1. IntroductionThe Token Test (TT) [1,2,3] is widely used test to assess auditory comprehension in persons with developmental and acquired disorders affecting language, where the patient is verbally required to provide a gestural response (pointing to or moving plastic tokens) in response to a verbal command. Most versions include 20 tokens with different forms (i.e., rectangles and circles), sizes (i.e., large and small), and colors (i.e., red, blue, green, yellow, and white). During the test, the examiner provides a set of increasingly difficult commands, requiring token identification and/or manipulation. Since its first publication in the early sixties, the use of the TT in clinical practice has rapidly spread and the tool has been translated into more than 40 languages [4].Over the past years, several versions have been proposed, that differ in the number of items, type of stimuli, type of population, and scoring modalities; a digital version is also available [5] and, recently, a version for mobile phones has been proposed [6].Although the TT has been specifically developed to assess auditory language comprehension, its performance involves other cognitive processes, as it often happens with neuropsychological tests. Such processes include verbal short-term memory, working memory, and inhibitory control, that is the ability to ignore distracting and competing lexical information [7]. This is consistent with the hypothesis of the role of verbal short-term memory [8,9], along with executive functions [10,11], in sentence comprehension. Thus, TT versions with several items presenting increasing length and syntactic complexity of the orders are more likely to involve verbal span and working memory.TT is included in widespread batteries for Aphasia, such as the Aachener Aphasia Test, (AAT) [12], originally developed in German and later translated into many other languages, including Italian [13]. The Italian version is composed of five parts. In parts I–IV, the patient is verbally required to identify at first one and then more tokens, identified by a progressively increasing number of features. In part V, the examiner requires the patient to manipulate tokens, by providing verbal commands with a complex syntactic structure. Since the last sections of this TT may require quite a long time, some authors pointed out that the overall score may not truly represent verbal comprehension alone and, therefore, suggested examining the performances for parts I to IV and for part V separately [14,15]. Indeed, using such long versions of TTs could be misleading, considering the requirements over working memory abilities, which are frequently reduced in individuals with aphasia [16,17].Several studies have attempted to assess which functions, other than language abilities, may influence TT performance [18,19,20,21,22,23,24,25] but the results are somewhat conflicting. The crucial role of verbal and non-verbal memory components in TT performance was first reported by Lesser et al. [18]. Namely, a significant correlation between the last section of the TT and the non-verbal measures of the visual and gestural sequencing span was observed, supporting the hypothesis that the TT may overload the auditory–verbal sequencing span in patients with left brain damage [18]. More recently, [23], the relationships between verbal working memory, sentence comprehension, and severity of impairment in aphasic patients with a history of left hemisphere cerebrovascular accidents have been explored. The listening and reading versions of the computerized revised TT that assesses the sentence comprehension and the sentence span task as a measure of the working memory were used: the patients with low compared to high memory capacity, compared to those with high working memory scores, showed a significantly worse performance in the computerized revised TT, particularly in the subtests with syntactically more complex structures [23]. These findings support the view that the working memory’s influence on verbal comprehension is mainly evident when working the memory capacity is taxed by task demands [26,27,28].Other evidence, however, does not support this relationship. For example, in a study conducted on a large sample of veterans with acquired brain lesions, Koenigs et al. [29] observed that patients with damage to the inferior frontal and posterior temporal regions were impaired either on digit span or on language tests. However, regression analyses revealed that the digit span performance was significantly associated only with the tests assessing language production (i.e., Boston Naming Test and WAIS Vocabulary subtest), whereas no association was found with the TT.

Cognitive control has also been linked to receptive language (10) (24). In these last papers the role of inhibitory control, tested by the Stroop test, was evaluated on auditory comprehension in patients with Wernicke’s aphasia. A significant negative correlation was observed; namely, the greater the Stroop interference effect, the lower the TT performance.

Based on these premises, we aimed to investigate which other components besides language comprehension may affect TT performance. To pursue this goal, we studied TT performance in stroke patients with right hemisphere lesion (RHL). Although patients with RHL may experience communicative–linguistic difficulties (in particular, communication disorders such as turn-taking, argument management, and using non-literal language [30,31] and contextually appropriate language and understanding figurative meaning and the social rules of conversation [32,33]), RHL does not seem to involve the lexical–sematic circuits related to the pure linguistic comprehension.Within the context of a large prospective study on predictors of rehabilitation outcomes in patients addressing intensive inpatient post-stroke rehabilitation, the Intensive Rehabilitation Post-Stroke (RIPS) study [34], we verified the association between each of the five TT sub-tests and the ability to maintain and manipulate information in working memory (as tested by forward and backward digit spans, respectively) and with the cognitive areas investigated by Montreal Cognitive Assessment, following Aiello et al. [35] grouping, in a sample of non-aphasic, right hemisphere stroke patients. 3. ResultsOut of the 278 stroke patients who were eligible for the RIPS study, 235 (85%) signed the informed consent and were enrolled. Of these, 37 met the inclusion criteria and were included in this analysis. The participants had a mean age of 73.5 years (SD: 13.9 years, range 41–94 years). Most of the participants were male (n = 23, 62.2%). Twenty-two participants (59.5%) had an ischemic stroke, while 15 (40.5%) had a hemorrhagic stroke. Most of the participants (n = 16) had a lobar lesion (43.2%); 37.8% (n = 14), presented a lesion in subcortical structures. There were seven (18.9%) participants with any other lesion locations. The specifics on the lesion site for individual subjects are reported in the Supplementary Materials. The demographic and clinical characteristics of the sample are presented in Table 1.

The FDS corrected score obtained by participants ranged between 3.5 and 7.9 (mean value of 5.7). The lower scores were obtained in the BDS test where values ranged from 1.8 to 7.1 (mean value 4.0). A performance lower than 5% of the normative sample was observed in 10.8% of the participants for FDS (score not exceeding 4.26) and 8.1% of the participants for BDS (score not exceeding 2.65). The MoCA mean corrected score obtained by participants was 19.5 (SD: 3.8); the higher score was recorded in the orientation area (median score: 5, IQR: 1.7), while the lower score was recorded in the memory area (median score 1.6, IQR: 1.9).

The neuropsychological test scores obtained by the participants are summarized in Table 2.The median number of errors in the TT was 3, ranging from 0 to 25. In particular, 43.2% of participants made less than 3 errors, 29.7% made from 3 to 11 errors, and 27.0% made more than 11 errors, mostly concentrated in parts IV and V. The TT errors by age tertiles are reported in the Supplementary Materials (Table S1). The Spearman’s correlation analysis showed a significant negative correlation between the number of errors performed on the TT and the digit span scores. In particular, the corrected FDS scores had a weak–moderate correlation with the errors recorded in the TT subparts IV and V, with the strongest correlation observed with subpart V (r = −0.408, p = 0.0013). No significant correlation was found between FDS and subparts I–III (r = −0.064 p = 0.712; r = −0.210 p = 0.219; and r = −0.219 p = 0.200, respectively). The corrected BDS scores correlated only with the TT subpart V, (r = −0.371, p = 0.026). Subparts I–IV showed no significant correlation with BDS (r = −0.181 p = 0.290; r = −0.066 p = 0.702; r = −0.296 p = 0.080, and r = 0.010 p = 0.954, respectively (Table 3).The significant moderate negative correlations were found between the score obtained in the executive functioning and orientation domain of the MoCA test and TT errors (subparts V) (r = −0.468, p = 0.007 and r = −0.499, p = 0.003). A correlation was also found between orientation and TT subpart III (r = −0.504, p = 0.002) (Table 4).The TT total error distributions according to the corrected score obtained in FDS and BDS tests are presented in Figure 1.

When the association between the number of TT total errors and the lesion location was investigated, no significant differences were observed (p = 0.485) in the number of errors according to the lesion site. Similarly, no significant difference was found in FDS (p = 0.629) and BDS (p = 0.568) corrected scores between participants with subcortical, lobar, or other lesion locations.

4. Discussion

This study aims to investigate which other cognitive domains, besides auditory–verbal comprehension, may affect performance in a TT. To perform this, we conducted a correlation study to explore the association between the TT performance and extra-linguistic factors (i.e., the ability to maintain and manipulate information in working memory and the global cognitive status) in a group of thirty-seven patients with right hemispheric stroke and without aphasia; these were prospectively recruited within a multicentric observational study. Although it is not possible to completely exclude an influence of the right hemispheric lesions on the verbal production necessary for the execution of the neuropsychological tests, by the choice of these inclusion/exclusion criteria, we aimed at excluding a significant linguistic component to the TT performance, while taking into consideration other non-verbal cognitive aspects that could be affected by a stroke.

In order to exclude aphasic patients, we decided to select right-handed patients with unilateral right brain regions. To prevent the risk of including persons with inverted cortical representation, the aphasia NIHSS score was used to exclude patients with aphasia following right hemisphere stroke. This choice was aimed at focusing on potential pathological performances in the TT, most likely unrelated to verbal comprehension problems.

Our sample included patients with stroke, which occurred within 30 days before the recruitment, of either ischemic or hemorrhagic etiology, by a proportion of either in line with the literature [42,43]. The site of the brain injury was evenly distributed between the subcortical and lobar, with a mild global index of severity at NIHSS. Concerning global cognitive functioning, the average MoCA score corresponded to moderate impairment. In our sample, almost 60% of the patients made two or more errors on the TT. This first result suggests that, in patients with stroke, TT performance can be compromised also by aspects other than aphasia. Some of our patients presented short-term and working memory impairment (a performance lower than 5% of the normative sample, in 10.8% for FDS and 8.1% for BDS). A significant negative correlation between the number of errors performed in the TT subpart IV and V and the digit span scores was found. In particular, the errors performed in subparts IV and V showed a weak–moderate correlation with the FDS score, while BDS correlated only with TT subpart V. Interestingly, only part V correlates both with FDS and BDS. Part V is constituted of long orders, with complex syntactic constructions that need a high span and working memory load. Additionally, part IV is composed of long orders, although without syntax complexity. Coherently, part IV correlates with the FDS, while unexpectedly part IV does not correlate with BDS.In our analysis, we did not observe any difference between the forward and backward span, used as measures of short-term memory and working memory, respectively. This was rather unexpected, since working memory, namely the capacity to simultaneously process verbal information, should be theoretically more related to complex sentence decoding, than the simple maintenance of linguistic information over a short period (verbal span) [44]. However, unlike previous works (e.g., Gajardo-Vidal et al., [45] that included patients tested >3 months and Among the cognitive models of verbal short-term memory, the phonological loop integrated into the working memory model proposed by Baddeley [40] is probably the most influential. The phonological loop is a limited capacity subsystem involved in the temporary store of verbal information controlled by a supervisory system (i.e., the central executive). According to this model, the verbal span represents the passive temporary maintenance of information, whereas working memory refers to both the maintenance and manipulation of information. Although recent studies have further investigated this concept, and using neuroimaging techniques [46,47,48], the original model is still acknowledged within the scientific community. The auditory short-term memory capacity was found to depend on the structural integrity of a posterior region of the superior temporal gyrus and sulcus [49], while a system involving the auditory cortex and projections from higher-order areas, including the hippocampus and frontal cortex, is considered to be crucial for actively maintaining sounds in memory [50]. The specific role that the brain area involved in the temporary maintenance of linguistic information and working memory resource allocation exerts in sentence comprehension is still a matter of debate [28,51].

Concerning the analysis conducted with MoCA groupings, again part V presents a correlation with executive functions and orientation, while part III also correlated with orientation. The executive functions refer to complex higher-order functions and are considered to be linked to frontal cortical–subcortical circuits. They are involved in carrying out all the more complex tasks, including attentive supervision and self-monitoring. Instead, the significant relationship between the orientation area and the more complex TT subtest could be interpreted as an effect of more severe cognitive impairment: patients who fail in orientation MoCA subtests are those with a severe cognitive impairment and that for this reason are the ones who also fail in the TT complex subtests. On the other hand, it is important to remember that MoCA is a screening test, with very short tests for each cognitive function, and for this reason it does not provide a detailed neuropsychological investigation.

Our results suggest that the existence of an association between auditory–verbal span/auditory working memory and TT performance in right-hemisphere stroke patients. Considering that both right and left hemisphere lesions can compromise short-term and working memory [52,53,54], the effect presented in right hemisphere patients might also be present in left-hemisphere-damaged patients. Hence, our results might support the hypothesis that the TT, and when used with aphasic patients, is probably affected not only by linguistic but also by non-linguistic abilities.

However, further considerations are necessary. Not only the cognitive functions are mutually influenced, but also the neuropsychological tests aimed at assessing one specific function are in some measure influenced by other cognitive performances. For example, the digit span includes a linguistic component and attention underlies all other cognitive functions. Each conclusion must therefore be interpreted considering the numerous factors co-involved in the phenomenon observed. Furthermore, the TT Italian normative data do not need correction for age, while in other languages, such as German, a correction for demographic information is required. This could have influenced the cut-off, which is particularly high in the Italian population, in particular for the assessment of older persons.

From a pragmatic, clinical practice perspective, our results point out other factors that may affect performance at the TT. Evaluating a non-aphasic right hemisphere patient with a TT may thus reveal or confirm impairments in the short term and working memory, while, when administering a TT to an aphasic patient, we must consider that the performance could also be affected by working memory components and attention. The clinical reasoning on the pattern of errors in a TT as well as in other neuropsychological tests, and the observation and interpretation of the patient’s behavior during the test administration, may guide the examiner in the analysis of the verbal comprehension disorder and help to adequately weigh the influence of linguistic and extra-linguistic factors, respectively.

This study presents several limitations. First of all, the sample size is numerically restricted. This did not allow further analyses, such as the evaluation of a possible age effect by a further division into groups. Moreover, to assess the cognitive deficits related to the TT’s performance, we used screening tests, which are not as sensitive as a complete neuropsychological evaluation. Finally, a complete and exhaustive assessment of the language skills of patients was also not performed.

On the other hand, the strengths of this study lie in its prospective nature, as well as in the homogeneity of this cohort, in reference to distance from the acute event.

From the clinical perspective, our results emphasize the importance to investigate verbal short-term memory when assessing and treating verbal comprehension disorders, screening for possible deficits and eventually addressing them with appropriate cognitive rehabilitation treatment. Furthermore, our results also suggest that some caution should be adopted in interpreting TT results in aphasic patients. Indeed, TT errors may not highlight an exclusive problem in linguistic decoding, so the potential effect of other extra-linguistic factors must also be taken into account. This would imply that tests that are less dependent on these highlighted cognitive factors should possibly be used to assess verbal comprehension along with the TT.

In fact, the “Aachener Aphasie Test” evaluation battery [12], which comprises the Token test, includes other tests of lexical and morphosyntactic comprehension, and it is important to consider all of them together to provide a clinical diagnosis. Other tests, included in the classical aphasia evaluation batteries, should also be considered along with the TT to fully investigate verbal comprehension and to obtain a complete profile of the communication skills in aphasic patients. Among them, there are the picture indication tasks (e.g., “Boston Diagnostic Aphasia Examination”, Goodglass and Kaplan, [55]; “Western Aphasia Battery”, Risser et al. [56]; “Esame Neuropsicologico per l’Afasia”, Capasso and Miceli, [57]), as well as a more recent test that investigates both the level of syntactic complexity and the memory–attention load required to perform the task (e.g., “Comprendo”, Cecchetto et al. [58]). Indeed, if our results will be confirmed by subsequent research, we should consider the TT as an integrative and non-exclusive evaluation tool for verbal comprehension in aphasic patients. From this perspective, by only considering the possible extra-linguistic influences observed during TT administration and supplementing the evaluation with lexical and grammatical comprehension tests, the clinician will be able to globally interpret verbal comprehension disorders.