TYPE Original Research PUBLISHED 10 October 2022 DOI 10.3389/fpsyg.2022.880398 Short-term memory and OPEN ACCESS sentence comprehension in Catalan aphasia EDITED BY Maria Andreou, University of Peloponnese, Greece REVIEWED BY Seçkin Arslan, Io Salmons1,2*, Helena Muntané-Sánchez1 and Anna Gavarró1,2 Centre National de la Recherche Scientifique (CNRS), France 1 Acquisition and Pathology Lab, Departament de Filologia Catalana, Universitat Autònoma de Matthew Walenski, Barcelona, Bellaterra, Spain, 2 Centre de Linguïstica Teòrica, Universitat Autònoma de Barcelona, East Carolina University, United States Barcelona, Spain Giuditta Smith, University of East Anglia, United Kingdom The main goal of the present study is to investigate visual and verbal short- *CORRESPONDENCE Io Salmons term memory side to side with sentence comprehension in Catalan-speaking io.salmons@uab.cat subjects with aphasia in comparison with subjects without brain damage. SPECIALTY SECTION We aim to examine whether there are any significant correlations between This article was submitted to their performance on short-term memory and comprehension tasks in order Language Sciences, a section of the journal to evaluate the hypothesis that linguistic and memory deficits in aphasia Frontiers in Psychology are the result of a dysfunction of a common mechanism, usually short- RECEIVED 21 February 2022 term memory. Eigthy-four control subjects and twelve individuals suffering ACCEPTED 12 September 2022 from different types of aphasia were assessed using the Catalan version of PUBLISHED 10 October 2022 the Comprehensive Aphasia Test (CAT-CAT), which includes one recognition CITATION Salmons I, Muntané-Sánchez H and task and two digit and word span tests to evaluate visual and verbal short- Gavarró A (2022) Short-term memory term memory, respectively, as well as a sentence-to-picture comprehension and sentence comprehension in task. The results showed that the performance of subjects with aphasia was Catalan aphasia. Front. Psychol. 13:880398. significantly low on all tasks. Yet, the logistic regression analysis revealed doi: 10.3389/fpsyg.2022.880398 that the magnitude of the differences between the control and experimental COPYRIGHT group varied across subtests, and that visual short-term memory was better © 2022 Salmons, Muntané-Sánchez preserved than verbal memory. The results also showed that there were no and Gavarró. This is an open-access article distributed under the terms of significant correlations between memory and language comprehension, which the Creative Commons Attribution rules out the hypothesis that the deficits observed are due to a common License (CC BY). The use, distribution or reproduction in other forums is underlying mechanism. Individual variation was also observed, specially on permitted, provided the original memory subtests, which suggest that memory impairments cannot explain the author(s) and the copyright owner(s) comprehension deficit in aphasia. are credited and that the original publication in this journal is cited, in accordance with accepted academic KEYWORDS practice. No use, distribution or reproduction is permitted which does aphasia, short-term memory, sentence comprehension, neuropsychological not comply with these terms. assessment, cognitive disorders, Catalan, syntactic comprehension 1. Introduction The association between language and other cognitive skills in aphasia has been explored for long (see, among others, Archibald et al., 1967; Helm- Estabrooks et al., 1995; Kasselimis et al., 2013; Fonseca et al., 2016; Gonzalez et al., 2020). Despite the fact that aphasia has traditionally been considered a language-primary deficit (Geschwind, 1970), several studies have reported significant cognitive impairments in individuals with aphasia. In fact, there is evidence that cognitive abilities such as visual and auditory attention, Frontiers in Psychology 01 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 verbal and visuospatial short-term and working memory or found that a higher educational level did correlate with a higher executive function are impaired in aphasia (Nicholas et al., performance in the nonverbal tasks from the Cognitive Test 2005; Seniów et al., 2009; Murray, 2012; El Hachioui et al., Battery for Global Aphasia (Marinelli et al., 2006), but not age or 2014; Lee and Pyun, 2014; Choinski et al., 2020). For instance, time post onset. Murray (2012) argued that different patterns of in a review of 47 works on the subject, Fonseca et al. (2016) performance could be associated with different aphasia types, as found that 61.3% of the studies reported a lower performance her findings showed that only individuals with anomic aphasia in nonverbal cognitive tasks of subjects with aphasia compared presented relatively spared attention measured through the Test to healthy subjects. This has led several authors to question of Everyday Attention (Robertson et al., 1994), whereas variables whether the core deficit in aphasia is linguistic in nature and to like age, education or aphasia severity did not have any effect argue that the linguistic difficulties are rather caused by attention on performance. Laures-Gore et al. (2011), on the other hand, and/or memory dysfunctions (Murray, 1999; Aboitiz et al., 2006; found a significant association between severity of aphasia and McNeil et al., 2011; Code, 2018). However, this conclusion is working memory measures, as well as Choinski et al. (2020). In controversial in view of many other studies reporting spared or summary, even though there is wide evidence that individuals relatively spared nonverbal cognition (Gathercole and Baddeley, with aphasia tend to present nonverbal cognitive deficits, it is 2001; Potagas et al., 2011; Murray, 2012; Fedorenko and Varley, still unclear to what extent and what causes them, and whether 2016; Little et al., 2019). they are directly correlated or not with their linguistic deficits. The studies on the relationship between specific nonverbal To further investigate this issue, in the present study we and verbal cognitive skills in individuals with aphasia are examine visual and verbal short-term memory (STM), which also inconclusive. While some studies have reported significant refers to the ability to temporary store and maintain information associations between linguistic and nonverbal cognitive tasks (Baddeley, 2003), and its relationship to language skills. The (Fucetola et al., 2009; Murray, 2012; Lee and Pyun, 2014; relevance of memory in the linguistic deficits observed in Marinelli et al., 2017; Wall et al., 2017; Choinski et al., 2020), aphasia was already pointed out in the first descriptions of others have not found any significant relationship between them aphasia (Benton and Joynt, 1960; Luzzatti and Whitaker, 1996). (van Mourik et al., 1992; Helm-Estabrooks, 2002; Ivanova et al., In more recent years, many authors (e.g., Baddeley, 2003; 2017; Little et al., 2019). Aboitiz et al., 2006; Sung et al., 2009; Potagas et al., 2011) Also, most of the studies observed a great variability among have claimed that individuals with aphasia present primary individuals with aphasia in nonverbal cognitive measures which, deficits in STM or working memory (WM), a specific form as some have already argued (Murray, 2012; Marinelli et al., of STM that is responsible for the manipulation of the 2017), suggests that cognitive deficits alone cannot explain information while executing cognitive operations (Baddeley and the linguistic impairments in aphasia. In fact, there are other Hitch, 1974). The Baddeley and Hitch’s STM model involves factors that may explain the cognitive difficulties observed. different components, among which a phonological loop and a Fonseca et al. (2016), who carried out a systematic review of visuospatial sketchpad as temporary storage systems of verbal- studies published between 1995 and 2015, found that most acoustic and a visuospatial information. In addition, the central of the subjects with post-stroke aphasia performed in several executive system was postulated as an attentional control nonverbal cognitive tasks similar to left and right brain damaged system. According to Baddeley (2003), conduction aphasia is the subjects without aphasia. The authors interpreted these results as paradigmatic example of a disruption of the verbal STM which evidence against the assumption that aphasia, mostly caused by results in the impaired ability to repeat sentences and sequences left hemisphere damage, causes nonverbal cognitive deficits, and of digits. argued instead that the nonverbal cognitive impairment may STM deficits in fact have been observed in different types be the result of the brain dysfunction itself or even dementia, of aphasia. There is ample evidence that people with aphasia despite the fact that the relationship between aphasia and (PWA) often perform worse than control subjects on span tasks dementia is not well-understood yet. Other researchers like, that evaluate WM and STM (e.g., Friedmann and Gvion, 2003; El Hachioui et al. (2014) argued that depression could be the Seniów et al., 2009; Christensen and Wright, 2010; Laures- reason behind the cognitive deficits in individuals with aphasia, Gore et al., 2011; Wall et al., 2017; Christensen et al., 2018). since they are much more prone to suffer from depression than Yet, as already discussed, the results are subject to great healthy subjects. variability. Potagas et al. (2011), for example, conducted a study Although several authors have pointed out that other on spatial and verbal short-term and working memory of a variables could account for the lack of a consistent pattern group of PWA, whose poor performance on both types of in aphasic performance, there is discrepancy on the factors memory correlated with the severity of the aphasia. They used that interact with cognitive function. According to Helm- a battery of tests that included the WAIS-III digits forward Estabrooks et al. (1995), age, educational level, and the severity and backward tests, the Corsi block-tapping task and the of aphasia did not influence the aphasic performance in Greek Boston Aphasia Examination—Short Form (Tsapkini et al., nonverbal cognitive tasks. By contrast, Marinelli et al. (2017) 2009). They also observed a dissociation between both types Frontiers in Psychology 02 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 of memory in most patients, as spatial memory was intact in capacity does not affect the accuracy of participants in 43 out of 58 patients and, interestingly, the results between comprehension tasks. spatial and verbal memory did not correlate. The authors Many studies have found significant correlations between interpreted these findings as evidence against the assumption the performance of PWA on STM and sentence comprehension that there is an underlying common mechanism that explains tasks (Fucetola et al., 2009; Seniów et al., 2009; Sung et al., language and memory deficits in aphasia, and argued that other 2009; Christensen and Wright, 2010; Lee and Pyun, 2014; Wall variables would account for the covariance between memory and et al., 2017; Zakariás et al., 2018). Varkanitsa and Caplan (2018) language deficits and aphasia severity. conducted a meta-analysis of studies published between 1980 Similarly, Lang and Quitz (2012) found that the results and 2017 and concluded that the results showed significant on memory tasks from the Kurze Aphasieprüfung KAP Short associations between STM and sentence comprehension. Some Assessment for Aphasia (Lang et al., 1999) and the Wechsler authors interpreted them as evidence that STM measures could Memory Scale Revised (Härting et al., 2000) correlated with predict the comprehension abilities of PWA, whereas others the severity of aphasia, rather than the type of aphasia. They claimed that language difficulties explained the STM deficits also observed that verbal tasks were more likely to be impaired (see Wright and Fergadiotis, 2012 for a review). Yet, these than nonverbal tasks, which they interpreted as evidence of correlations could reflect the influence of other factors rather disruption of a more general component of WM in contrast than causal relationships and, in any case, they do not reveal with Potagas et al. (2011). On the other hand, Fedorenko and whether the common cause is a language- or a memory-related Varley (2016) examined neuroimaging data from a group of deficit. One of the challenges of assessing cognitive skills is subjects with severe global aphasia and concluded that they were that most behavioral tasks rely on different cognitive domains able to carry out nonverbal cognitive tasks that required storage that cannot be tested separately. STM is required in sentence of information in working memory. Gathercole and Baddeley comprehension and, similarly, linguistic abilities are needed to (2001) also claimed that nonverbal cognition is preserved in complete verbal STM tasks. Broca’s aphasia. Hence, despite some lack of consistency in the In summary, despite many unsolved issues, it is well- data, verbal STM seems to be more affected than nonverbal established that aphasia often involves non-linguistic cognitive memory in aphasia. deficits that need to be assessed (and subsequently taken into In the present study, we also assess the auditory consideration in treatment). Thus, further research is needed to comprehension of sentences which requires, among others, examine the relationship between linguistic and other cognitive syntactic and semantic knowledge, and investigate whether skills in aphasia. The goal of the present study is to investigate it significantly correlates with STM measures. In spite of the visual and verbal short-term memory as well as sentence fact that anomia was traditionally considered the core deficit comprehension of Catalan-speaking subjects with different types in aphasia, from the 70’s sentence comprehension has been of aphasia and, in the second place, to examine whether there extensively investigated in several languages, and it is well- is any correlation between their performance on the short-term known that it is compromised even in non-fluent aphasias (e.g., tasks and their scores in the sentence comprehension task in Caramazza and Zurif, 1976; Schwartz et al., 1980; Grodzinsky, order to establish the nature of the deficit. 1990; Hickok et al., 1993; Grillo, 2009). The comprehension Let us consider the hypothesis that linguistic and memory deficit of certain sentence types has been explained in terms of deficits in aphasia are the result of a dysfunction of a common memory impairment (e.g., Hickok, 2000; Stowe, 2000; Aboitiz mechanism. If so, the prediction that follows is that PWA will et al., 2006; Varkanitsa and Caplan, 2018), and also as the perform poorly on all tasks, but also that a significant correlation result of linguistic deficits (e.g., Grodzinsky, 2000; Bastiaanse between STM and language comprehension subtests will be and van Zonneveld, 2005; Friedmann, 2006; see Garraffa and observed. Moreover, an association between visual and verbal Fyndanis, 2020). In fact, both language and STM are argued STM scores is to be expected if a common component of STM, to rely on extensive neural networks and have been often namely the central executive (Baddeley and Hitch, 1974), is located in the same areas (see Varkanitsa and Caplan, 2018 affected. On the other hand, if the memory deficit is domain- for a review), in particular, phonological working memory specific and affects only one of the two subsystems responsible relies on extensive temporoparietal-prefontal connections for the storage of information, then a dissociation between the according to Hickok and Poeppel (2000) or the inferior PWA’s performance on visual and verbal tasks is predicted, as frontal gyrus according to Aboitiz et al. (2006). According to well as a significant correlation between the impaired STM type Caplan and Waters (1999), the single-resource (SR) hypothesis and the comprehension task [in line with the SR hypothesis makes the prediction that the accuracy of participants in a postulated by Caplan and Waters (1999)]. comprehension task is associated with their memory capacity, Alternatively, if the primary impairment in aphasia is whereas the separate-sentence-interpretation-resource (SSIR) language-related but not dependent on memory capacity hypothesis makes the opposite prediction, that is, that memory (following the SSIR hypothesis and other grammatical Frontiers in Psychology 03 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 TABLE 1 Demographic characteristics of the participants. Llenguatge de l’Hospital de Sant Pau and the Grup de Suport Neuropsicològic. The inclusion criteria involved self-reported Control group n = 84 Aphasic group n = 12 language and cognitive skills within normal range before the Age (years) stroke. Details of age, education, handedness, etiology, aphasia 18–29 18 (21.4%) 0 (0%) subtype, and time post-onset collected from the medical health 30–39 8 (9.5%) 0 (0%) record of the PWA appear in Table 2. The participants with 40–49 12 (14.3%) 5 (41.7%) aphasia were diagnosed by speech pathologists and neurologists in the abovementioned centers according to clinical criteria and 50–59 17 (20.2%) 3 (25%) formal or informal tests mostly carried out in Spanish, since 60–69 14 (16.2%) 1 (8.3%) there are no available standardized tools in Catalan to diagnose 70–79 8 (9.5%) 2 (16.7%) aphasia. Since one of the goals of the study was to determine +80 7 (8.3%) 1 (8.3%) the feasibility of cognitive testing with CAT-CAT, the aphasic Education sample represents the variability found in clinical practice (The Basic 18 (21.4%) 0 (0%) CAT does not aim at discriminating among aphasia types and Intermediate 34 (40.5%) 5 (41.7%) does include an aphasia severity scale; Swinburn et al., 2004). Higher 32 (38.1%) 7 (58.3%) A chi-square goodness of fit test revealed that the Sex proportions in both groups differed by dialect use (χ 2 = 10.57, Female 50 (59.9%) 7 (58.3%) p = 0.005), but not by education level (χ 2 = 5.76, p = 0.056). Male 34 (40.5%) 5 (41.7%) On the other hand, a Wilcoxon-Mann-Whitney and a Fisher Dialect exact tests indicated that there were no significant differences Western 30 (35.7%) 0 (0%) between the two groups with respect to age (U = 658.5, p = Eastern 54 (64.3%) 12 (100%) 0.399) and sex (two-tailed p = 1). characterizations of aphasia), we would predict poor 2.2. Materials performance of PWA on comprehension and, to a lesser extent, verbal STM tasks, since linguistic skills are required to The participants were administered the Catalan version of carry them out. Importantly, significant correlations between the Comprehensive Aphasia Test (CAT; Swinburn et al., 2004) STM and comprehension subtests would not be expected, given adapted by Salmons et al. (2021), which consists in a battery of that sentence comprehension and STM tasks rely mainly on twenty-seven subtests that evaluate both cognitive and linguistic different cognitive mechanisms. This does not exclude the skills, including the four behavioral tasks reported in the present possibility of more general cognitive impairments in some study. Three of these tasks assessed visual and verbal short- individuals, in line with previous research. term memory, and required the storage and maintenance of information (Baddeley, 2007). These type of tasks have been shown to be appropriate for use with subjects with brain damage 2. Materials and methods (Wright and Fergadiotis, 2012). The last task evaluated the comprehension of different sentence types. The words and 2.1. Participants structures tested are not subject to variation between Eastern and Western Catalan, and therefore the tasks were suitable for Eighty-four control subjects of ages between 18 and 90 all participants independently of the dialect they spoke. years (M = 50.6) participated in the study, as well as twelve participants of ages between 44 and 92 years (M = 58.5) suffering from different types of chronic aphasia, due to acquired brain injury in the left hemisphere. All the participants were 2.2.1. Visual short-term test bilingual speakers of Catalan and Spanish, though Catalan The first test assessed visual STM through a recognition task, was their dominant language (and they spoke various dialects and it included a practice item and ten experimental items. The of Catalan), and they had different educational backgrounds participants were presented with four images and were asked (Table 1). According to a self-report, none of the control to point to the one that they had already seen in a previous participants had a history of brain injury, cognitive disorders, task, administered at least 3 min before, that evaluated semantic or learning disabilities. memory. Each token includes the target picture and three The participants with different types of aphasia were selected unrelated distractors; the pictures can be found in Salmons et al. from the patient pools of several hospitals in the Barcelona area, (2021), and cannot be reproduced here since they are subject to namely the Hospital Sant Rafael, the Escola de Patologia del copyright. The score was the number of correct responses. Frontiers in Psychology 04 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 TABLE 2 Individual characteristics of subjects with aphasia. Subject Age Sex Education Handedness Etiology TPO (years) Aphasia 1 78 F 3 Right Tumor 12 Anomic 2 56 F 3 Right CVA 9 Anomic 3 92 M 2 Right CVA 0.84 Conduction 4 47 F 3 Right Tumor 5 Global 5 45 M 2 Right CVA 9 TM 6 78 F 2 Right HCVA 2 TM 7 44 M 3 Right HCVA 3 TM 8 54 F 2 Right CVA 10 Wernicke 9 48 M 2 Right CVA 6 – 10 60 M 3 Right CVA 8 – 11 49 F 3 right HCVA 11 – 12 51 F 3 right Tumor 24 – Sex: F, female; M, male. Education: 1, basic; 2, intermediate; 3, higher. Etiology: CVA, cerebrovascular accident; H, hemorrhagic; TPO, time post-onset. Aphasia: TM, transcortical motor aphasia. 2.2.2. Verbal short-term memory tests In both tasks, each level had two trials. Hence, the Verbal SMT was measured through two repetition tasks in participants had two opportunities per level to repeat the digit which subjects were asked to repeat digit strings and sentences string or the sentence correctly. If the participant failed to repeat that gradually increased in length. The digit repetition test (or the digit string or the sentence on the first trial, the examiner digit span test) consisted in a total of six tokens, starting with asked him/her to repeat a second string or sentence in the a two-digit string (e.g., 7 2) and increasing the length by one same level. If the participant repeated it correctly, the examiner in each token up to a string of seven digits (e.g., 2 8 7 4 5 1 proceeded with the first trial of the next level. However, if the 2). The score was the number of digits that the participant was participant failed to repeat both trials at one level, the task able to repeat without mistakes (digit span). All numbers were was terminated. Phonetic and dyspraxic errors were not taken monosyllables (vuit “eight”), except for number four (qua.tre). into account. In the sentence repetition task (or sentence listening span test), participants were asked to repeat sentences that gradually increased in length starting from sentences with three content 2.2.3. Sentence comprehension test words (1) to sentences with six content words. The complete list The fourth subtest consisted in a sentence-picture matching of the items can be found in the Supplementary materials. task. The participants were shown four pictures and were asked to listen to a sentence read by the examiner, and point to the picture that matched the sentence heard (Figure 1). The task (1) El gat atrapa el ratolí. included a total of 18 sentences with simple and common words “The cat catches the mouse.” (2), given that its purpose is to detect syntactic disorders rather than lexical difficulties (Swinburn et al., 2004). The main goal The score was the number of content words (e.g., nouns of the task is to identify a problem in sentence comprehension and verbs) that the participant was able to repeat without error without going into the diagnosis of aphasia type, and so a (listening span). Function words are not taken into account wide range of syntactic structures are included, such as active in this type of task since the aim of the test is to evaluate sentences with one and two arguments (2a), or constructions the memory capacity rather than the grammatical competence that have been shown to be problematic in aphasia like passives of participants (Swinburn et al., 2004). As an anonymous and clitic left dislocations (2b) (see Gavarró and Dotti, 2014; reviewer pointed out, difficulties in the repetition of grammatical Salmons, 2015 for Catalan). morphemes could possibly be associated with agrammatism, but the scoring system of CAT does not contemplate these measures (2) a. L’home menja una poma. given the goal of the test—see, however, the discussion on this the-man eats an apple point. In fact, other types of repetition tasks are used to evaluate “The man is eating an apple.” the linguistic abilities of PWA (e.g., Friedmann, 2001) and other b. A la cartera, la persegueix la cuinera. populations (see, for example, Lust et al., 1996; Marinis and to the postwoman her chases the cook Armon-Lotem, 2015). “The postwoman, the cook is chasing her.” Frontiers in Psychology 05 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 FIGURE 1 (A–D) Materials presented in the sentence comprehension task for the item in (2b). Reproduced with permission from Servei de Publicacions de la UAB, available at https://ddd.uab.cat/pub/llibres/2021/250143/prointafa_a2021b.pdf. The task includes five active sentences with two arguments, by far a natural pause/delay, and may reflect difficulties with three active sentences with one argument, two passives, two clitic executive function (decision making), attention, memory, or left dislocations, one sentence with a relative clause, and five motor function to execute the response; therefore one might sentences with Prepositional Phrases (PP). Whereas, all passives have expected a shorter cuttoff point to evaluate the participant’s and clitic left dislocations were semantically reversible sentences, delay in producing an answer. Admittedly, response time cutoffs only some of the actives with two arguments and PPs were vary from test to test (see Evans et al., 2020 for a review), but semantically reversible. The complete list of items can be found other aphasia diagnostic tools use the 5 s cutoff, for example the in the Supplementary materials. Boston Diagnosis Aphasia Evaluation (Goodglass et al., 2001) in The materials for semantically reversible sentences (2b) its word comprehension task. Therefore, the choice made in the included the target picture, and two lexical foils and a role CAT is by no means exceptional and we adhere to it here. reversal as distractors (Figure 1). The agents were placed both on the left and on the right of the picture to control for any bias resulting from picture paralleling the order of mention of 2.3. Procedure the subjects and objects. There were two scoring systems in this task. The first one is based on a 0–1 scale: correct responses The procedure of the study was approved by the UAB scored 1, whereas incorrect or no responses scored 0. On the Ethics Committee (CEEAH 5656) and followed the Declaration other hand, the second one is based on a 0–2 scale: incorrect of Helsinki ethical standards. All the subjects provided their or no responses scored 0; correct responses initiated within the written informed consent prior to participation. Participants first 5 s were assigned a value of 2; correct responses after a 5 were tested in medical institutions or at home by trained s-delay, a repetition of the item on request or a self-correction examiners. The experimental tasks were conducted in a quiet were penalized and given a value of 1. By taking into account room to minimize distractions. Control subjects completed these variables, this latter system allows to assess qualitative the CAT-CAT (Salmons et al., 2021) in a 40 min session, differences in the participants’ responses (Howard et al., 2010). whereas subjects with aphasia needed up to 1 h sessions. An anonymous reviewer pointed out that the 5 s cuttoff of Prior to the task, the participants were interviewed to collect the Comprehension Aphasia Test may be too long as it exceeds relevant personal and medical information. Then the examiner Frontiers in Psychology 06 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 TABLE 3 Correct responses by task and group. Subtest Max Group Mean SD Range Median IQR Visual STM 10 Control 9.69 1.15 2–10 10 10–10 Aphasic 9.08 1.51 5–10 10 8.5–10 Verbal STM Digit span 7 Control 5.99 1.11 3–7 6 4–7 Aphasic 4 1.13 2–6 4 3.5–4 Listening span 6 Control 5.99 0.11 5-6 6 6–6 Aphasic 4.75 1.22 3–6 4.5 4-6 Sentence comprehension 0–1 scale 18 Control 17.61 0.68 14–18 18 17–18 Aphasic 13.67 2.71 7–17 14 12.5–17 0–2 scale 36 Control 34.39 1.87 24–36 35 24–35 Aphasic 22.17 5.83 12–33 23.5 12–23.5 IQR, interquartile range; Max, maximum score; SD, standard deviation. explained the task. All the tests included one practice item 3. Results in order to ensure that the participants comprehended the task. Once the practice item was performed correctly, the The mean correct responses and other descriptive statistics experimental items were presented and the responses were of the control and experimental groups in the four tasks appear collected manually. in Table 3. The individual scores of the PWA and cutoff points appear in Table 4, as well as results for other subtests that assessed relevant skills, namely, semantic memory, and word repetition and comprehension. 2.4. Statistical analysis Descriptive statistics were presented as mean, standard deviation, median, range and interquartile range. Distribution 3.1. Visual short-term memory for normality was assessed with the Shapiro–Wilk test. The Mann–Whitney-Wilcoxon test was used to compare Both groups obtained high scores on the visual STM task, the distributions of the two groups given the non-normal but the control participants’ mean of correct responses (M = distribution of the data. Since the sample size for the aphasic 9.69, SD = 1.15) was slightly higher than the aphasics’ (M = group was small, a fixed effects model for binomial data was 9.08, SD = 1.51). The responses of both groups were not performed to determine whether there was a significant effect normally distributed (WControl = 0.29, p < 0.001; WAphasic = of group, to model the probability of success, and to calculate 0.68, p = 0.001), and their distributions differed significantly, the odds ratio and 95% confidence intervals. Cutoff values were U = 437, p = 0.016. The fixed-effects model revealed a also calculated for each subtest in order to discriminate impaired significant main effect of group, F = 9.47, p = 0.003, and and unimpaired performance. The cutoff points corresponded indicated that the estimated success rate for the control group to the score that the 95% of control participants exceeded, was of 96.9% (95% CI [95.5, 97.9]), and of 90.8% (95% CI [84.1, following the methodology used in other versions of the CAT 94.9]) for PWA. According to the parameters of the model, (Swinburn et al., 2004; Zakariás and Lukács, 2021). Scores the probability of success of the control participants was three below the cutoff represent impaired performance. A logistics times higher than the aphasics’ (OR = 3.26, 95% CI [1.5, regression analysis was conducted to estimate and compare the 6.64]). This difference was statistically significant, t = 3.08, percentages of participants at or above the cutoff point in both p = 0.003. groups. Finally, Pearson and Spearman correlation coefficients If we look at the individual responses as shown in Table 4, were used to measure lineal and monotonic associations nine out of the twelve PWA scored at or above the cuttoff between the four tasks. The correlation coefficients were value. Two of the three participants who did not obtained corrected using the Bonferroni correction method. Statistical a very close score of 8/10, while only one patient scored significance was set at p < 0.05. The statistical analysis very low (5). However, the difference between both groups’ was performed using SAS software, version 9.4 (SAS Institute percentages of participants that reached the cutoff point was Inc., USA). significant (Fisher’s exact test = 8.23, p = 0.025). In Frontiers in Psychology 07 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 TABLE 4 Individual correct responses of subjects with aphasia by task. Subtest Cutoff Subjects with aphasia 1 2 3 4 5 6 7 8 9 10 11 12 Arithmetic 5/6 4 4 1 5 3 1 5 5 5 4 6 6 Semantic memory 9/10 10 9 7 10 9 7 10 10 10 10 10 10 Visual STM 9/10 9 10 5 10 10 8 10 9 10 10 8 10 Verbal STM Digit span 4/7 6 4 3 4 4 6 3 4 4 2 4 4 Listening span 6/6 6 6 4 3 6 6 3 5 4 4 4 6 Word repetition 0–1 scale 16/16 16 15 10 16 16 15 14 16 15 15 16 16 0–2 scale 31/32 32 30 20 32 32 28 22 32 30 29 31 32 Word comprehension 0–1 scale 14/15 12 15 9 15 14 12 14 15 14 15 15 15 0–2 scale 28/30 24 30 17 29 25 20 27 29 27 30 28 30 Sentence comprehension 0–1 scale 17/18 17 12 7 14 13 14 14 15 13 12 17 16 0–2 scale 32/36 33 19 12 27 24 26 16 22 23 15 24 25 addition, the estimated percentages of passing the cutoff point 3.2.2. Sentence listening span of control and PWA was of 96.4% (95% CI [89.4, 98.9]) and The aphasic group obtained a mean listening span of 4.75 75% (95% CI [44.4, 91.9]), respectively. The difference was (SD = 1.22), which was lower than the control group’s mean significant, t = 2.47, p = 0.015, the odds of the control of 5.99 (SD = 0.11). The distribution of the data was not group being nine times higher than the aphasics’ (95% CI normal (WControl = 0.09, p < 0.001; WAphasic = 0.82, [1.54, 52.57]). p = 0.015), and differed between the groups, S = 291, p < 0.001. Moreover, less than half of the subjects with aphasia (5/12) reached the cutoff point in this subtest, which differed significantly from the percentage of control subjects that exceeded it (Fisher’s exact test = 44.88, p < 0.001). According 3.2. Verbal short-term memory to the logistic regression analysis, there was a main effect of group (F = 16.69, p < 0.001) with control subjects being 116 3.2.1. Digit span times more likely to score at or above the cutoff point than the On average, the PWA obtained a lower digit span (M = 4, PWA (t = 4.09, p < 0.001; OR = 116.2, 95% CI [11.52, SD = 1.13) than the control subjects (M = 5.99, SD = 1.11). 1172]). The normality test showed that the responses were not normally distributed (WControl = 0.81, p < 0.001; WAphasic = 0.84, p = 0.025). The difference between the two groups’ distributions was significant, S = 313.5, p < 0.001. And despite the fact 3.3. Sentence comprehension that nine subjects with aphasia obtained a score at or above 4, the cutoff point, the percentage of individuals that exceeded it The mean correct responses of the subjects with aphasia differed significantly from the controls’ (Fisher’s exact test = was lower than the controls’: 13.67 (SD = 2.71) and 17.61 14.91, p = 0.005). Also, the generalized linear model revealed (SD = 0.68) on the 0–1 scale scoring and 22.17 (SD = 5.83) that there was an effect of group if we considered the cutoff point, and 34.39 (SD = 1.87) on the 0–2 scale scoring, respectively. F = 7.57, p = 0.007, and that the estimated percentages of The differences between groups were significant: S = 114, the aphasic and control groups of reaching it was of 75% (95% p < 0.001 and S = 97, p < 0.001 for scores based on the CI [44.4, 91.9]) and 98.8% (95% CI [91.8, 99.8]), respectively. 0–1 and the 0–2 scales, respectively. With regard to the scores The difference was significant (t = 2.75, p = 0.007); in fact, based on the 0–1 scale, which only takes account of correct the control participants’ probability of reaching the cutoff was and incorrect responses, the results of the fixed effects model twenty-eight times higher than the PWA’s (OR = 27.7, 95% CI revealed a main effect of group, F = 16, p < 0.001. The [2.52, 303.83]). estimated percentage of success of PWA was only of 50% (95% Frontiers in Psychology 08 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 TABLE 5 Pearson correlation coefficients (subjects with aphasia). Visual STM Digit span Listening span Sentence comprehension 0–1 scale 0–2 scale Visual STM −0.05 0.06 0.48 0.30 p = 0.8687 p = 0.8479 p = 0.1179 p = 0.3454 Adj p = 1.0000 Adj p = 1.0000 Adj p = 1.0000 Adj p = 1.0000 Digit span −0.05 0.60 0.51 0.83 p = 0.8687 p = 0.0405 p = 0.0934 p = 0.0008 Adj p = 1.0000 Adj p = 0.4054 Adj p = 0.9336 Adj p = 0.0084 Listening 0.06 0.60 0.22 0.43 span p = 0.8479 p = 0.0405 p = 0.4901 p = 0.1631 Adj p = 1.0000 Adj p = 0.4054 Adj p = 1.0000 Adj p = 1.0000 Sentence comprehension 0–1 scale 0.48 0.51 0.22 0.76 p = 0.1179 p = 0.0934 p = 0.4901 p = 0.0038 Adj p = 1.0000 Adj p = 0.9336 Adj p = 1.0000 Adj p = 0.0381 0–2 scale 0.30 0.83 0.43 0.76 p = 0.3454 p = 0.0008 p = 0.1631 p = 0.0038 Adj p = 1.0000 Adj p = 0.0084 Adj p = 1.0000 Adj p = 0.0381 Adj, adjusted p-values (Bonferroni). CI [24.1, 75.9]), much lower than that of control subjects, 96.4% 3.4. Correlations between subtests (95% CI [89.4, 98.9]). The difference was significant, t = 4, p < 0.001, the odds of success of the control group being In order to establish the relationship between language 27 times higher than the aphasics’ (95% CI [5.26, 138.65]). comprehension and STM deficits in Catalan-speaking subjects In this case, only two PWA reached the cutoff threshold. The with aphasia, correlations between the scorings on the four tasks percentage of individuals who scored at or above the cutoff were calculated (Tables 5, 6). Spearman correlation coefficients point was significantly lower than that of the control participants of 0.69 (p = 0.013) and 0.76 (p < 0.001) were obtained (Fisher’s exact test = 52.04, p < 0.001). The fixed effects model between the two scores of the comprehension subtest for aphasic revealed an effect of group (F = 24.59, p < 0.001), the estimated and control subjects, respectively, indicating a moderate level percentage of exceeding the cutoff being of 16.7% (95% CI [4.1, of association. With regard to the performance of PWA, the 48.2]) and 95.2% (95% CI [87.9, 98.2]) for subjects with and score based on the 0–2 scale was strongly associated with their without aphasia, respectively. The difference was significant, t = score on the digit span task [r(10) = 0.85; p < 0.001; see 4.96, p < 0.001, and the odds of success of the control group was Figure 2]. The results of the two verbal STM scores of the 100 times the odds of the experimental group (95% CI [15.82, aphasic group were also moderately correlated, r(10) = 0.62; 632.16]). p = 0.03. After applying the Bonferroni correction test, the If we consider the scoring system based on the 0–2 scale, only only significant association obtained was between the score one participant scored above the cutoff point, which differed of PWA based on the 0–2 scale in the comprehension task significantly from the percentage of control participants that and digit span (Figure 2). Regarding control subjects, the only scored at or above the cutoff point (Fisher’s exact test = 65.42, significant correlation observed was between the two scores of p < 0.001). As previously stated, this scoring system is more the comprehension subtest. sensitive as it takes into account variables such as delayed These results were in line with the Pearson correlation response, request for repetition and self-correction. Not only a analysis (Tables 7, 8): both scores for the comprehension task main effect of group was observed, F = 22.57, p < 0.001, were positively associated in the aphasic [r(10) = 0.76; p = but the magnitude of the difference between the control and 0.004] and control [r(82) = 0.85; p < 0.001] groups. Like aphasic group was greater than the one observed on the 0– before, the digit span of PWA was correlated with their score 1 scale: OR = 297, 95% CI [27.49, 3208.4]; t = 4.75, p < based on the 0–2 scale in the comprehension task [r(10) = 0.001. 0.83; p < 0.001; see Figure 2] and their listening span Frontiers in Psychology 09 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 TABLE 6 Pearson correlation coefficients (control subjects). Visual STM Digit span Listening span Sentence comprehension 0–1 scale 0–2 scale Visual STM 0.02 0.07 −0.05 −0.02 p = 0.8860 p = 0.5494 p = 0.6534 p = 0.8880 Adj p = 1.0000 Adj p = 1.0000 Adj p = 1.0000 Adj p = 1.0000 Digit span 0.02 0.20 0.20 0.27 p = 0.8860 p = 0.0724 p = 0.0662 p = 0.0116 Adj p = 1.0000 Adj p = 0.7236 Adj p = 0.6616 Adj p = 0.1160 Listening 0.07 0.20 0.10 0.26 span p = 0.5494 p = 0.0724 p = 0.3701 p = 0.0171 Adj p = 1.0000 Adj p = 0.7236 Adj p = 1.0000 Adj p = 0.1714 Sentence comprehension 0–1 scale −0.05 0.20 0.10 0.85 p = 0.6534 p = 0.0662 p = 0.3701 p < 0.001 Adj p = 1.0000 Adj p = 0.6616 Adj p = 1.0000 Adj p < 0.001 0–2 scale −0.02 0.27 0.26 0.85 p = 0.8880 p = 0.0116 p = 0.0171 p < 0.001 Adj p = 1.0000 Adj p = 0.1160 Adj p = 0.1714 Adj p < 0.001 Adj, adjusted p-values (Bonferroni). FIGURE 2 Relationship between the digit span (x) and scores based on the 0-2 scale on the comprehension task (y) of control subjects (open circles) and PWA (black-filled circles). [r(10) = 0.6; p = 0.04]. In addition, two weak associations 4. Discussion were observed in the control group responses between their score based on the 0–2 scale in the comprehension task and One of the goals of the present study was to examine their digit span [r(82) = 0.27; p = 0.012], on the one visual and verbal STM and sentence comprehension in Catalan hand, and their listening span [r(82) = 0.26; p = 0.017] aphasia. The aphasic performance was significantly worse than on the other. After applying the Bonferroni correction test the performance of the control group on all tasks, but the to the Pearson correlation analysis, significant associations magnitude of the difference varied remarkably across subtests. In were observed between the two scores of the comprehension addition, there were considerable individual differences among task in both groups, and between the score of PWA based PWA, specially on STM tasks. We also investigated whether on the 0–2 scale in the comprehension task and their digit there were any significant correlations between STM and span (Figure 2). language comprehension tasks. The results showed that there Frontiers in Psychology 10 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 TABLE 7 Spearman correlation coefficients (subjects with aphasia). Visual STM Digit span Listening span Sentence comprehension 0-1 scale 0-2 scale Visual STM −0.25 −0.10 −0.20 −0.03 p = 0.4332 p = 0.7632 p = 0.5285 p = 0.9373 Adj p = 1.0000 Adj p = 1.0000 Adj p = 1.0000 Adj p = 1.0000 Digit span −0.25 0.62 0.56 0.85 p = 0.4332 p = 0.0308 p = 0.0556 p = 0.0005 Adj p = 1.0000 Adj p = 0.3078 Adj p = 0.5560 Adj p = 0.0050 Listening −0.10 0.62 0.15 0.36 span p = 0.7632 p = 0.0308 p = 0.6460 p = 0.2533 Adj p = 1.0000 Adj p = 0.3078 Adj p = 1.0000 Adj p = 1.0000 Sentence comprehension 0–1 scale −0.20 0.56 0.15 0.69 p = 0.5285 p = 0.0556 p = 0.6460 p = 0.0134 Adj p = 1.0000 Adj p = 0.5560 Adj p = 1.0000 Adj p = 0.1339 0–2 scale −0.03 0.85 0.36 0.69 p = 0.9373 p = 0.0005 p = 0.2533 p = 0.0134 Adj p = 1.0000 Adj p = 0.0050 Adj p = 1.0000 Adj p = 0.1339 Adj, adjusted p-values (Bonferroni). TABLE 8 Spearman correlation coefficients (control subjects). Visual STM Digit span Listening span Sentence comprehension 0–1 scale 0–2 scale Visual STM 0.10 0.26 0.10 0.10 p = 0.3844 p = 0.0182 p = 0.3857 p = 0.3815 Adj p = 1.0000 Adj p = 0.1824 Adj p = 1.0000 Adj p = 1.0000 Digit span 0.10 0.17 0.15 0.26 p = 0.3844 p = 0.1215 p = 0.1684 p = 0.0166 Adj p = 1.0000 Adj p = 1.0000 Adj p = 1.0000 Adj p = 0.1656 Listening 0.26 0.17 0.15 0.19 span p = 0.0182 p = 0.1215 p = 0.1824 p = 0.0889 Adj p = 0.1824 Adj p = 1.0000 Adj p = 1.0000 Adj p = 0.8891 Sentence comprehension 0–1 scale 0.10 0.15 0.15 0.76 p = 0.3857 p = 0.1215 p = 0.1824 p < 0.001 Adj p = 1.0000 Adj p = 1.0000 Adj p = 1.0000 Adj p < 0.001 0–2 scale 0.10 0.26 0.19 0.76 p = 0.3815 p = 0.0166 p = 0.0889 p < 0.001 Adj p = 1.0000 Adj p = 0.1656 Adj p = 0.8891 Adj p < 0.001 Adj, adjusted p-values (Bonferroni). were no significant correlations between STM and sentence impairments observed in the four tasks are due to a single- comprehension tasks. In view of the results we argue that system deficit, given that no significant associations were found our findings are inconsistent with the assumption that the between STM and comprehension measures. Frontiers in Psychology 11 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 4.1. Short-term memory deficits An anonymous reviewer pointed out that verbal spans may have reflected different types of production deficits, Our results are in line with the literature reviewed above, grammatical deficits in particular. We analyzed the sentences according to which visual and verbal STM is often impaired produced by PWA in this task, and found that PWA made in aphasia, but subject to individual variability (Gonzalez et al., a total of 28 errors involving content words: 24 omissions 2020). Interestingly, the performance of PWA on the visual STM and 4 substitutions of content words. All the substitutions task was very high despite being significantly lower than the except one were synonyms or semantically related words controls’ and, as already pointed out, most participants reached (e.g., llegir el conte “to read the story” instead of explicar el the cutoff point. Other studies have already reported mild or conte “to tell the story”). In two cases, the error consisted no impairment in visuospatial STM (e.g., Seniów et al., 2009; in repeating the sentence in a different word order. Except Potagas et al., 2011). for one case in which the participant produced a sentence In contrast, the results of the aphasic group on the verbal with an infinitive as the main verb, as well as unfinished STM subtests were much lower and, if we look at the individual sentences (El gat... “The cat...” instead of El gat atrapa el scores, fewer participants scored at or above the cutoff point ratolí “The cat catches the mouse”), the resulting utterances on the sentence repetition task. In fact, the probability of PWA were grammatical (e.g., La dona tanca la porta “The woman of scoring at or above the cutoff point decreased from 9 to closes the door” instead of La dona marxa i tanca la 28 and 116 times less in visual, digit and sentence STM tasks, porta “The woman leaves and closes the door”). The PWA respectively. omitted and substituted 17 and 9 grammatical morphemes, The difference in performance between visual and verbal respectively, and one patient produced one extra preposition, STM tasks has also been found in studies that assessed but these omissions and substitutions were ancillary of the visuospatial and verbal STM through other measures (Seniów changes in content words, since they did not result in et al., 2009; Potagas et al., 2011). In our study, no significant ungrammaticality. Therefore, even if function words were correlations between visual and verbal STM subtests were found. not taken into consideration for the purpose of evaluating These findings rule out the possibility that the deficit observed short-term memory, it does not seem that the 12 subjects in STM tasks is due to a disruption of a common memory with aphasia that participated in the study produced ill- mechanism, more specifically the central executive, and rather formed sentences in this particular task. Finally, most mistakes suggest a selective impairment of the phonological loop. It could affected longer sentences, which suggests problems with PWA’s also be argued that the difficulties shown by the PWA in verbal memory capacity rather than agrammatism or difficulties with span tasks are due to a deficit in repetition, a function that syntactically complex sentences, as Caplan and Waters (1999) can be selectively impaired in aphasia (Geschwind, 1970). Yet, argued. most of the subjects that participated in our study presented very high scores on a task that assessed their ability to repeat simple words (Table 4), and no significant correlations between 4.2. Sentence comprehension deficits the scores on this task and those on the STM tasks were observed. The only exception is subject 2, whose mistakes The aphasic performance on the sentence comprehension involved mainly low-frequency words (five out of six errors) task was significantly worse than the controls’, which is in and words with more than two syllables (four out of six line with the results on the other versions of the CAT (see errors). Table 9) and the other studies reviewed above. This was The scores on the two verbal STM subtests did correlate actually the task where the least participants scored at or significantly, which reflects the fact that both tasks evaluate the above the cutoff point, this being 100 times less likely for same subtype of memory but, as already mentioned, fewer PWA PWA than for controls. In fact, their performance was more reached the cutoff threshold on the sentence repetition task consistent than the results on the other tasks despite the than on the digit span subtest. Previous studies reported similar heterogeneity of the sample. The deficit observed in this subtest results (Martin and Ayala, 2004; Lang and Quitz, 2012). The cannot be due to an impairment in word comprehension possibility that the poor performance on the digit repetition task (Baddeley, 2003), as the results of the aphasic group on a may be due to a problem with numerical skills can be ruled out word-to-picture matching task revealed (Table 4). Also, no based on the PWA’s results on the arithmetic task (see Table 4). significant associations were found between word and sentence The lower performance on the listening span subtest could be comprehension. attributed to the higher complexity of sentence repetition as The sentence comprehension task of the CAT does not a task, since it requires both production and comprehension aim at evaluating the comprehension of specific syntactic skills. Based on the results on the word repetition task, the structures (Swinburn et al., 2004), yet it includes a wide possibility of a word length effect (Baddeley, 2007) can be range of constructions. If we look at the error distribution, ruled out. the PWA made a total of 52 mistakes (see Table 10) that Frontiers in Psychology 12 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 TABLE 9 Mean scores by subjects with aphasia in other versions of the CAT. Subtest Max Language n Mean Visual STM 10 Arabic (Abou El-Ella et al., 2013) 100 7.57 Croatian (Kuvač Kraljevića et al., 2020) 114 8.82 English (Swinburn et al., 2004) 194 8.81 Hungarian (Zakariás and Lukács, 2021) 99 8.24 Turkish (Maviş et al., 2021) 20 8.29 Digit span 7 Arabic (Abou El-Ella et al., 2013) 100 3.86 Croatian (Kuvač Kraljevića et al., 2020) 114 4.14 English (Swinburn et al., 2004) 195 3.94 Hungarian (Zakariás and Lukács, 2021) 90 3.35 Turkish (Maviş et al., 2021) 20 4.8 Listening span 6 Arabic (Abou El-Ella et al., 2013) 100 4.68 Croatian (Kuvač Kraljevića et al., 2020) 114 3.5 English (Swinburn et al., 2004) 195 3.21 Hungarian (Zakariás and Lukács, 2021) 87 3.39 Turkish (Maviş et al., 2021) 20 3.3 Sentece comprehension 32 Arabic (Abou El-Ella et al., 2013) 100 22.39 Croatian (Kuvač Kraljevića et al., 2020) 114 21.15 English (Swinburn et al., 2004) 195 18.73 Hungarian (Zakariás and Lukács, 2021) 95 19.92 Turkish (Maviş et al., 2021) 20 16.35 Max, maximum score; n, number of subjects. TABLE 10 Errors by sentence type in the comprehension subtest passives, object relatives or clitic left dislocations (among others, (subjects with aphasia). Caramazza and Zurif, 1976; Hickok et al., 1993; Grodzinsky, Sentence type Errors/Items % 2000; Luzzatti et al., 2001; Friedmann, 2008; Salmons and Gavarró, 2013; Varlokosta et al., 2014; Adelt et al., 2017; Terzi Actives with one argument 0/36 0 and Nanousi, 2018; Garraffa and Fyndanis, 2020). Moreover, Actives with two arguments 13/60 21.7 the fact that the comprehension task of the CAT, despite Clitic left dislocations 7/24 29.2 being a general comprehension task, is sensitive to the specific Passives 11/24 45.8 linguistic deficits suggests that it is an efficient diagnostic tool Relative clauses 2/12 16.7 for aphasia. Sentences with PPs 19/60 31.7 We also took into consideration the results on the comprehension task based on the two scoring systems which, as expected, were correlated. The scoring system based on the 0–2 scale provides additional information as it penalizes mainly involved semantically reversible sentences with non- response delays, repetition requests and self-corrections, and the canonical word orders, like passives or clitic left dislocations individual scores were low. These low scores probably reflected (2b), and with PPs such as The glass is under the plate the greater complexity of the task, given that it demanded which corresponded to the 34.6 and 36.5% of the total errors, not only sentence comprehension, but also spatial search, respectively. On the other hand, fewer mistakes were found scene analysis, word retrieval and sentence-to-picture matching with irreversible (2a) and reversible canonical sentences (The (Grodzinsky, 2010; Caplan et al., 2013). The cutoff point based postwoman is chasing the cook), which only represented 5.8 on the controls’ scores based on the 0–2 scale favors this view, and 19.2% of all errors, respectively, or on irreversible object since their results in sentence comprehension were very poor relatives (3.8%). These findings suggest that the problems to compared to the other tasks (Table 4). Interestingly, Sung et al. understand the sentences arose when their interpretation relied (2018) carried out a study on the production abilities of a group on particular syntactic operations. There is actually extensive of Korean-speaking aphasics, and the results showed that task crosslinguistic evidence that PWA present impairments in type related to individual WM capacity, but not to sentence type comprehension that affect specific syntactic structures like (active vs. passive). Frontiers in Psychology 13 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 4.3. The relationship between short-term of the comprehension subtest. In fact, some of the studies that memory and sentence comprehension have reported significant correlations between memory and sentence comprehension used tasks that could have been more The present study also aimed at testing the hypothesis that sensitive to STM deficits. This is the case of studies that used the difficulties of PWA in STM and sentence comprehension complex span tasks to assess WM, which are cognitively more tasks are due to a common cause, whether it be an attention demanding (Ivanova et al., 2017), or sentence comprehension (McNeil et al., 2011), memory (Caplan and Waters, 1999; Aboitiz tasks that involved items that gradually increased in length et al., 2006) or language deficit (Christensen and Wright, 2010). requiring a greater memory load and, hence, relied heavily on If that was the case, we would expect strong correlations between short-term memory. To illustrate, Choinski et al. (2020) used STM and comprehension subtests. However, the observation both the Token Test (De Renzi and Faglioni, 1978) and a that no significant associations were found between the scores sentence comprehension task with 30 PWA, and they obtained on these subtests rules out this possibility and suggests that a lower scores in the first task. These findings are in line with single-system deficit cannot explain the impairments observed Caplan and Waters (1999)’s hypothesis, since the scores based on in these tasks. Rather, we hypothesize that the disrupted tasks the 0–2 scale could actually reflect post-interpretive processes, reflect deficits in different cognitive systems, namely, short-term such as remembering and using the meaning of the sentence memory and language. to perform the task of analyzing the images and pointing to Other studies have reported significant associations between the correct one. According to these authors, a contrast between forward digit and listening spans and sentence comprehension an active and a passive sentences involves mainly interpretive tasks (among others, Sung et al., 2009; Lee and Pyun, processes, while contrasts like the ones included in the Token 2014; Choinski et al., 2020), interpreted as evidence that Test rather reflect post-interpretive processing. a common underlying mechanism was affected, usually a Our findings are therefore compatible with the assumption component of the STM (see Wright and Fergadiotis, 2012 that the primary deficit in aphasia is linguistic; this in itself does for a review). This view also finds support from the fact not exclude the presence of other cognitive impairments or less that short-term memory is needed in sentence comprehension direct associations between STM and sentence comprehension and, hence, that a deficit in this domain probably impacts (Caplan and Waters, 1999; Varkanitsa and Caplan, 2018), in on comprehension (Baddeley, 2003). Under this view, it line with the SSIR hypothesis. This would account for the could be argued that the impairments observed in sentence fact that, despite the heterogeneity of the sample, the deficits comprehension were triggered by a memory disorder, given that observed in sentence comprehension were more consistent than sentences with syntactic dependencies require greater memory the ones observed in STM tasks. In fact, as argued before, there and impose higher processing demands (Caplan and Waters, is wide evidence that the pattern of performance of aphasics 1999). However, this cannot account for the results from in sentence comprehension tasks is robust across languages behavioral studies on the comprehension of other types of (Drai and Grodzinsky, 2006a,b). In contrast, the deficits in STM syntactic dependencies that, despite requiring STM, are well- tasks were subject to individual variability as several participants comprehended by PWA (Santi and Grodzinsky, 2007). performed within the normal range, specially on the visual and Hence, even if memory and language measures correlated, a digit span tasks (e.g., participants 1, 3, 6, and 10). Other studies STM disorder could not explain the pattern of syntactic deficits have also observed dissociations among participants in non- observed in the comprehension tasks in the present study and in linguistic cognitive measures (Seniów et al., 2009; Potagas et al., previous literature (see Grodzinsky, 2000 for a review). 2011; Caplan et al., 2013; Lee and Pyun, 2014; Gonzalez et al., While admittedly it is difficult to assess different cognitive 2020). systems in isolation and to identify the impact of memory in In our view, the conflicting results reported in some of sentence comprehension tasks, we believe that in the present the literature, as well as the discrepancies with regard to the study the impact of STM disorders was better captured by correlation between memory and comprehension measures in the scoring system based on the 0–2 scale. In fact, significant aphasia, favor the idea that aphasia does not always entail correlations were found between the score on the sentence memory disorders, and that memory deficits alone cannot comprehension task based on the 0–2 scale and the digit explain the linguistic impairment, as others have already and listening spans. Hence, even though higher spans did argued (Murray, 2012; Fonseca et al., 2016; Marinelli et al., not translate into higher accuracy rates, the 0–2 scoring 2017). The non-linguistic cognitive disorders that often co- system reflected greater difficulties with the comprehension task occur with aphasia could be the result of different factors correlating with lower spans (Figure 2). This, however, does that have already been pointed out in the literature, including not hold for all participants (e.g., 1, 7, and 10) which, in turn, the presence of brain damage (Wright and Fergadiotis, 2012) highlights the variability of STM deficits in aphasia. As we have and other medical conditions like dementia or depression (El argued before, we believe this is due to the higher task demands Hachioui et al., 2014). This is consistent with the literature Frontiers in Psychology 14 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 on cognitive abilities that states that brain-damaged patients for that purpose (Salis et al., 2018), as it aims at evaluating present different deficits regardless of the hemisphere damaged both verbal and nonverbal cognitive skills in a relatively or the presence of aphasia (see Fonseca et al., 2016 for short administration time, which makes it suitable for clinical a review), as well as with the observation that aphasia use. In the present study we presented four subtests of the severity is often related to the STM capacity (Gonzalez Catalan version of the test (Salmons et al., 2021) that evaluate et al., 2020) as more severe aphasias often involve larger visual and verbal STM, and sentence comprehension, and lesions. we have shown that it can be a useful tool to evaluate One of the arguments used to argue that a short-term Catalan-speaking subjects with aphasia. Yet, further research memory impairment underlies the comprehension deficits is needed to enlarge the PWA sample of the present study. observed in aphasia is that both functions have been located Also, this study does not allow us to investigate whether in the same brain areas (Hickok and Poeppel, 2000; Aboitiz different aphasia types correlate with different patterns of et al., 2006; Choinski et al., 2020), including the inferior comprehension and STM impairment, given that the CAT does frontal gyrus (IFG). Neuroanatomical data from aphasic and not distinguish among aphasia types; furthermore we were healthy subjects support the co-occurrence of STM and lacking in information about the participants in our sample. comprehension disorders in aphasia. However, as argued Similarly, the CAT is a tool developed to be used in clinical by Santi and Grodzinsky (2007), these deficits reflect the practice, and the sentence comprehension task does not allow multimodal nature of the brain damaged areas rather than a to investigate whether there are significant correlations between working memory deficit. Also, general cognitive impairments the comprehension of different syntactic structures and STM. have been claimed to explain linguistic deficits in several Therefore, establishing links, on the one hand, between aphasia clinical conditions such as schizophrenia (see Kuperberg, 2010 types, and comprehension and STM and, on the other hand, for a review), Down syndrome (Baddeley and Jarrold, 2007) between syntactic structures and STM deficits, remains a topic or primary progressive aphasia (Gorno-Tempini et al., 2004). for future research. Yet, the relationship between linguistic and other cognitive abilities may vary across clinical populations. Little et al. (2019), for example, compared the performance on verbal and 5. Conclusion nonverbal cognition tasks of two groups of twenty subjects The aim of the study was to investigate visual and verbal with aphasia and thirty subjects with schizophrenia. The short-term memory and sentence comprehension in Catalan- results showed that while both groups presented significant speaking subjects with aphasia and to compare them with linguistic deficits, a significant nonverbal cognitive impairment subjects without brain damage. Within the limits of our only occurred in schizophrenia. An association between verbal sample, the results showed that the aphasic performance and nonverbal cognition tests was only observed in the was significantly worse than the controls’ on the four tasks schizophrenia group, in line with previous studies (Kerns, 2007). and, hence, that subjects with aphasia had difficulties in This also implies that, while there is clearly an association short-term memory and comprehension. Yet, the logistic between verbal and nonverbal cognitive skills, it is not a direct regression analysis revealed that the magnitude of the differences one. between groups varied remarkably across subtests, and that Taken together this lead us to the conclusion that non- visual short-term memory was much better preserved that linguistic short-term memory disorders often coexist with verbal short-term memory. Moreover, our results showed that language deficits in aphasia. Yet, the present study and previous there were no significant correlations between short-term research show that non-linguistic cognitive deficits are subject memory and language comprehension, which rules out the to wide individual variability while linguistic deficits remain hypothesis that the deficits observed are due to a common constant. This emphasizes the need to assess people with aphasia underlying mechanism. We argued that the deficit in aphasia exhaustively in order to precisely describe each patient’s profile is linguistic in nature, though short-term memory disorders and plan an adequate intervention program (see van Mourik can also occur in some individuals. In fact, there were great et al., 1992; Hinckley et al., 2001; Helm-Estabrooks, 2002; individual differences among participants with aphasia, which Seniów et al., 2009; Murray, 2012; Kuzmina and Weekes, 2017; emphasize the importance of a comprehensive assessment and, Marinelli et al., 2017; Fonseca et al., 2018; Zakariás et al., hence, the use of diagnostic tools like the CAT in clinical 2018). practice. There are some standardized tests in different languages that include both verbal and nonverbal cognitive tasks and are specifically designed to evaluate individuals with aphasia, Data availability statement such as the Cognitive Linguistic Quick Test (Helm-Estabrooks, 2001) or the Comprehensive Aphasia Test (Swinburn et al., The datasets presented in this study can be 2004) in English. The CAT is one of the most used tools found in online repositories. The names of the Frontiers in Psychology 15 frontiersin.org Salmons et al. 10.3389/fpsyg.2022.880398 repository/repositories and accession number(s) can be from the Servei d’Estadística Aplicada of the UAB for the found at: https://doi.org/10.5565/ddd.uab.cat/255717. statistical analysis. We are grateful to the reviewers of Frontiers for their comments. Any remaining errors are our own. Ethics statement The studies involving human participants were reviewed Conflict of interest and approved by UAB Ethics Committee (CEEAH 5656). The patients/participants provided their written informed consent to The authors declare that the research was conducted in participate in this study. Written informed consent was obtained the absence of any commercial or financial relationships from the individual(s) for the publication of any potentially that could be construed as a potential conflict identifiable images or data included in this article. of interest. Author contributions Publisher’s note AG and IS contributed to the conception and design of the All claims expressed in this article are solely those of the study. HM-S and IS organized the database. IS wrote the first authors and do not necessarily represent those of their affiliated draft of the manuscript. All authors contributed to manuscript organizations, or those of the publisher, the editors and the revision, read, and approved the submitted version. reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. Acknowledgments Special thanks to all participants, as well as the Hospital Supplementary material Sant Rafael, and the Escola de Patologia del Llenguatge de l’Hospital de Sant Pau and the Grup de Suport Neuropsicològic. The Supplementary Material for this article can be Thanks also to Duna Ninyerola and Mireia Sangenís for found online at: https://www.frontiersin.org/articles/10.3389/ their help in testing participants, and to Ester Boixadera fpsyg.2022.880398/full#supplementary-material References Aboitiz, F., García, R., Brunetti, E., and Bosman, C. (2006). “The origin of Broca’s Benton, A. L., and Joynt, R. J. (1960). Early descriptions of aphasia. Arch. Neurol. area and its connections from an ancestral working memory network,” in Broca’s 3, 205–222. doi: 10.1001/archneur.1960.00450020085012 Region, eds Y. Grodzinsky and K. 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