTs and accuracy. Cycle [F(3,36) = 17.41, p < 0.001, η2p = 0.59] were significant, but not Language [F(1,12) = 0.05, p = 0.82]. The interaction Flanker Task between Condition and Cycle was also significant [F(3,36) = 5.79, Target stimuli consisted of a row of five horizontal black p = 0.002, η2p = 0.33]. Post hoc analyses showed that, in the lines with arrowheads pointing left or right, with the central Heterogeneous condition, naming latencies became faster over arrow acting as the true target. Participants were instructed to cycle (1st cycle: M = 712.91 ms, SD = 34.88; 2nd cycle: M = 664.67, indicate the direction (left or right) of the central arrow via SD = 27.47 ms; 3rd cycle: M = 639.18 ms, SD = 27.01; 4th cycle: pressing one of two keys on the keyboard. The target (central M = 629.23 ms, SD = 24.06; ps < 0.05). On the other hand, arrow) was presented in two main conditions: with congruent naming latencies in Homogeneous conditions only decreased flankers (same direction as the target) and incongruent flankers from the first (M = 709.32 ms, SD = 27.71) to the second cycle (opposite direction). The event presentation was as follows: (a) (M = 672.24 ms, SD = 28.72) (p = 0.04). No other interaction a fixation point (a plus sign) appeared at the center of the was significant. screen for 400 ms, and (b) the target arrow and the flankers The analysis that included both groups showed that the main were presented simultaneously until the participants responded effects of Condition [F(1,22) = 58.12, p < 0.001, η2p = 0.72] and or for up to 2000 ms. The experiment consisted of two blocks Cycle [F(1,22) = 9.28, p < 0.001, η2p = 0.29] were significant, but of 48 trials each, for a total of 96 trials. The proportion of not Language [F(1,23) = 0.52, p = 0.48]. Also, the main effect of congruent trials was 75% (n = 72) to 25% for incongruent Group was significant [F(1,22) = 39.79, p < 0.001, η2p = 0.64] trials (n = 24). Participants gave their responses by pressing indicating that patients overall were slower (M = 1107.41 ms, either the ‘V’ or ‘M’ key according to the direction in which SD = 44.05) than controls (M = 671.75 ms, SD = 46.87) in the arrow target was pointing. The dependent variables were performing the task (see Figure 1 and Table 3). RTs and accuracy. The interaction between Condition and Cycle was also significant [F(3,66) = 5.25, p = 0.003, η2p = 0.19]. Post hoc analyses showed that in the Heterogeneous condition naming latencies RESULTS became faster from the first cycle (M = 960.27 ms, SD = 33.98) to the second (M = 917.93 ms, SD = 34.17) to the third cycle Language Impairment in Two Languages (M = 873.25 ms, SD = 39.12) (ps < 0.05). On the other hand, For each participant, we compared the scores of the BAT-C of naming latencies in Homogeneous conditions only decreased the two languages using a Chi-squared test with Yates’ correction; from the first (M = 966.16, SD = 32.45 ms) to the second cycle ten out of eleven patients showed parallel language deficits (only (M = 918.51 ms, SD = 36.78) (p = 0.03). Pt10 showed a significantly more impaired score in their non- Finally, the Language × Condition × Cycle interaction dominant compared to their dominant language, see Table 1). [F(3,66) = 4.05, p = 0.01, η2p = 0.15] as well as the Language × For connected speech, paired t-tests were used to analyze Condition × Cycle × Group interaction were significant differences between languages (dominant vs. non-dominant); [F(3,69) = 3.15, p = 0.03, η2p = 0.12]. Further analyses were and no difference was found between the two languages in any conducted by comparing the semantic interference effects (diffe- patient [log type/log token: dominant language = 0.87, non- rence in naming latencies between the Homogenous and the dominant language = 0.86; t(10) = −0.09, p = 0.92] (see Table 1). Heterogeneous condition) within the two groups of participants These two results show that our patients had parallel for each language separately. In the non-dominant language, language impairments. the magnitude of the semantic interference effect was larger in patients than in controls for the cycles 3 [patients: M = 178.27 ms, SD = 41.90; controls: M = 39.69 ms, SD = 38.54; F(1,24) = 5.92, Semantic Blocked Cyclic Naming Task p = 0.02, η2p = 0.21] and 4 [patients: M = 182.36 ms, SD = 52.61; We first explored the effects of semantic blocking in healthy controls: M = 39.46 ms, SD = 48.40; F(1,24) = 3.99, p = 0.05, η2p individuals by performing repeated-measures ANOVAs = 0.15]. In the dominant language, the magnitude of the semantic including Condition (Homogenous vs. Heterogeneous), interference effect did not differ between patients and healthy Language (Dominant vs. Non-dominant), and Cycle (1, 2, 3, controls across cycles (all ps > 0.05). and 4) as within-subject factors in the control group only. In a further analysis, we performed repeated-measures ANOVAs including the same within-subject factors and Group as a Accuracy between-subject factor (patients with aphasia vs. healthy The analysis with healthy controls revealed no main effect or controls). The analyses were performed for two dependent interaction that was statistically significant. variables—RTs and accuracy—separately. RTs were analyzed The analysis with both groups showed that the main effect of for correct responses only. Moreover, RTs across all conditions Group was significant [F(1,22) = 14.51, p = 0.001, η2p = 0.40], exceeding three standard deviations above or below mean were indicating that the patients’ performance (M = 82.25%, SD = 3.22) excluded from the analyses for each participant. was lower than that of controls (M = 98.83%, SD = 2.95). Also, the Frontiers in Human Neuroscience | www.frontiersin.org 7 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia FIGURE 1 | Naming latencies (ms) of the semantic blocked cycling naming task as a function of languages, semantic conditions, cycles, and groups of participants. main effect of Cycle [F(3,66) = 7.33, p < 0.001, η2p = 0.25] and the The analyses were performed for two dependent variables—RTs interaction between Cycle and Group [F(3,66) = 5.61, p = 0.002, and accuracy—separately. Two patients did not complete this η2p = 0.20] were significant. Post hoc analyses reveal that patients, task; therefore, the group comparison was carried out between 10 but not controls, showed little increase of accuracy in the cycle 3 patients and 13 healthy controls. RTs were analyzed for correct (M = 83.93%, SD = 3.09, p = 0.03) and 4 (M = 84.34%, SD = 2.96, responses only. Moreover, RTs across all conditions exceeding p = 0.02) compared to the first (M = 78.91%, SD = 3.62). three standard deviations above or below mean were excluded from the analyses for each participant. Error Analysis The frequency of error types for the two languages is detailed below: TABLE 3 | RTs in the semantically blocked cyclic naming task for healthy controls - No response: 54.23% of dominant language errors and 51.10% and patients with aphasia. of non-dominant language errors; Dominant language - Phonological errors: 12.31% of dominant language errors and 11.16% of non-dominant language errors; Cycle 1 Cycle 2 Cycle 3 Cycle 4 - Semantic errors: 14.46% of dominant language errors and M SE M SE M SE M SE 15.61% of non-dominant language errors; - Cross-language intrusions: 9.23% of dominant language errors Patients with aphasia and 12.26% of non-dominant language errors; Heterogeneous 1160 54 1041 62 1032 58 983 52 - Unrelated: 9.77% of dominant language errors and 9.87% of Homogeneous 1158 43 1109 54 1046 64 1113 64 non-dominant language errors. Healthy controls Heterogeneous 728 52 668 60 642 55 630 50 Bilingual Word-Picture Matching Task Homogeneous 723 41 678 52 668 62 662 61 In an initial analysis, repeated-measures ANOVAs were Non-dominant language performed including Type of Trial (repeat vs. switch) and Patients with aphasia Language (Dominant vs. Non-dominant) as within-subject Heterogeneous 1151 70 1143 74 1028 73 1051 84 factors in healthy controls only. Following said analysis, Homogeneous 1186 84 1095 74 1205 83 1225 87 repeated-measures ANOVAs were performed with the same Healthy controls within-subject factors but also including Group (patients Heterogeneous 705 68 661 71 637 70 630 81 with aphasia vs. healthy controls) as a between-subject factor. Homogeneous 695 80 668 71 678 80 676 84 Frontiers in Human Neuroscience | www.frontiersin.org 8 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia Reaction Times (M = 92.79%, SD = 1.71) were less accurate than healthy controls The analysis with healthy controls revealed no main effect (M = 97.84%, SD = 1.52). No other main effect or interaction was or interaction that was statistically significant [Type of Trial: statistically significant (see Table 4). F(1,12) = 0.87, p = 0.37; Language: F(1,12) = 0.23, p = 0.64; Type of Trial × Language: F(1,12) = 0.03, p = 0.86]. Flanker Task In the analysis with both groups, the main effect of Type of Repeated-measures ANOVAs were performed including Type of Trial [F(1,22) = 3.28, p = 0.08] and Language [F(1,22) = 1.57, Trial (congruent vs. incongruent) as a within-subject factor and p = 0.22] were not statistically significant. However, the main Group (patients with aphasia vs. healthy controls) as a between- effect of Group was significant [F(1,22) = 57.85, p < 0.001, subject factor for RTs and accuracy separately. RTs were analyzed η2p = 0.72], indicating that patients (M = 1942.52 ms, SD = 75.45) for correct responses only. Moreover, RTs across all conditions performed more slowly than healthy controls (M = 1051.88 ms, exceeding three standard deviations above or below mean were SD = 72.24). Also, the interactions between Type of Trial and excluded from the analyses for each participant. Language [F(1,22) = 4.95, p = 0.04, η2p = 0.18] and Type of trial × Language × Group [F(1,22) = 4.44, p = 0.05, η2p = 0.17] Reaction Times were significant (see Table 4). The main effect of Type of Trial was significant [F(1, 22) = To explain the triple interaction, further ANOVAs were 1191.73, p < 0.001, η2p = 0.85], suggesting than participants performed including Type of Trial and Language as within- were slower in incongruent (M = 990.33 ms, SD = 285.6) subject factors for the groups separately. In healthy individuals, than in congruent (M = 879.64 ms, SD = 278.52) trials. Also, no main effect nor interactions were statistically significant the main effect of group was significant [F(1,22) = 28.31, [F s < 1]. In patients, only the interaction between Type of p < 0.001, η2p = 0.57], indicating that patients with aphasia Trial and Language was significant [F(1,10) = 4.87, p = 0.05, were slower (M = 1148.32 ms, SD = 285.74) than healthy η2p = 0.35]. Post hoc analysis showed that patients performed controls (M = 711.09 ms, SD = 86.19) to perform the task. similarly in repeat (M = 1949.81, SD = 92.91 ms) and switch trials Finally, the interaction between Type of Trial and Group was not (M = 1938.27 ms, SD = 128.88 ms; p = 0.80) in their dominant statistically significant [F(1,22) = 2.11, p = 0.17], suggesting that language, but significantly slower in switch (M = 1998.90 ms, the magnitude of the conflict cost was the same for the groups SD = 104.61) than repeat (M = 1882.09 ms, SD = 76.80) trials (see Table 5). when they performed the task in their non-dominant language (p = 0.04). This result suggests that patients suffered switch cost Accuracy in their non-dominant language whereas controls did not. The main effect of Type of trial was significant [F(1,22) = 7.05, p = 0.01, η2p = 0.25], suggesting higher accuracy in congruent Accuracy (M = 98.97%, SD = 4.14) than in incongruent trials (M = 97.56%, In the analysis with healthy controls, we found a main effect SD = 2.31). However, no significant difference was found between of Type of trial to be significant [F(1,12) = 7.19, p = 0.02, patients with aphasia (M = 97.12%, SD = 3.07) and healthy η2p = 0.37], suggesting that participants were less accurate in controls (M = 99.26%, SD = 1.45) [F(1, 22) = 2.78, p = 0.11]. switch (M = 96.86%, SD = 0.74) than repeat (M = 98.82%, SD = 0.29) trials (see Table 4). No other main effects or Correlations Between Linguistic and interactions were statistically significant. Non-linguistic Measures In the analysis with both groups, the main effect of To address one of our hypotheses that language deficits might Type of trial was significant [F(1,22) = 5.11, p = 0.03, be related to non-linguistic control deficits, we performed η2p = 0.21], suggesting that participants were less accurate in correlations between each individual’s performance on the tasks switch (M = 93.91%, SD = 1.32) than repeat (M = 96.43%, used to assess both domains. SD = 1.53) trials. Also, the main effect of Group was significant [F(1,22) = 4.09, p = 0.05, η2p = 0.17] indicating that patients TABLE 5 | RTs and accuracy in the flanker task for healthy controls and patients with aphasia. TABLE 4 | RTs and accuracy in the bilingual word-picture matching task for Healthy Patients with healthy controls and patients with aphasia. controls aphasia Healthy controls Patients with aphasia Type of trial Means SE Means SE Repeat SE Switch SE Repeat SE Switch SE RTs RTs Congruent 649 47 1087 51 Dominant language 1051 61 1059 82 1949 66 1882 90 Incongruent 772 45 1200 49 Non-dominant language 1041 64 1052 87 1938 70 1998 95 Conflict costs 123 113 Accuracy Accuracy Dominant language 98.8 1.5 96.5 2.7 94.1 1.6 89.8 2.9 Congruent 99.9 0.7 98.0 0.6 Non-dominant language 98.6 1.1 97.0 2.1 94.1 1.2 92.6 2.2 Incongruent 98.6 1.2 96.5 1.2 Frontiers in Human Neuroscience | www.frontiersin.org 9 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia FIGURE 2 | Correlations between non-linguistic (speed of processing and conflict cost) and the linguistic (semantic interference) measures for the two languages. For the non-linguistic domain, we used the individual speed of [speed of processing: r(10) = −0.35, p = 0.16; conflict cost: processing (congruent and incongruent trials) and the magnitude r(10) = 0.19, p = 0.61] or linguistic performance in patients for of the conflict cost (RTs on incongruent trials minus RTs on both languages on the semantic blocked naming task [dominant congruent trials) on the flanker task. For the linguistic domain, language: r(10) = −0.45, p = 0.14; non-dominant language: we used the magnitude of the semantic interference effect (RTs r(10) = 0.41, p = 0.24] and on the bilingual matching task in homogeneous blocks minus RTs in heterogeneous block) and [dominant language: r(10) = 0.09, p = 0.82; non-dominant switch costs at the individual level for both dominant and non- language: r(10) = 0.15, p = 0.70]. dominant languages within the semantic blocked cyclic naming task and the bilingual matching task, respectively. For the dominant language, the magnitude of the semantic DISCUSSION interference did not correlate with the speed of processing [r(24) = 0.15, p = 0.48] and the conflict cost of the flanker task With this study we aimed to investigate the language dependency [r(24) = −0.06; p = 0.77] (see Figure 2). The switch costs in their of semantic processing in bilinguals. To address this question, dominant language did correlate with the speed of processing we explored the performance of bilinguals with fluent aphasia [r(24) = 0.89, p < 0.001], but not with the cost seen in the flanker and parallel language impairment on tasks of production task [r(24) = −0.13; p = 0.55]. and comprehension within their two languages. Furthermore, However, for the non-dominant language, the magnitude we used an EC task to explore whether the control mechanisms of the semantic interference did correlate with the speed of in the linguistic and non-linguistic domain may overlap. processing [r(24) = 0.62, p = 0.001] and the conflict cost of the We found three main results. First, semantic control processes flanker task [r(24) = −0.43; p = 0.05]. The switch costs for the related to lexical selection are language-dependent, as measured non-dominant language correlated with the speed of processing by a larger semantic interference effect during non-dominant [r(24) = 0.86, p < 0.001] but not with the cost seen in the flanker language production in bilingual patients with aphasia. Second, task [r(24) = −0.26; p = 0.22]. the retrieval of semantic representations might have also a certain Moreover, the degree of language impairment as indexed by degree of language dependency under specific conditions, such as the AQ of the WAB did not correlate with either non-linguistic dual language contexts. Third, the linguistic processes of semantic Frontiers in Human Neuroscience | www.frontiersin.org 10 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia control show only partial overlap with those of domain-general Different hypotheses have been proposed for the pathological EC (i.e., during conflict monitoring). effects found in patients when they have to name elements within semantically homogeneous conditions (Schnur et al., 2006, 2009; Harvey and Schnur, 2015). Our results seem to suggest that the Language Dependency of Semantic problem experienced by aphasic patients in reducing semantic Control in Production competition possibly comes from an excessive inhibition of We found evidence of language dependency for the semantic lexical representations (McCarthy and Kartsounis, 2000). The control system in bilinguals. Our bilingual patients with aphasia semantic similarity between items would cause an increased showed a higher semantic interference effect than healthy level of inhibition on non-target words that would spread controls and, interestingly, to a greater degree when they did throughout the network; this same inhibition would then make the task in their non-dominant language. First, it is important a following, semantically related lexical item less accessible. to stress that this result cannot be attributed to an imbalance Indeed, patients with aphasia showed more omissions than of proficiency in the two languages in patients. In studies such semantic errors, supporting the notion that they were not as ours, it becomes necessary to exclude this variable as one of able to retrieve the correct name because it was completely the factors that could explain differences in semantic processing inhibited. Moreover, this inhibitory process seems to be within- between languages in bilingual patients with aphasia (Kiran language since our patients did not produce many cross-language and Edmonds, 2004; Lorenzen and Murray, 2008; Kiran and intrusions. This interpretation is more compatible with our Roberts, 2010; Kiran et al., 2013a,b; Khachatryan et al., 2016). findings than other hypotheses that proposed over-activation at Given that patients in our study acquired their non-dominant the semantic level that builds up across cycles (Belke et al., 2005; language early on and had a similar frequency of usage in both Schnur et al., 2006; for a non-competitive selection account see their languages before injury, this possible confounding factor Navarrete et al., 2014). of language proficiency cannot account for the greater semantic Interestingly, patients’ ability to inhibit competitors during interference in the non-dominant language observed. lexical retrieval was especially reduced while they were Our results regarding semantic control complement previous performing the task in their non-dominant language. This is not studies that investigated the network of semantic representation to say that the semantic representations of their non-dominant in bilinguals. As reviewed in the Introduction, most of the language were more affected. Rather, in control-demanding neuroimaging studies have shown that bilinguals use very situations such as naming in their non-dominant language similar neural networks while they process semantic features during homogenous conditions, lexical retrieval engaged the of their L1 and L2 (e. g., Illes et al., 1999; Chee et al., control network of semantic cognition to a greater degree 2001; Pillai et al., 2003; Grogan et al., 2009; Correia et al., and, in turn, resulted in a slowing down of the process. These 2014; Van de Putte et al., 2017). Similarly, neuropsychological results could be explained by some of the models of bilingual studies of bilingual patients with semantic memory impairment language production that have proposed language-dependency indicate a comparable decline of the two languages, suggesting of lexico-semantic processing. For instance, Kroll and Stewart a common and shared neural network in the temporal lobe (1994) asserted that the lexico-semantic connections between (Mendez et al., 1999; Hernández et al., 2008, 2010). However, L2 and L1 are weaker than those between L1 and L2; Gollan it is important to highlight that, in the case of bilingual et al. (2008) also claimed that difference in frequency of language aphasia, we do not expect a deficit in semantic memory at usage might explain why L2 retrieval is more demanding for the representational level, but rather a deficit in the control bilinguals. However, Kroll and Stewart (1994)’s proposal is components of semantic retrieval (Jefferies and Lambon Ralph, mainly based on data with late bilinguals and the predictions of 2006; Noonan et al., 2010). Similar to some extent to the their model are not entirely applicable to the population of early previous concept of “access,” semantic control is in charge bilinguals that we studied (for a critical discussion of this issue, of retrieving the semantic information needed for a specific see Hernández et al., 2010). The only way to interpret our results context and depends upon cognitive demand (Jefferies et al., with the Kroll and Stewart (1994)’s model would be to assume 2008). Given this distinction, semantic control would be more difference in the level of activation for lexical competition of the affected in patients having lesions in fronto-temporoparietal two languages (Kroll et al., 2010). areas due to decreased capacity to inhibit semantic competitors while their semantic representations could be spared (Jefferies Language Dependency of Semantic and Lambon Ralph, 2006; Jefferies et al., 2008; Rogers et al., Control in Comprehension 2015). Therefore, we believe that our patients relied more on Differential language impairment observed in speech production these control processes, within the linguistic domain, while also extended to comprehension. Our main aim was originally they named pictures in those semantically blocked conditions to study semantic processing during word production, but we where they were required to inhibit competitors. This type of decided to also include a comprehension task to check the competitive process has consequences at the lexical level, during integrity of the semantic representations. Although the matching selection and retrieval of the words. Accordingly, although we task was not designed to measure the blocking and cycling effects manipulated the degree of semantic competition within our task, of semantic interference, we found that when the two languages we cannot exclude a possible effect at the lexical level since it is are mixed in a semantic matching task, the non-dominant interconnected with the semantic units. is more affected than the dominant one. Conversely, healthy Frontiers in Human Neuroscience | www.frontiersin.org 11 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia controls did not show any switch cost and this is probably biased by patients’ performance: given they are already very slow due to the nature of task. The studies that have used semantic to respond in the congruent conditions, their “reduction” in categorization and lexical decision in healthy individuals have conflict cost might be reflecting this generalized slowness rather showed that switch costs are not always reliable in the matching than a true decrease in cost. In any case, this result seems to tasks or they are reduced compared to production, probably indicate that semantic competition does not overlap with general- because they require less involvement of language activation and domain EC mechanisms responsible for conflict resolution, inhibition (e.g., Orfanidou and Sumner, 2005; Macizo et al., contrary to what other studies have suggested (Crowther and 2012; Mosca and de Bot, 2017). We might say that this result Martin, 2014; Canini et al., 2016). Moreover, our patients were in patients at the comprehension level could be related to some not impaired in conflict resolution as they had similar levels of deficits in the access of lexical representations for the non- conflict costs as healthy controls. However, they were generally dominant language. Following brain damage, the competitive slower, suggesting that the EC deficit they likely possessed was process (possibly of inhibitory nature) for lexical selection in the in conflict monitoring (Botvinick et al., 1999; Botvinick et al., non-dominant language could be affected and this would explain 2001; Yeung, 2013). Conflict monitoring allows for the detection why patients are more impaired in that language. Previous of potentially conflicting situations and subsequent adjustment neuroimaging studies in bilinguals found mixed results: some of behavior when there is a switch from non-conflict situations that the control network described for language production (congruent trials) to conflict ones (incongruent trials) and (Abutalebi and Green, 2007, 2016; Calabria et al., 2018) is also vice versa. Therefore, the positive correlation between semantic active during word comprehension and recognition tasks (Peeters interference and speed of processing may be interpreted in terms et al., 2019), but some other studies suggest that the overlap of an overlap of monitoring abilities (or deficits in these abilities between the two system is only partial (Abutalebi et al., 2007; for aphasic patients) between the linguistic domain (semantic Blanco-Elorrieta and Pylkkänen, 2017). control) and non-linguistic EC. Conflict resolution has been These results show that the language-dependent nature of related to frontal activity (anterior cingulate cortex, Botvinick semantic control processes in bilinguals with aphasia during et al., 2001; for evidence in bilinguals see Abutalebi et al., 2012) word production in single language contexts extends to word and it is possible that this region was spared in our patients comprehension in dual language contexts. However, caution since they have fluent aphasia, a type of language disorder more is required when interpreting these results due to important strongly related to temporo-parietal damage. Therefore, we have methodological differences between the two tasks. Despite the to acknowledge the possibility that they did not show a deficit fact that the bilingual word-picture matching task could also be in conflict resolution because they did not have brain damage in defined as a semantic task, participants performed it in a dual frontal areas. Indeed, we know that higher semantic interference language condition, whereas, in the semantic blocked naming effects in bilingual patients are related to EC deficits when task, the two languages were not mixed. Future research should they have brain damage extending to the inferior frontal gyrus, examine whether semantic control processes continue to exhibit as shown in a study by Schnur et al. (2009). a language-dependent nature during word comprehension when Previous studies that have compared linguistic to non- tested in single language contexts. linguistic performance using a flanker task in bilingual patients with aphasia (Green et al., 2010; Verreyt et al., 2013; Dash and Semantic Control and EC in Bilinguals Kar, 2014; Gray and Kiran, 2015) have shown that there is an The ‘executive selection account’ proposes that the effect of incomplete overlap between the two control systems. Further interference generated in the semantic blocked cyclic naming studies should explore other EC components, such as working task is mediated by the involvement of domain-general EC memory and switching abilities, to determine whether these mechanisms that are outside of the linguistic domain (Wilshire non-linguistic control mechanisms are more closely related to and McCarthy, 2002). In fact, there is evidence that performance language control deficits in bilingual speakers. on the Stroop task correlates with naming latencies in homogeneous conditions, suggesting that inhibition at response selection level would be the same in EC and semantic control CONCLUSION (Crowther and Martin, 2014). Similarly, the involvement of the The results of our study suggest that semantic control may be left inferior frontal gyrus and the left caudate nucleus has been language-dependent and selective language impairment could interpreted as the EC network being responsible for resolving be explained by an excessive inhibition placed upon the lexical interference of semantic competitors (Canini et al., 2016). Given representations of the non-dominant language. Additionally, this evidence, we included the flanker task to measure individual semantic interference seems to be at least somewhat related to domain-general EC performance. conflict monitoring deficits, suggesting a certain degree of overlap Our results partially support this account. We found a positive between EC and semantic control. correlation between the magnitude of the semantic interference effect and the speed of processing in the flanker task, but only for the non-dominant language. There was also a negative ETHICS STATEMENT correlation between semantic interference and conflict cost, suggesting that a reduced magnitude of semantic interference is This study was carried out in accordance with the associated with smaller conflict costs. This observation is likely recommendations of the “Parc de Salut MAR - Research Ethics Frontiers in Human Neuroscience | www.frontiersin.org 12 June 2019 | Volume 13 | Article 205 Calabria et al. Semantic Processing in Bilingual Aphasia Committee” with written informed consent from all subjects. Regional (FEDER, European Regional Development Fund) under All subjects gave written informed consent in accordance with project PSI2017-87784-R. This work was also supported by grants the Declaration of Helsinki. The protocol was approved by the from the Catalan government (2017 SGR 268 and 2009 SGR “Parc de Salut MAR - Research Ethics Committee” (reference 1521) and the European Union’s Seventh Framework Program number: 2018/8029/I). for Research (No. 613465). AUTHOR CONTRIBUTIONS ACKNOWLEDGMENTS MC conceived the research, designed the experiments, We would like to dedicate this publication in memory of AC. His and analyzed the data. NG, CS, and MS collected the scientific contributions have been of great importance to the field experimental and neuropsychological data. Moreover, all the of bilingualism and we are infinitely grateful to him for having authors equally contributed to writing of the manuscript and been part of this study as one of the authors. discussion of the results. FUNDING SUPPLEMENTARY MATERIAL MC was supported by the postdoctoral Ramón y Cajal fellowship The Supplementary Material for this article can be found (RYC-2013-14013) and Agencia Estatal de Investigación (AEI, online at: https://www.frontiersin.org/articles/10.3389/fnhum. National Research Agency) and Fondo Europeo de Desarrollo 2019.00205/full#supplementary-material REFERENCES and connectivity study. Hum. Brain Map. 37, 4179–4196. doi: 10.1002/hbm. 23304 Abutalebi, J., Brambati, S. M., Annoni, J.-M., Moro, A., Cappa, S. F., and Caramazza, A., and Costa, A. (2000). The semantic interference effect in the Perani, D. (2007). The neural cost of the auditory perception of language picture-word interference paradigm: does the response set matter? Cognition switches: an event-related functional magnetic resonance imaging study in 75, B51–B64. bilinguals. J. Neurosci. 27, 13762–13769. doi: 10.1523/JNEUROSCI.3294-07. Chee, M. W. L., Hon, N., Lee, H. L., and Soon, C. S. (2001). 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