Skip to main content
Open AccessReview

Arithmetisches Lernen in neurologischen Patienten

Published Online:https://doi.org/10.1024/2235-0977/a000377

Abstract

Abstract.Background: Numbers are an integral part of our life. Being competent with numbers is crucial for coping with the challenging demands of our modern times. Anyone who lacks basic numerical and calculation skills due to, for example, lower education, developmental disorders or acquired brain damage is socially disadvantaged and destined to remain marginalized. Improvement of basic numerical and calculation skills must therefore be an important goal of cognitive rehabilitation and intervention. Methods: We summarize the most recent studies regarding the rehabilitation of simple calculation deficits in adult neurological patients. Results: Over the last decades, several studies have reported acquired selective deficits in number processing and calculation skills in adult brain-damaged patients. It has also been shown in single case-studies that targeted rehabilitation based on theoretical neuropsychological models may lead to significant improvements of acquired deficits. Discussion: Systematic interventions may be successful in the case of acquired calculation deficits. Improvement of numerical competence in adult patients are possible even in very unfavorable circumstances (e.g., chronic stage, older age, severe deficits). This finding is of high relevance as numbers are essential in our daily life, and deficits in number processing may have a strong impact on a person's every-day autonomy.

Arithmetisches Lernen in neurologischen Patienten

Zusammenfassung.Hintergrund: Kompetenz im Umgang mit Zahlen ist wesentlich, um den Anforderungen unserer modernen Zeit gewachsen zu sein. Jeder, der Schwierigkeiten mit Zahlen und einfachen Rechenfertigkeiten hat, zum Beispiel wegen niederer Bildung, Entwicklungsstörung oder Hirnschädigung, ist im sozialen Leben benachteiligt und bleibt ausgegrenzt. Die Verbesserung der grundlegenden numerischen Fertigkeiten und des Rechnens muss daher ein wichtiges Ziel kognitiver Rehabilitation sein. Methode: Wir fassen die neuesten Studien zusammen, die sich mit der Rehabilitation von einfachen Rechendefiziten bei erwachsenen neurologischen Patienten beschäftigen. Ergebnisse: Mehrere Studien haben erworbene selektive Defizite in der Zahlenverarbeitung und in den Rechenfertigkeiten erwachsener Patienten nach Hirnschädigung berichtet. Es wurde in Einzelfallstudien gezeigt, dass gezielte Rehabilitation, die auf theoretischen neuropsychologischen Modellen beruht, zu signifikanten Verbesserungen der erworbenen Störungen führen kann. Diskussion: Systematische Interventionen können im Fall von erworbenen Rechenstörungen erfolgreich sein. Die Verbesserung numerischer Kompetenz bei erwachsenen Patienten ist auch unter ungünstigen Umständen möglich (z.B. chronisches Stadium, fortgeschrittenes Alter, schwere Störung). Dieses Ergebnis ist höchst relevant, da Zahlen eine essentielle Rolle in unserem Alltagsleben spielen und Störungen der Zahlenverarbeitung stark die Autonomie im Alltag beeinträchtigen können.

Introduction

The number processing and calculation system

Humans have developed different “tools” for the daily use of the number processing and calculation system. The most basic tool is the representation of numbers in a specific code such as Arabic (5), Roman (V), phonological (/five/), alphabetic (five), etc. This tool is needed for tasks such as counting. An important aspect of using codes is the transformation (i.e. “transcoding”) from one code to another. Transcoding is a skill required by many numerical tasks. For example, reading Arabic numerals aloud requires converting an Arabic code into a “spoken” phonological code. Calculation requires also the use of more complex tools such as arithmetic signs (e.g., +, −, ×, :, = ), arithmetic facts (e.g., 6 × 3 = 18, 6 + 2 = 8, 6 − 3 = 3), rules (e.g., 3 × 0 = 0, 3 × 1 = 3), procedures (multi-digit addition, subtraction, multiplication, and division problems with carrying and borrowing procedures) or principles (e.g., commutativity principle: 5 × 6 = 6 × 5). As shown by many neuropsychological studies, the use of these tools requires different skills, which can be selectively disrupted or spared in conditions that go under the generic name of acalculia. The high degree of modularity of the number processing and calculation system is perhaps the main reason why the rehabilitation of number competences is very difficult. Indeed, rehabilitating one numerical skill does not necessarily imply a positive effect on other skills.

The number processing and calculation system can be described from different points of view, that is, according to different theoretical models. These models are useful not only to understand how the brain/mind processes and uses numbers, but also to identify which components of the system are no longer working in a patient. They can also help in the development of rehabilitation strategies and in measuring the treatment effects. Here, we briefly summarize the main hypotheses underlying two of the most influential theoretical models on number cognition. In particular, we highlight assumptions on calculation, as this is the focus of the intervention studies presented below (for a review on number transcoding and its rehabilitation, e.g., Willmes, 2008). Each of these two models has been extended in subsequent studies: for the sake of simplicity, these extensions are considered here as variants or additions to the main models. The first model is that of McCloskey and colleagues (McCloskey, 1992; McCloskey, Caramazza & Basili, 1985). It emphasizes the use of numbers in various codes and is purely cognitive, i.e. it does not make any reference to anatomy. The second model is that of Dehaene and Cohen (Dehaene, 1992; Dehaene, Piazza, Pinel & Cohen, 2003; Dehaene & Cohen, 1995, 1997) and is commonly known as the “Triple Code” model. This model makes assumptions about the anatomical basis of each of its components.

In McCloskey's model (McCloskey, 1992; McCloskey et al., 1985), a central semantic system is accessed during all numerical and calculation processes, independently from the input (and output) format of the numbers involved (Fig. 1). According to this model, all number formats (spoken number words, written number words, Arabic digits) are converted into abstract representations, which specify the magnitude of the number. These abstract representations serve as input and output for the calculation system (see below). The transformation (or “transcoding”) from one code to another as well as calculation necessarily occurs through the central semantic system (for “asemantic” points of view, see Cipolotti & Butterworth, 1995; Dehaene, 1992; Deloche & Seron, 1982).

Figure 1 Schematic representation of the McCloskey et al.’s (1985) model.

In addition to number processing and transcoding, the model by McCloskey provides assumptions on the calculation system. This system entails three main components: “arithmetic signs”, “arithmetic fact knowledge”, and “procedures”. Arithmetic signs constitute an independent component, in which each sign (e.g., +, −, ×, :, =, etc.) can be selectively lost. Arithmetic fact knowledge includes information on simple calculation that is stored in semantic memory as a result of overlearning and can be accessed directly from there. As demonstrated by its preservation in severe cases of semantic dementia (Zamarian, Karner, Benke, Donnemiller & Delazer, 2006), this information constitutes a relatively independent portion of semantic memory. Examples of arithmetic facts are the multiplication tables (e.g., 2 × 3) and single-digit operations (e.g., 3 + 4, 7 − 3), whose result can be retrieved from memory quickly, without actually calculating it. According to Dagenbach & McCloskey (1992), there are segregated memory networks specific for each operation. The so-called “arithmetic rules” are also learned by heart and are part of this semantic knowledge. Arithmetic rules are operations whereby one of the elements (e.g., the addend or the multiplier) can be replaced by any number (e.g., n × 0 = 0, n × 1 = n, n + 0 = n, n + 1 = next number, n − 1 = previous number). Procedures define how to perform multi-digit addition, subtraction, multiplication, and division. They define not only the specific steps to be done (e.g., carrying or borrowing), but also the spatial arrangement and alignment of partial results in multi-digit operations.

Dehane and Cohen proposed the so-called “Triple Code” model of number processing and calculation, which has strongly influenced research and clinical practice in the following decades (Dehaene, 1992; Dehaene et al., 2003; Dehaene & Cohen, 1995, 1997). Importantly, this model makes also assumptions about the underlying anatomical correlates of its components. The model specifies three different codes (Fig. 2). The visual Arabic number code represents numbers as sequences of simple digits. This code is used for number reading and writing, in multi-digit operations and also for parity judgments. The visual Arabic code is implemented in the bilateral posterior superior parietal lobe (PSPL). The auditory verbal number code regards verbal sequences of words. This code is used in counting, reading aloud, writing verbally expressed numbers, and reciting arithmetic fact knowledge (e.g., “two-times-three-is-six”). This code depends on the perisilvian language regions of the left hemisphere, particularly on the left angular gyrus (AG). The analogue-magnitude code represents the quantity associated with a number as local distributions of activation on an oriented mental number line. It is used in number comparison, subitizing, quantitative estimation, back-up strategies, and approximate calculation. Subitizing refers to the ability to immediately appreciate small quantities, typically from 1 to 4, without apparent serial processing. The analogue-magnitude code is supported by the horizontal portion of the interparietal sulcus (HIPS) bilaterally.

Figure 2 Schematic representation of the Triple-code model (e.g., Dehaene, 1992).

The “Triple Code” model also postulates a “two-way” pathway for simple calculation (Dehaene & Cohen, 1997). A direct, asemantic verbal-route is used for overlearned calculations (in particular, multiplication tables and small additions). This direct route is supported by a cortico-subcortical circuit located in the left hemisphere, including the thalamus and the basal ganglia. An indirect, semantic route is employed in answering simple calculation problems when no verbal association is available (typically, subtraction and division problems). This indirect route requires access to quantity representations and is supported by the parietal areas bilaterally (Dehaene et al., 2003). Further extensions of the “Triple Code” model and updates on the cerebral correlates at the basis of number processing and calculation can be found in recent meta-analysis studies (Arsalidou, Pawliw-Levac, Sadeghi & Pascual-Leone, 2018; Arsalidou & Taylor, 2011; Hawes, Sokolowski, Ononye & Ansari, 2019).

Other models have been proposed as well. The “preferred-entry code” hypothesis emphasizes individual differences (Noel & Seron, 1995; Noel & Seron, 1993). Each person may use an individually preferred code to access number meaning and perform numerical tasks. Accordingly, some people would perform a calculation using a verbal entry code, while others would prefer a visual entry code. It follows that impairments of the transcoding from one specific notation (e.g., Arabic) to the preferred-entry code (e.g., verbal) will impair all numerical tasks (e.g., number comparison or calculation) presented in this notation (Arabic). In sum, some models on calculation assume that arithmetic facts are stored as verbal sequences, while others suggests that they are stored as abstract memory representations. As a consequence, models differ in their explanations of the typical effects observed in acquired calculation disorders.

Acquired impairments of calculation and number processing

The number processing and calculation system is, to a high degree, modular, i.e. its components are anatomically and functionally independent. As a consequence this system can be damaged in many ways and, therefore, acalculia is actually an extremely variable syndrome that may consist of very different and often independent symptoms. The study of single cases, conducted with the methods of cognitive neuropsychology, has indeed highlighted a great variety of very selective deficits (for a recent and exhaustive discussion, see Semenza, 2019).

In the clinical setting, the traditional classification of numerical disorders is still regarded for. Lewandowski & Stadelmann (1908) are generally considered to be the first authors who described a patient with a severe calculation disorder without linguistic disturbances. The first systematic observations of numerical disorders led to a first classification (Bergen, 1926; Henschen, 1919, 1926), later revised by Hecaen and colleagues (Hecaen, Angelergues & Houillier, 1961). This classification was based on the distinction between acalculia secondary to language disorders (due to a damage to language areas, primarily to the perisilvian areas of the left hemisphere), primary acalculia (“anarithmetia”, consequent to a left parietal damage), and spatial acalculia (secondary to generic or specific spatial disturbances, typically due to unilateral spatial neglect, generally following a damage to the right hemisphere). However, this simple classification does not account for the great variety of numerical disorders reported in the literature, whose explanation definitely profits from the theoretical models described above. Here, we shortly describe the main forms of number processing and calculation disorders.

Number transcoding

Transcoding disorders can be more or less selective and affect distinct tasks. An important distinction has to be done between “lexical” errors and “syntactic” errors (Deloche & Seron, 1982). Lexical errors consist of the incorrect production of one or more of the individual digits in a number (e.g., 6 instead of 8, 25 instead of 49, 5723 instead of 5743). In syntactic errors, there are violations of the order of magnitude, while the correct lexical elements are spared. In these errors, the power of ten is thus different from that of the target. As a consequence syntactic errors may result in longer numbers, as in “60035” instead of “635”, or in shorter numbers, as in “43” instead of “403”, while maintaining the same digits appearing in the target. Although these two types of errors usually coexist, cases are reported mostly featuring one type only. Deloche & Seron (1982) and Seron & Deloche (1983) found that syntactic errors tend to be associated with syntactic disorders (as in Broca's aphasia), while lexical errors are more frequently observed in patients with lexical disorders (like in Wernicke's aphasia). The syntax governing the use of language is, however, much more complex than the so-called “syntax of numbers” and the analogy between the two is a superficial one. Benavides-Varela and colleagues (2016), studying the effect of right hemisphere lesions, found several syntactic errors in the transcoding of numbers including zero (e.g., 30203 or 20500). These errors emerged in particular following lesions involving the insula. This is interesting insofar these patients did not suffer from linguistic disorders. The same study showed that these errors do not depend on spatial problems such as, for example, unilateral spatial neglect (Benavides-Varela et al., 2016). Other studies (Bencini et al., 2011; Messina, Denes & Basso, 2009; Semenza et al., 2007) showed that aphasics may commit numerous phonological errors with non-numerical words, while with number words they commit exclusively substitutions of the component digits, i.e. lexical errors.

Arithmetic signs

In relatively rare cases, patients do not understand and/or name the arithmetic signs but can perfectly calculate (Ferro & Silveira Botelho, 1980; Laiacona & Lunghi, 1997). For example, they indicate 7 instead of 12 as the result of 3 × 4, thus confusing “×” with “+”. Remarkably the same patients are able to understand words such as minus, plus, times, and divided, to match these words to the correct operation, and to correctly perform the same calculations in the oral modality.

Arithmetic facts

The term “arithmetic facts” typically refers to one-digit problems (addition, subtraction, multiplication, and possibly division; e.g., 3 + 4, 7 − 3, 2 × 5, 6 : 2) that do not require further computational processes or strategies to be solved and can be directly retrieved from long-term memory (LTM). Neuropsychological studies have described various patterns of selectively preserved and selectively impaired operations. There have been reported cases of impaired multiplication fact knowledge in association with better or entirely preserved addition and/or subtraction knowledge (Delazer et al., 2004; Hittmair-Delazer, Semenza & Denes, 1994; van Harskamp & Cipolotti, 2001), cases with the reverse dissociation (Dehaene & Cohen, 1997; Delazer, Benke, Trieb, Schocke & Ischebeck, 2006; Delazer & Benke, 1997; van Harskamp & Cipolotti, 2001), cases where subtraction was relatively better preserved than multiplication and addition (Dagenbach & McCloskey, 1992; Pesenti, Seron & van der Linden, 1994), and also a case with the opposite dissociation, i.e. selectively impaired subtraction (van Harskamp & Cipolotti, 2001). Theoretical models have proposed divergent explanations for these operation-specific deficits. While Dagenbach & McCloskey (1992) suggested that dissociations between operations arise from a selective damage to segregated memory networks specific for each operation, Dehaene & Cohen (1995) emphasised different processing levels for answering the four basic operations (rote-verbal memory with multiplication and very simple addition vs. backup strategies and semantic manipulation of numerical quantities with subtraction, more complex addition, and division). Although there is a correlation between language and calculation, neuropsychological single-case studies point to a relative autonomy of both domains, suggesting that possible dissociations between language and calculation skills as well as between arithmetic operations might be related to the depth of processing of arithmetic problems (for a discussion, see Zamarian, López-Rolón & Delazer, 2007).

Arithmetic rules

Arithmetic rules involving zero are generally the ones that are most affected (McCloskey, Aliminosa & Sokol, 1991). The ability to use zero may vary depending on the context: for example, a patient may use zero in the context of complex operations, but not when presented in isolation as arithmetic rule, or vice versa (Semenza, Grana & Girelli, 2006).

Procedural knowledge

The impairment of arithmetic procedures can concern single operations. Selective deficits have been, in fact, found for subtraction, multiplication, or division (Chiarelli, Menichelli, Zadini & Semenza, 2011; Cipolotti & de Lacy Costello, 1995; McCloskey et al., 1985; Venneri & Semenza, 2011). Although patients may present with deficits in both, procedures and arithmetic fact knowledge (Benson & Weir, 1972), different cases have shown that these two components of the calculation system are functionally independent and may dissociate from each other (Hittmair-Delazer et al., 1994; Miceli & Capasso, 1999; Sokol, McCloskey, Cohen & Aliminosa, 1991). Procedures and conceptual knowledge may also dissociate (Cappelletti, Kopelman, Morton & Butterworth, 2005; Girelli & Delazer, 1996). Deficits with arithmetic procedures may be specific to the single operations and may resemble the “bugs” of computer programmes. A patient described by Girelli and Delazer (1996) ignored the borrowing procedure with complex subtraction problems: he systematically subtracted the smaller number from the larger number, even when the procedure would have required the use of borrowing. This is the only type of error the patient committed. He made it every time a complex subtraction problem required the borrowing procedure. Various attempts to teach him what he should do were not successful (Girelli & Delazer, 1996). The authors argued that such errors resulted from the application of an erroneous algorithm. Semenza, Miceli and Girelli (1997) proposed that a monitoring deficit as well may cause difficulties in complex calculation. The correct application of calculation procedures requires not only the knowledge of the single steps to be done but also the execution of the steps in the correct order. Their patient, MM, indeed showed a “monitoring defect”, i.e. an inability to maintain attention over time and monitor the sequence of sub-steps specified in the procedure. As often seen, MM experienced greater difficulty with more complex problems and more difficulties in the final steps of the procedure (Semenza et al., 1997).

Conceptual knowledge

Calculation is not only supported by the retrieval of arithmetic facts from LTM or by the execution of learnt arithmetic procedures, but also by conceptual knowledge, i.e. the understanding of arithmetic operations and principles. Hittmair-Delazer and colleagues (Hittmair-Delazer et al., 1994, Hittmair-Delazer, Sailer & Benke, 1995) reported cases of patients with selectively preserved conceptual knowledge with severe deficits in facts retrieval. For example, patient BE could not retrieve the answer to simple fact problems from memory (e.g. 7 × 6), but invented complex and mathematically correct strategies to answer problems. These strategies impressively showed the preservation of conceptual knowledge of mathematics. Later, Delazer & Benke (1997) described the opposite dissociation, i.e. no conceptual understanding but intact recall of arithmetic facts from memory.

Spatial acalculia

Spatial acalculia has been traditionally considered as secondary to generic or specific spatial disturbances. A patient suffering from object-centered neglect, for example, would neglect the leftmost side of a multi-digit operation, thus making a series of errors reflecting the omission of the leftmost digits. Other errors stem from the inability to use spaces to join or separate numbers, difficulty keeping numbers aligned, etc. A typical error is the incorrect alignment of the partial products, which, in multiplication, requires the sliding of the sub-products (depending on the country, either on the left or on the right). Errors can be very selective and, in some cases, cannot be directly attributable to generic disturbances in spatial exploration and organization. Granà, Hofer and 71-2Semenza (2006), for example, reported a patient suffering from a right hemisphere lesion, whose errors seemed to have a precise cause. According to the authors, these errors were associated with a memory loss of “where” the digits must be arranged in the various steps necessary to complete a complex multiplication. In fact, the patient did not present with other spatial disturbances that could explain the deficit; in particular, no sign of neglect was detectable. Granà et al. (2006) suggested that the patient suffered of a defect in the spatial schema that helps normal individuals to know where exactly each sub-step of complex multiplications must be placed.

Clinical assessment of number processing and calculation

To detect and precisely characterize numerical disorders in neurological patients, the clinical evaluation of numerical skills should consider separately the different components of the number processing and calculation system described above. Not only the patient's response times and accuracy but also the type of errors committed may be very informative of the type of numerical disorder presented. It is advisable that the evaluation of numerical skills takes place within a comprehensive neuropsychological assessment, in order to exclude a possible influence of more general cognitive deficits such as deficits in attention, memory or language. Different standardized test batteries including normative data have been proposed (Arcara et al., 2019; Claros-Salinas, 1993; Delazer, Girelli, Granà & Domahs, 2003; Dellatolas, Deloche, Basso & Claros-Salinas, 2001; Deloche et al., 1994; Ibrahimovic, Bulheller & Häcker, 2002; Kalbe, Brand & Kessler, 2002; Semenza et al., 2014). In general, these are (more or less extensive) screening batteries, i.e. typically, it is necessary to administer more items of the type that the patient has failed, once a selective numerical deficit is identified, in order to fully understand the nature and severity of the deficit. One example of numerical test batteries that is also standardized for German-speaking patients is the Number Processing and Calculation (NPC) Battery (Delazer et al., 2003). This battery assesses:

  1. 1.
    Counting skills: Counting sequences (tested in oral and written format; e.g., counting backward starting from 15, counting forward two by two starting from 3); dot counting (“how many dots are there?”; dot sets of different numerosity are presented).
  2. 2.
    Numerical understanding: Number comparison (“which of these two numbers is larger?”, tested in three formats: Arabic numerals, written number words, and spoken numerals); Parity judgments (“is this number odd or even?”); Analogue number scale (the position corresponding to an Arabic numeral has to be indicated on two analogue scales, one from 1 to 100, the other from 1 to 50, choosing from among three alternatives); Transcoding from Arabic numerals into tokens (the tokens are of value 1, 10 or 100, and have to be used to indicate the value of a given Arabic numeral: e.g., 33 = three tokens of 10 and three tokens of 1).
  3. 3.
    Numerical transcoding: Reading aloud Arabic numerals or written number words; Writing Arabic numerals to dictation; Transcoding from written number words or from tokens into Arabic numerals.
  4. 4.
    Calculation skills and arithmetic principles: Arithmetic facts (simple additions, subtractions, multiplications, and divisions, presented in Arabic format and answered orally); Multiplication multiple choice (the answer to a simple multiplication problem has to be selected among four alternatives, one of which is correct, one belonging to the same multiplication table, one belonging to another multiplication table, one not belonging to the multiplication tables); Approximate calculation (multi-digit additions, subtractions, multiplications and divisions, where the value that comes closest to the correct answer has to be chosen among four alternatives); Text problems (involving the use of one of the four operations presented in a concrete context; e.g., “A fire truck costs € 232,000 and four municipalities share the costs. How much does each pay?”); Mental calculation (multi-digit operations that must be solved orally); Written calculation (multi-digit operations that must be solved in written format); Arithmetic principles (e.g., “32 + 56 = 88, 56 + 32 = ?”).

In addition to the “classic” test batteries, one can also use more sophisticated, experimental computer tasks. Different paradigms have been proposed, including production, verification, matching, and bisection tasks. In computerized verification tasks, healthy subjects are typically slower in rejecting related results (e.g., 5 × 6 = 35) than in rejecting unrelated results (e.g., 5 × 6 = 32). Such tasks may be revealing about the degree of automaticity in arithmetic fact retrieval from LTM (Lefevre, Bisanz & Mrkonjic, 1988). In “number-matching” tasks, pairs of digits (e.g., 5 9) are presented on the screen and followed by a target number (e.g. 59). The subject has to decide whether the first two numbers are identical to the second pair of numbers presented. Healthy subjects are slower in rejecting false target numbers that match the sum (14) or product (45) of the previously presented pair than in rejecting unrelated target numbers (e.g., 47) (Galfano, Rusconi & Umiltà, 2003). Number matching tasks have been used in the assessment of arithmetic fact knowledge in patients with Alzheimer's dementia (Jurado & Rosselli, 2017) and mild cognitive impairment (Zamarian, Stadelmann, et al., 2007), as well as in a single case with semantic dementia (Zamarian et al., 2006). Table 1 gives an overview of numerical and calculation skills together with typical tasks assessing these skills.

Table 1 Examples of numerical and calculation skills together with typical tasks for their assessment

As seen above, the components of the number processing and calculation system can be selectively disrupted or spared following brain damage. Before starting a treatment, a comprehensive neuropsychological assessment is necessary to characterize the pattern of disrupted/spared numerical abilities. In this work, we aim to present evidence that systematic rehabilitation can lead to improvement of numerical competence in adult neurological patients, even in very unfavorable circumstances (e.g., older age, chronic stage or severe impairments).

Methods

This review focusses on the rehabilitation of simple calculation, i.e. on the (re-)learning of arithmetic fact knowledge and competence. Its purpose is not to be exhaustive but to summarize the most recent rehabilitation studies and which training methods are mostly used. It also aims to give an idea of which improvements can be expected through a specific intervention. As it will be inferred from the examples below, the rehabilitation of simple calculation tends to be very specific. In other words, it may sometimes have only an effect on the trained material/task, without this effect necessarily extending to other similar (but untrained) materials/tasks.

Also, improvements in calculation can be expected only after a targeted calculation training. That means, the rehabilitation of other functions, such as attention or language, has normally little if no effect on numerical disorders, although it might have beneficial effects on the patient's performance in general. Here below, we provide a summary of the main rehabilitation approaches, followed by concrete examples of their application. Note that most of the studies concern the treatment of single cases.

Results

Rehabilitation methods

Most rehabilitation studies on simple calculation in neurological patients have adopted the “drill” approach, i.e. intensive repetition. Usually, in this approach, the patient is presented repeatedly with specific problems and receives immediate feedback on the correctness of the answer. This approach is based on the principles of associative learning, shared by the most current cognitive models on the representation of arithmetic fact knowledge in LTM (Ashcraft, 1995; Campbell, 1987; Siegler, 1988; for a review, Domahs & Delazer, 2005). According to these models, arithmetic facts, once they are learned by heart, are stored in an associative network in declarative memory. Through intensive repetition, the association between a problem and its correct solution should be (re-)strengthened. Immediate feedback is given to prevent the formation or strengthening of incorrect associations. Similarly, to foster error-free learning, one can present simultaneously a problem together with its correct answer. Some studies have combined intensive repetition with the use of a sort of help or “cue” (see below; Domahs,Lochy, Eibl & Delazer, 2004, Domahs, Zamarian & Delazer, 2008). In principle, simple calculation relies not only on the retrieval of arithmetic facts from LTM but also on the execution of procedures and the application of conceptual knowledge (Delazer, 2003). It follows that the (re-)learning of arithmetic facts can be based not only on intensive repetition but also on the improvement of procedural or conceptual knowledge (Girelli, Bartha & Delazer, 2002). For example, one can teach the patients backup strategies that are based on the use of arithmetic principles (e.g., decomposition principle; e.g., 6 × 3 = 6 + 6 + 6) (Girelli et al., 2002). Some studies have also shown positive training effects by adopting both conceptual and drill approaches (Domahs, Bartha & Delazer, 2003) (see Table 2 for a summary of the main rehabilitation approaches on simple calculation).

Table 2 Rehabilitation approaches on simple calculation

Rehabilitation of arithmetic fact knowledge through intensive repetition

As described above, most rehabilitation studies on simple calculation have used the “drill” approach (Miceli & Capasso, 1999). For example, Kashiwagi, Kashiwagi and Hasegawa (1987) described eight aphasic patients having difficulty with multiplication and division but not with addition and subtraction. Patients underwent a month or two of daily intensive “drill” training of multiplication tables. After training, all patients showed an improvement in multiplication facts retrieval. This improvement was, however, very specific as it was evident only in tasks where the presentation and response modes were identical to those used during training.

Hittmair-Delazer and colleagues (1994) also adopted intensive training of multiplication facts. They reported on a 45-year-old accountant (patient BE), who had suffered from a cerebral embolism in the left basal ganglia and had a highly selective deficit with multiplication and division facts. BE could retrieve from memory only the 2 times table and the so-called “ties” (e.g., 4 × 4). Other problems were solved through strategies based on arithmetic principles (e.g., 8 × 4 = 8 × 2 + 8 × 2), which led him to the correct solution but were complicated and time-consuming. Problems that could not be solved through direct retrieval from memory were divided into two sets and presented separately according to an experimental design of the ABACA type (where A indicates a test session, B the training with the first set, C the training with the second set) (Hittmair-Delazer et al., 1994). After an intensive training of four weeks with each set, BE showed highly specific performance improvements. That is, he could quickly solve the problems exercised but not, for example, problems complementary to those practiced during the training (e.g., problem practiced 3 × 4; complementary problem 4 × 3). BE was, however, able to apply the learned multiplication facts to solve complex written calculations and divisions.

Girelli, Delazer, Semenza and Denes (1996) also used a very similar training with their patients TL and ZA, who had severe difficulties in retrieving multiplication facts from memory. After an intensive training of eight weeks, which had an experimental design of the ABACA type (see above), TL and ZA showed significant improvements by responding correctly to more than 90% of the trained problems. Improvements of both patients were greater with the trained problems than with untrained problems, although they also showed some generalization effects. Through training, accuracy increased but also the type of errors changed. For example, before training, TL mostly committed mistakes of the type 2 × 9 = 44, where the answer given did not belong to any tables. After training, however, TL's errors were mostly of the type 6 × 3 = 21, where the answer given belonged to the same table as the correct one. ZA's errors before training were similar to those of TL. However, after training, ZA mostly committed errors that were numerically close to the correct answer (e.g., 5 × 6 = 31). According to the authors (Girelli et al., 1996), the type of errors after training reflected the type of strategies adopted. Likely, TL recited the series of multiplications belonging to a table, stopping one answer before or after the correct one. ZA used repeated addition, sometimes committing calculation errors (e.g. 4 × 6 = 6 + 6 + 6 + 6 = 25). Patients ZA and TL could also apply the acquired knowledge in new contexts such as, for example, with divisions or written problems.

Difficulties in the retrieval of multiplication facts were also presented by patient MC, a 42-year-old computer programmer, who had a brain tumor in his left parietal lobe surgically removed (Whetstone, 1998). During training, MC intensely repeated three different sets of multiplications that were presented separately in a single specific format (phonological, graphemic or Arabic code). Problems were presented together with their correct answer to avoid the formation or strengthening of incorrect associations. Each training session was, however, preceded and followed by a test in which MC had to produce the solution himself. After training, MC responded highly accurately (97% correct) but tended to give faster responses with the problems presented in the exercised code than in a different one.

The next two studies adopted both intensive repetition and the use of some sort of help (or “cue”). Domahs and colleagues (2004) described ME, a 38-year-old mechanic who had suffered a head injury three years prior to their investigation. ME had difficulties in particular with multiplication and division. He could answer most problems correctly (98.0% and 93.3% correct answers, respectively) but was extremely slow (he needed up to 90 seconds), which suggests the use of backup strategies rather than direct retrieval from LTM. During training (12 sessions), problems were presented in nine different colors based on the unit of the result (e.g., the 4 × 3, 6 × 2, 8 × 4, 7 × 6 and 9 × 8 problems were all presented in yellow since the unit “2” of the result, i.e. 12, 12, 32, 42 and 72, was associated with the color yellow). After ten “colored” training sessions, ME could respond fast to the trained problems, even when these were presented in black. ME also showed improvements with complementary multiplications and untrained multiplications.

In a subsequent study, Domahs and colleagues (2008) aimed to understand whether this facilitating effect was due to a special relationship between colors and numbers in the brain. In their new study, Domahs and colleagues (2008) administered a “sound”-based training to their patient EK, an 81-year-old accountant who had suffered a cerebral infarction a few years earlier. During training (15 sessions), two sets of different multiplications (set A and set B) were repeated intensively. While problems of set A were presented without cue, those of set B were presented together with a cue (a sound). According to the same principle used in the previous study, problems of set B were presented together with different sounds, associated with the second digit of the result. Unlike the previous study, however, the authors did not explicitly explain to the patient the function of the sounds and the underlying association principle. After training, EK showed significantly faster reaction times with both sets. Improvements in accuracy were, however, higher with problems of set B (with cue) than with those of set A (without cue). Considering the effectiveness of the “sound”-associated training, the results reported by Domahs et al. (2004) cannot be simply explained by a “special relationship” between numbers and colors. Results of both studies demonstrate the effectiveness of a multimodal rehabilitation approach and that “implicit” cues can help in the rehabilitation of simple calculation in adult patients whose numerical abilities are partly preserved.

Rehabilitation of arithmetic fact knowledge through a conceptual training

A conceptual approach to the rehabilitation of simple calculation in adult neurological patients was adopted, for example, by Girelli et al. (2002) and by Domahs et al. (2003). In Girelli et al. (2002), patient FS, a 64-year-old retired bank employee, had severe difficulties to retrieve multiplication facts and to use independently back-up strategies to find out solutions. The authors focused the training on the strategic use of FS's residual knowledge and on the explicit reference to arithmetic principles (for example, commutativity or decomposition principle). Aim of the training was to help FS deriving unknown solutions from problems that he could retrieve automatically and, at the same time, reducing the amount of information to be stored. FS was taught a specific backup strategy for each problem to be learned (e.g., 2 × 4 = 4 × 2; 3 × 4 = 3 × 3 + 3; 3 × 9 = 3 × 10 − 3). Problems were divided into two sets, one set practiced a first week, a second set on the following week. After the first training week, FS showed greater accuracy with both trained and untrained sets. Improvements were, however, greater with the trained set. After the second week, FS achieved a perfect performance. After training, FS also showed to be able to use different strategies than the ones explicitly taught.

Domahs et al. (2003) used both a conceptual and a drill approach. Patient HV, an year-old former manager, had a severe calculation deficit. He was unable to retrieve multiplication tables from memory and showed little conceptual knowledge of the underlying operation. HV had, however, less difficulty with addition. Therefore, he underwent first a “conceptual” training, where he learned to solve a set of multiplication problems through repeated additions. After five “conceptual” training sessions, he was presented with six sessions of “drill” training, where he intensely repeated the same problems. Accuracy with trained multiplications improved to 63.6% after the conceptual training and to 70.0% after the “drill” training. Improvements with both, trained and untrained problems, were only found after the conceptual training but not after the drill training. As a result of conceptual training, the type of errors also changed qualitatively, becoming more plausible.

Overall, these two studies demonstrate the effectiveness of a short conceptual rehabilitation approach to simple calculation. Furthermore, they show that the newly acquired conceptual knowledge proves to be flexible, as it can be also applied to new contexts. As the studies suggest, repetition training alone is not successful in cases of conceptual deficits. Indeed, in these cases conceptual training should precede any form of repetition or drill. Although in some cases after a conceptual training performance fails to reach perfection, errors become more plausible, due to the type of strategies used.

Neural correlates of performance improvements following a rehabilitation of arithmetic fact knowledge

There are also studies that have addressed which brain activation changes occur following the rehabilitation of calculation skills in neurological patients (Claros-Salinas et al., 2014; Zaunmüller et al., 2009). Zaunmüller and colleagues (2009) administered an intensive training of multiplication facts (40 sessions over 4 weeks) to WT, a 49-year-old patient, who suffered a left brain damage 29 months earlier. Both before and after training, WT was assessed with functional magnetic resonance imaging (fMRI). Post-training fMRI results showed an activation increase in the right AG in the contrast trained versus untrained problems. An increase was, therefore, found in the hemisphere contralateral to the side of the lesion, in an area homologous but contralateral to that typically activated by healthy subjects during arithmetic fact retrieval (for a review see Zamarian, Ischebeck, & Delazer, 2009). Claros-Salinas and colleagues (2014) described seven patients with dyscalculia following differently located brain lesions. Patients underwent a computer training on the four basic operations (14 sessions over 4 weeks). As in the study by Zaunmüller and colleagues (2009), they were assessed through fMRI both before and after training. Post-training fMRI results showed an association between performance improvements and a reduction in activation of prefrontal areas, specifically in the middle and superior prefrontal gyrus. According to the authors, these results suggest that performance improvements following training reflect an increased effectiveness in the functioning of the prefrontal lobes.

The results of these two studies are indeed very interesting, but they must be interpreted with some caution. In fact, the great variability among the participants, regarding both the localization and etiology of the lesion and the type of disorders shown, calls for further confirmation.

“Unspecific” arithmetic training in older people with or without cognitive decline

The studies reported above should be differentiated from those using calculation as training material to maintain or improve cognitive functioning in older age. For example, Kawashima et al. (2005) administered a 6-months cognitive training to patients with Alzheimer's disease, who were required to perform 20min a day (2–6 days a week) both reading and arithmetic tasks. Compared to patients in the control group, who did not perform any training, patients in the experimental group showed at follow-up improvements in a screening test battery of executive functions (Kawashima et al., 2005). Similar results were reported for healthy older people (Nouchi et al., 2016) and older postoperative patients who underwent general anesthesia (Kulason et al., 2018). Although interesting, these studies cannot be considered as direct evidence of training-related arithmetic improvements. However, they demonstrate the indirect positive effects of an intensive, although unspecific training on general cognitive functioning in older adults.

Discussion

Brain-damaged adult patients can show very specific deficits in number processing and calculation. These deficits may appear in association with – but be independent of – deficits in other cognitive functions such as memory, executive functions or attention. The clinical assessment of these numerical deficits requires the use of appropriate tests that are possibly based on well-established theoretical models. In general, the studies reported here show that deficits in simple calculation can significantly improve following a targeted intervention program. Positive training effects are possible even in very unfavorable circumstances such as, for example, during the chronic stage, with older age or in the presence of severe calculation deficits. Research has demonstrated that a targeted rehabilitation program may lead to improvements in other numerical skills as well, such as, for example, numerical transcoding (Ablinger, Weniger & Willmes, 2006; Deloche, Seron & Ferrand, 1989, Deloche et al., 1992), the solution of arithmetic text problems (Fasotti, 1992), arithmetic procedures (Capasso, 2012), or the understanding and use of complex numerical concepts such as percentages, proportions and fractions (Burgio et al., 2018; Zamarian et al., 2019). The appropriate training program should be chosen depending on the type of deficit.

There are two main rehabilitation approaches for simple calculation: conceptual and drill (i.e. intensive repetition). As for the rehabilitation of other cognitive functions, the choice of which approach is the more appropriate as well as of other training-relevant criteria (e.g., material, format, duration or intensity) depends on the type of numerical/calculation disorders presented but also on the patient’s residual abilities and limits. For some patients, it may be advantageous to resort to an answer format facilitating the correct answer in order to prevent errors. For example, one could use a verification task, a multiple-choice task, or give part of the correct solution, which the patient has to complete. The use of cues (colours, sounds, or other) may also be helpful. The error rate should always be kept low during the learning process.

Improvements following training are usually characterized by higher accuracy and faster response times with the trained material. In some cases, patients even show some improvements with untrained material. Improvements in accuracy and response times may be in some cases associated with changes in the type of errors committed, going from absolutely implausible errors to more plausible errors. Recent evidence has shown that performance improvements following training are accompanied by a reorganization of calculation-relevant brain activations. Importantly, improvements in number processing and calculation typically lead to better mastering of every-day situations (e.g., comparing prices, calculating train times) and thus to higher autonomy of patients in daily life. In conclusion, arithmetic (re-)learning in neurological patients is feasible and may be very effective. It must therefore be highly recommended for the full restoring of the autonomy in daily activities.

Limitations

Although the literature search used various databases, we cannot rule out that individual relevant works were not included in the study. In addition, the review includes only works written in English. It is possible that further research written in other languages would have contributed to a more comprehensive picture of the existing literature. This review does not claim to be systematic or exhaustive.

Relevance for the practice

This study shows that improvements of calculation deficits are possible through a targeted training program even in very unfavorable circumstances. Although tailored to the patient's needs and characteristics, the clinical assessment and the training program should be systematic and possibly based on well-established theoretical assumptions and evidence. For the professionals involved (psychologists, therapists …), this implicates an ad-hoc preparation that includes both theoretical and practical knowledge on number cognition. Thus far, very few Universities and post-gradual training institutes, at least in German-speaking countries, offer seminars or practical opportunities in this area. Professionals are therefore mostly required to rely on their own initiative and self-education. This makes the rehabilitation of number deficits something “elitist”, if compared to the rehabilitation of other cognitive deficits (e.g., language, memory, executive functions, attention, or visual exploration), which cannot be offered to all the patients needing it. Specific training for professionals in number cognition should be posit among the priorities of public health policies, strategies, and plans.

Dr. Laura Zamarian, PhD, Department of Neurology (Neuropsychology Unit), Medical University of Innsbruck, Anichstr. 35, 6020 Innsbruck, Austria

References

  • Ablinger, I., Weniger, D. & Willmes, K. (2006). Treating number transcoding difficulties in a chronic aphasic patient. Aphasiology, 20(1), 37–58. https://doi.org/10.1080/02687030500298719 First citation in articleCrossrefGoogle Scholar

  • Arcara, G., Burgio, F., Benavides-Varela, S., Toffano, R., Gindri, P., Tonini, E. et al. (2019). Numerical Activities of Daily Living – Financial (NADL-F): A tool for the assessment of financial capacities. Neuropsychological Rehabilitation, 29(7), 1062–1084 https://doi.org/10.1080/09602011.2017.1359188 First citation in articleCrossrefGoogle Scholar

  • Arsalidou, M., Pawliw-Levac, M., Sadeghi, M. & Pascual-Leone, J. (2018). Brain areas associated with numbers and calculations in children: Meta-analyses of fMRI studies. Developmental Cognitive Neuroscience, 30, 239–250. https://doi.org/10.1016/j.dcn.2017.08.002 First citation in articleCrossrefGoogle Scholar

  • Arsalidou, M. & Taylor, M. J. (2011). Is 2 + 2 = 4? Meta-analyses of brain areas needed for numbers and calculations. NeuroImage, 54(3), 2382–2393. https://doi.org/10.1016/j.neuroimage.2010.10.009 First citation in articleCrossrefGoogle Scholar

  • Ashcraft, M. H. (1995). Cognitive Psychology and Simple Arithmetic: A Review and Summary of New Directions, 1(1), 3–34. First citation in articleGoogle Scholar

  • Benavides-Varela, S., Passarini, L., Butterworth, B., Rolma, G., Burgio, F., Pitteri, M. et al. (2016). Zero in the brain: A voxel-based lesion-symptom mapping study in right hemisphere damaged patients. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 77, 38–53. https://doi.org/10.1016/j.cortex.2016.01.011 First citation in articleCrossrefGoogle Scholar

  • Bencini, G. M. L., Pozzan, L., Bertella, L., Mori, I., Pignatti, R., Ceriani, F. et al. (2011). When two and too don’t go together: A selective phonological deficit sparing number words. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 47(9), 1052–1062. https://doi.org/10.1016/j.cortex.2011.03.013 First citation in articleCrossrefGoogle Scholar

  • Benson, D. F. & Weir, W. F. (1972). Acalculia: Acquired Anarithmetia. Cortex, 8(4), 465–472. https://doi.org/10.1016/S0010-9452(72)80008-X First citation in articleCrossrefGoogle Scholar

  • Bergen, H. (1926). Über Rechenstörungen bei Herderkrankungen des Grosshirns. Archives Psychiatrie und Nervenkrankheiten, 78, 236–263. First citation in articleGoogle Scholar

  • Burgio, F., Delazer, M., Meneghello, F., Pertl, M.-T., Semenza, C. & Zamarian, L. (2018). Cognitive Training Improves Ratio Processing and Decision Making in Patients with Mild Cognitive Impairment. Journal of Alzheimer's Disease: JAD, 64(4), 1213–1226. https://doi.org/10.3233/JAD-180461 First citation in articleCrossrefGoogle Scholar

  • Campbell, J. I. D. (1987). Network interference and mental multiplication. Cognition, 13, 109–123. First citation in articleGoogle Scholar

  • Capasso, R. (2012). Riabilitazione del sistema dei numeri e del calcolo. In A. MazzucchiEd., La Riabilitazione Neuropsicologica. Premesse Teoriche e Applicazioni Cliniche. (3rd.). Milan, Italy: Elsevier Health Sciences. First citation in articleGoogle Scholar

  • Cappelletti, M., Kopelman, M. D., Morton, J. & Butterworth, B. (2005). Dissociations in numerical abilities revealed by progressive cognitive decline in a patient with semantic dementia. Cognitive Neuropsychology, 22(7), 771–793. https://doi.org/10.1080/02643290442000293 First citation in articleCrossrefGoogle Scholar

  • Chiarelli, V., Menichelli, A., Zadini, A. & Semenza, C. (2011). Good division, but bad addition, subtraction and multiplication. A “leftmost-first” bug? Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 47(2), 250–258. https://doi.org/10.1016/j.cortex.2010.08.004 First citation in articleCrossrefGoogle Scholar

  • Cipolotti, L. & Butterworth, B. (1995). Toward a multiroute model of number processing: Impaired number transcoding with preserved calculation skills, 124(4), 375–390. First citation in articleGoogle Scholar

  • Cipolotti, L. & de Lacy Costello, A. (1995). Selective impairment for simple division. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 31(3), 433–449. https://doi.org/10.1016/s0010-9452(13)80058-5 First citation in articleCrossrefGoogle Scholar

  • Claros-Salinas, D. (1993). Texte verstehen. Materialien für Diagnostik und Therapie. [Text comprehension. Material for diagnostic and therapy.] (Bd. 3). Dortmund: Borgmann Publishing. First citation in articleGoogle Scholar

  • Claros-Salinas, D., Greitemann, G., Hassa, T., Nedelko, V., Steppacher, I., Harris, J. A. et al. (2014). Neural correlates of training-induced improvements of calculation skills in patients with brain lesions. Restorative Neurology and Neuroscience, 32(4), 463–472. https://doi.org/10.3233/RNN-130342 First citation in articleCrossrefGoogle Scholar

  • Dagenbach, D. & McCloskey, M. (1992). The organization of arithmetic facts in memory: Evidence from a brain-damaged patient. Brain and Cognition, 20(2), 345–366. https://doi.org/10.1016/0278-2626(92)90026-i First citation in articleCrossrefGoogle Scholar

  • Dehaene, S. (1992). Varieties of numerical abilities. Cognition, 44(1–2), 1–42. First citation in articleCrossrefGoogle Scholar

  • Dehaene, S., & Cohen, L. (1995). Towards an anatomical and functional model of number processing. Mathematical Cognition, 1, 83–120. First citation in articleGoogle Scholar

  • Dehaene, S. & Cohen, L. (1997). Cerebral pathways for calculation: Double dissociation between rote verbal and quantitative knowledge of arithmetic. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 33(2), 219–250. First citation in articleCrossrefGoogle Scholar

  • Dehaene, S., Piazza, M., Pinel, P. & Cohen, L. (2003). Three parietal circuits for number processing. Cognitive Neuropsychology, 20(3), 487–506. https://doi.org/10.1080/02643290244000239 First citation in articleCrossrefGoogle Scholar

  • Delazer, M. (2003). Neuropsychological findings on conceptual knowledge of arithmetic. In The development of arithmetic concepts and skills: Constructing adaptive expertise. (S.385–407). Mahwah, NJ, USA: Lawrence Erlbaum Associates Publishers. First citation in articleGoogle Scholar

  • Delazer, M. & Benke, T. (1997). Arithmetic facts without meaning. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 33(4), 697–710. First citation in articleCrossrefGoogle Scholar

  • Delazer, M., Benke, T., Trieb, T., Schocke, M. & Ischebeck, A. (2006). Isolated numerical skills in posterior cortical atrophy – An fMRI study. Neuropsychologia, 44(10), 1909–1913. https://doi.org/10.1016/j.neuropsychologia.2006.02.007 First citation in articleCrossrefGoogle Scholar

  • Delazer, M., Domahs, F., Lochy, A., Karner, E., Benke, T. & Poewe, W. (2004). Number processing and basal ganglia dysfunction: A single case study. Neuropsychologia, 42(8), 1050–1062. https://doi.org/10.1016/j.neuropsychologia.2003.12.009 First citation in articleCrossrefGoogle Scholar

  • Delazer, M., Girelli, L., Granà, A. & Domahs, F. (2003). Number processing and calculation – Normative data from healthy adults. The Clinical Neuropsychologist, 17(3), 331–350. https://doi.org/10.1076/clin.17.3.331.18092 First citation in articleCrossrefGoogle Scholar

  • Dellatolas, G., Deloche, G., Basso, A. & Claros-Salinas, D. (2001). Assessment of calculation and number processing using the EC301 battery: Cross-cultural normative data and application to left- and right-brain damaged patients. Journal of the International Neuropsychological Society: JINS, 7(7), 840–859. First citation in articleCrossrefGoogle Scholar

  • Deloche, G., Ferrand, I., Naud, E., Baeta, E., Vendrell, J. & Claros-salinas, D. (1992). Differential effects of covert and overt training of the syntactical component of verbal number processing and generalisations to other tasks: A single-case study. Neuropsychological Rehabilitation, 2(4), 257–281. https://doi.org/10.1080/09602019208401413 First citation in articleCrossrefGoogle Scholar

  • Deloche, G. & Seron, X. (1982). From one to 1: An analysis of a transcoding process by means of neuropsychological data. Cognition, 12(2), 119–149. First citation in articleCrossrefGoogle Scholar

  • Deloche, G., Seron, X. & Ferrand, I. (1989). Reeducation of number transcoding mechanisms: A procedural approach. In X. SeronG. DelocheEds., Cognitive approach in neuropsychological rehabilitation. (S.247–271). Mahwah, NJ, USA: Lawrence Erlbaum Associates Inc. First citation in articleGoogle Scholar

  • Deloche, G., Seron, X., Larroque, C., Magnien, C., Metz-Lutz, M. N., Noel, M. N. et al. (1994). Calculation and number processing: Assessment battery; role of demographic factors. Journal of Clinical and Experimental Neuropsychology, 16(2), 195–208. https://doi.org/10.1080/01688639408402631 First citation in articleCrossrefGoogle Scholar

  • Domahs, F., Bartha, L. & Delazer, M. (2003). Rehabilitation of arithmetic abilities: Different intervention strategies for multiplication. Brain and Language, 87(1), 165–166. https://doi.org/10.1016/S0093-934X(03)00252-9 First citation in articleCrossrefGoogle Scholar

  • Domahs, F. & Delazer, M. (2005). Some assumptions and facts about arithmetic facts. Psychology Science, 47(1), 96–111. First citation in articleGoogle Scholar

  • Domahs, F., Lochy, A., Eibl, G. & Delazer, M. (2004). Adding colour to multiplication: Rehabilitation of arithmetic fact retrieval in a case of traumatic brain injury. Neuropsychological Rehabilitation, 14(3), 303–328. https://doi.org/10.1080/09602010343000246 First citation in articleCrossrefGoogle Scholar

  • Domahs, F., Zamarian, L. & Delazer, M. (2008). Sound arithmetic: Auditory cues in the rehabilitation of impaired fact retrieval. Neuropsychological Rehabilitation, 18(2), 160–181. https://doi.org/10.1080/09602010701505648 First citation in articleCrossrefGoogle Scholar

  • Fasotti, L. (1992). Arithmetical word problem solving after frontal lobe damage: A cognitive neuropsychological approach. Amsterdam: Swets & Zeitlinger. First citation in articleGoogle Scholar

  • Ferro, J. M. & Silveira Botelho, M. A. (1980). Alexia for arithmetical signs. A cause of disturbed calculation. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 16(1), 175–180. https://doi.org/10.1016/s0010-9452(80)80032-3 First citation in articleCrossrefGoogle Scholar

  • Galfano, G., Rusconi, E. & Umiltà, C. (2003). Automatic activation of multiplication facts: Evidence from the nodes adjacent to the product. The Quarterly Journal of Experimental Psychology. A, Human Experimental Psychology, 56(1), 31–61. https://doi.org/10.1080/02724980244000332 First citation in articleCrossrefGoogle Scholar

  • Girelli, L., Bartha, L. & Delazer, M. (2002). Strategic learning in the rehabilitation of semantic knowledge. Neuropsychological Rehabilitation, 12(1), 41–61. https://doi.org/10.1080/09602010143000149 First citation in articleCrossrefGoogle Scholar

  • Girelli, L. & Delazer, M. (1996). Subtraction bugs in an acalculic patient. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 32(3), 547–555. First citation in articleCrossrefGoogle Scholar

  • Girelli, L., Delazer, M., Semenza, C. & Denes, G. (1996). The representation of arithmetical facts: Evidence from two rehabilitation studies. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 32(1), 49–66. First citation in articleCrossrefGoogle Scholar

  • Granà, A., Hofer, R. & Semenza, C. (2006). Acalculia from a right hemisphere lesion dealing with “where” in multiplication procedures. Neuropsychologia, 44(14), 2972–2986. https://doi.org/10.1016/j.neuropsychologia.2006.06.027 First citation in articleCrossrefGoogle Scholar

  • Hawes, Z., Sokolowski, H. M., Ononye, C. B. & Ansari, D. (2019). Neural underpinnings of numerical and spatial cognition: An fMRI meta-analysis of brain regions associated with symbolic number, arithmetic, and mental rotation. Neuroscience and Biobehavioral Reviews, 103, 316–336. https://doi.org/10.1016/j.neubiorev.2019.05.007 First citation in articleCrossrefGoogle Scholar

  • Hecaen, H., Angelergues, R. & Houillier, S. (1961). Les variétés cliniques des acalculies au cours des lésions retrorolandiques: Approche statistique du problême. Revue Neurologique (Paris), 105, 86–103. First citation in articleGoogle Scholar

  • Henschen, S. E. (1919). Über Sprach-Musik- und Rechenmechanismen und ihre Lokalisationen im Grosshirn. Zeitschrift für die gesamte Neurologie und Psychiatrie, 52, 273–298. First citation in articleCrossrefGoogle Scholar

  • Henschen, S. E. (1926). On the function of the right hemisphere of the brain in relation to the left in speech, music, and calculation. Brain, 49, 110–123. First citation in articleCrossrefGoogle Scholar

  • Hittmair-Delazer, M., Sailer, U. & Benke, T. (1995). Impaired arithmetic facts but intact conceptual knowledge – A single-case study of dyscalculia. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 31(1), 139–147. https://doi.org/10.1016/s0010-9452(13)80112-8 First citation in articleCrossrefGoogle Scholar

  • Hittmair-Delazer, M., Semenza, C. & Denes, G. (1994). Concepts and facts in calculation. Brain: A Journal of Neurology, 117, 715–728. https://doi.org/10.1093/brain/117.4.715 First citation in articleCrossrefGoogle Scholar

  • Ibrahimovic, N., Bulheller, S. & Häcker, H. (2002). Mathematiktest: Grundkenntnisse für Lehre und Beruf. Amsterdam: Swets and Zeitlinger. First citation in articleGoogle Scholar

  • Jurado, M. B.,& Rosselli, M. (2017). Automaticity of access to arithmetic knowledge in Alzheimer's disease and mild cognitive impairment. Psychology & Neuroscience, 10(1), 57–76. https://doi.org/10.1037/pne0000062 First citation in articleCrossrefGoogle Scholar

  • Kalbe, E., Brand, M. & Kessler, J. (2002). Zahlenverarbeitungs- und Rechentest – ZRT. Göttingen: Beltz Test. First citation in articleGoogle Scholar

  • Kashiwagi, A., Kashiwagi, T. & Hasegawa, T. (1987). Improvement of deficits in mnemonic rhyme for multiplication in Japanese aphasics. Neuropsychologia, 25(2), 443–447. https://doi.org/10.1016/0028-3932(87)90032-7 First citation in articleCrossrefGoogle Scholar

  • Kawashima, R., Okita, K., Yamazaki, R., Tajima, N., Yoshida, H., Taira, M. et al. (2005). Reading aloud and arithmetic calculation improve frontal function of people with dementia. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 60(3), 380–384. https://doi.org/10.1093/gerona/60.3.380 First citation in articleCrossrefGoogle Scholar

  • Kulason, K., Nouchi, R., Hoshikawa, Y., Noda, M., Okada, Y. & Kawashima, R. (2018). The Beneficial Effects of Cognitive Training With Simple Calculation and Reading Aloud (SCRA) in the Elderly Postoperative Population: A Pilot Randomized Controlled Trial. Frontiers in Aging Neuroscience, 10, 68. https://doi.org/10.3389/fnagi.2018.00068 First citation in articleCrossrefGoogle Scholar

  • Laiacona, M. & Lunghi, A. (1997). A case of concomitant impairment of operational signs and punctuation marks. Neuropsychologia, 35(3), 325–332. https://doi.org/10.1016/S0028-3932(96)00080-2 First citation in articleCrossrefGoogle Scholar

  • Lefevre, J.-A., Bisanz, J. & Mrkonjic, L. (1988). Cognitive arithmetic: Evidence for obligatory activation of arithmetic facts. Memory & Cognition, 16(1), 45–53. https://doi.org/10.3758/BF03197744 First citation in articleCrossrefGoogle Scholar

  • Lewandowski, M. & Stadelmann, E. (1908). Über einen bemerkenswerten Fall von Himblutung und über Rechenstörungen bei Herderkrankurg des Gehirns. Journal für Neurologie and Psychologie , 11, 249–265. First citation in articleGoogle Scholar

  • McCloskey, M. (1992). Cognitive mechanisms in numerical processing: Evidence from acquired dyscalculia. Cognition, 44(1–2), 107–157. First citation in articleCrossrefGoogle Scholar

  • McCloskey, M., Aliminosa, D. & Sokol, S. M. (1991). Facts, rules, and procedures in normal calculation: Evidence from multiple single-patient studies of impaired arithmetic fact retrieval. Brain and Cognition, 17(2), 154–203. https://doi.org/10.1016/0278-2626(91)90074-i First citation in articleCrossrefGoogle Scholar

  • McCloskey, M., Caramazza, A. & Basili, A. (1985). Cognitive mechanisms in number processing and calculation: Evidence from dyscalculia. Brain and Cognition, 4(2), 171–196. First citation in articleCrossrefGoogle Scholar

  • Messina, G., Denes, G. & Basso, A. (2009). Words and number words transcoding: A retrospective study on 57 aphasic subjects. Journal of Neurolinguistics, 22(5), 486–494. First citation in articleCrossrefGoogle Scholar

  • Miceli, G. & Capasso, R. (1999). Calculation and number processing. In G. DenesL. Pizzamiglioeds., Handbook of Clinical and Experimental Neuropsychology (S.583–612). London: Psychology Press. First citation in articleGoogle Scholar

  • Noel, M. P. & Seron, X. (1995). Lexicalization Errors in Writing Arabic Numerals – A Single-Case Study. Brain and Cognition, 29(2), 151–179. https://doi.org/10.1006/brcg.1995.1274 First citation in articleCrossrefGoogle Scholar

  • Noel, M.-P. & Seron, X. (1993). Arabic number reading deficit: A single case study or when 236 is read (2306) and judged superior to 1258. Cognitive Neuropsychology, 10(4), 317–339. https://doi.org/10.1080/02643299308253467 First citation in articleCrossrefGoogle Scholar

  • Nouchi, R., Taki, Y., Takeuchi, H., Nozawa, T., Sekiguchi, A. & Kawashima, R. (2016). Reading Aloud and Solving Simple Arithmetic Calculation Intervention (Learning Therapy) Improves Inhibition, Verbal Episodic Memory, Focus Attention and Processing Speed in Healthy Elderly People: Evidence from a Randomized Controlled Trial. Frontiers in Human Neuroscience, 10. https://doi.org/10.3389/fnhum.2016.00217 First citation in articleCrossrefGoogle Scholar

  • Pesenti, M., Seron, X. & van der Linden, M. (1994). Selective impairment as evidence for mental organisation of arithmetical facts: BB, a case of preserved subtraction? Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 30(4), 661–671. First citation in articleCrossrefGoogle Scholar

  • Semenza, C. (2019). I disturbi del sistema dei numeri e del calcolo. In G. DenesL. PizzamiglioC. GuarigliaS. CappaD. GrossiC. G. Luzzatti, Manuale di Neuropsicologia. Normalità e Patologia dei Processi Cognitivi. (S.349–371). Bologna: Zanichelli. First citation in articleGoogle Scholar

  • Semenza, C., Bencini, G. M. L., Bertella, L., Mori, I., Pignatti, R., Ceriani, F. et al. (2007). A dedicated neural mechanism for vowel selection: A case of relative vowel deficit sparing the number lexicon. Neuropsychologia, 45(2), 425–430. https://doi.org/10.1016/j.neuropsychologia.2006.07.006 First citation in articleCrossrefGoogle Scholar

  • Semenza, C., Grana, A. & Girelli, L. (2006). On knowing about nothing: The processing of zero in single- and multi-digit multiplication. Aphasiology, 20(9), 1105–1111. https://doi.org/10.1080/02687030600741659 First citation in articleCrossrefGoogle Scholar

  • Semenza, C., Meneghello, F., Arcara, G., Burgio, F., Gnoato, F., Facchini, S. et al. (2014). A new clinical tool for assessing numerical abilities in neurological diseases: Numerical activities of daily living. Frontiers in Aging Neuroscience, 6, 112. https://doi.org/10.3389/fnagi.2014.00112 First citation in articleCrossrefGoogle Scholar

  • Semenza, C., Miceli, L. & Girelli, L. (1997). A deficit for arithmetical procedures: Lack of knowledge or lack of monitoring? Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 33(3), 483–498. https://doi.org/10.1016/s0010-9452(08)70231-4 First citation in articleCrossrefGoogle Scholar

  • Seron, X. & Deloche, G. (1983). From 4 to four. A supplement to “From three to 3”. Brain: A Journal of Neurology, 106 (Pt 3), 735–744. https://doi.org/10.1093/brain/106.3.735 First citation in articleCrossrefGoogle Scholar

  • Siegler, R. S. (1988). Strategy choice procedures and the development of multiplication skill. Journal of Experimental Psychology. General, 117(3), 258–275. First citation in articleCrossrefGoogle Scholar

  • Sokol, S. M., McCloskey, M., Cohen, N. J. & Aliminosa, D. (1991). Cognitive representations and processes in arithmetic: Inferences from the performance of brain-damaged subjects. Journal of Experimental Psychology: Learning, Memory, and Cognition, 17(3), 355–376. https://doi.org/10.1037/0278-7393.17.3.355 First citation in articleCrossrefGoogle Scholar

  • van Harskamp, N. J. & Cipolotti, L. (2001). Selective impairments for addition, subtraction and multiplication. Implications for the organisation of arithmetical facts. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 37(3), 363–388. https://doi.org/10.1016/s0010-9452(08)70579-3 First citation in articleCrossrefGoogle Scholar

  • Venneri, A. & Semenza, C. (2011). On the dependency of division on multiplication: Selective loss for conceptual knowledge of multiplication. Neuropsychologia, 49(13), 3629–3635. https://doi.org/10.1016/j.neuropsychologia.2011.09.017 First citation in articleCrossrefGoogle Scholar

  • Whetstone, T. (1998). The representation of arithmetic facts in memory: Results from retraining a brain-damaged patient. Brain and Cognition, 36(3), 290–309. https://doi.org/10.1006/brcg.1998.0997 First citation in articleCrossrefGoogle Scholar

  • Willmes, K. (2008). Chapter 17 Acalculia. In Handbook of Clinical Neurology (Bd. 88, S.339–358). London: Elsevier. https://doi.org/10.1016/S0072-9752(07)88017-1 First citation in articleCrossrefGoogle Scholar

  • Zamarian, L., Delazer, M., Ehling, R., Pertl, M.-T., Bsteh, G., Wenter, J. et al. (2019). Improvement of medical judgments by numerical training in patients with multiple sclerosis. European Journal of Neurology, 26(1), 106–112. https://doi.org/10.1111/ene.13778 First citation in articleCrossrefGoogle Scholar

  • Zamarian, L., Ischebeck, A. & Delazer, M. (2009). Neuroscience of learning arithmetic – Evidence from brain imaging studies. Neuroscience and Biobehavioral Reviews, 33(6), 909–925. https://doi.org/10.1016/j.neubiorev.2009.03.005 First citation in articleCrossrefGoogle Scholar

  • Zamarian, L., Karner, E., Benke, T., Donnemiller, E. & Delazer, M. (2006). Knowing 7 × 8, but not the meaning of “elephant”: Evidence for the dissociation between numerical and non-numerical semantic knowledge. Neuropsychologia, 44(10), 1708–1723. https://doi.org/10.1016/j.neuropsychologia.2006.03.032 First citation in articleCrossrefGoogle Scholar

  • Zamarian, L., López-Rolón, A. & Delazer, M. (2007). Neuropsychological case studies on arithmetic processing. In D. B. BerchM. M. M. MazzoccoEds., Why is math so hard for some children? The nature and origins of mathematical learning difficulties and disabilities. (S.245–263). Baltimore: Paul H Brookes Publishing. First citation in articleGoogle Scholar

  • Zamarian, L., Stadelmann, E., Nürk, H.-C., Gamboz, N., Marksteiner, J. & Delazer, M. (2007). Effects of age and mild cognitive impairment on direct and indirect access to arithmetic knowledge. Neuropsychologia, 45(7), 1511–1521. https://doi.org/10.1016/j.neuropsychologia.2006.11.012 First citation in articleCrossrefGoogle Scholar

  • Zaunmüller, L., Domahs, F., Dressel, K., Lonnemann, J., Klein, E., Ischebeck, A. et al.(2009). Rehabilitation of arithmetic fact retrieval via extensive practice: A combined fMRI and behavioural case-study. Neuropsychological Rehabilitation, 19(3), 422–443. https://doi.org/10.1080/09602010802296378 First citation in articleCrossrefGoogle Scholar