Neuroscience and Biobehavioral Reviews 32 (2008) 1361–1372

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Neuroscience and Biobehavioral Reviews
journal homepage: www.elsevier.com/locate/neubiorev

Review

Visualizing numbers in the mind’s eye: The role of visuo-spatial processes in numerical abilities
Maria Dolores de Hevia a,b,*, Giuseppe Vallar a,c, Luisa Girelli a
a

` Universita degli Studi di Milano-Bicocca, Italy Harvard University, USA c Laboratorio di Neuropsicologia, IRCCS Istituto Auxologico Italiano, Milano, Italy
b

A R T I C L E I N F O

A B S T R A C T

Keywords: Numerical cognition Arithmetical abilities Visuo-spatial representation of numbers

In the study of numerical and arithmetical abilities, there is compelling evidence demonstrating that number and space representations are connected to one another. Historically the first source of support came more than a century ago, when Galton’s investigations on mental imagery suggested that the internal representation of numbers may evoke a stable, linear space. In the past few decades, empirical evidence lent further support to the hypothesis that numerical representation is spatially coded into a non-verbal ‘mental number line’, which in turn lead to considering this representation as the core of number meaning. Visuo-spatial processing is intuitively involved in various aspects of number processing and calculation: For instance, the meaning of a digit in a multi-digit number is coded following spatial information, given its association to its relative position within the number; similarly, to solve a complex written multiplication one has to know the correct location of the intermediate results. In this review behavioral, neuropsychological, and neuroimaging data concerning the close relationship between numerical abilities and visuo-spatial processes are considered. ß 2008 Elsevier Ltd. All rights reserved.

Contents 1. Numbers and visuo-spatial processing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1. The mental number line hypothesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2. Experimental paradigms and effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3. Neuropsychological evidence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4. Neuro-anatomical basis: lesion and neuroimaging data. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Calculation and visuo-spatial processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. The hypothesis of a visuo-spatial medium for arithmetic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Experimental paradigms and effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Neuropsychological evidence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Neural correlates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1362 1362 1362 1365 1366 1367 1367 1368 1369 1369 1370 1370 1370

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In the study of numerical and arithmetical abilities, there is compelling evidence demonstrating that number and space

* Corresponding author at: Harvard University, Department of Psychology, 33 Kirkland Street, Cambridge, MA 02138, United States. E-mail address: dehevia@wjh.harvard.edu (M.D. de Hevia). 0149-7634/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.neubiorev.2008.05.015

representations are connected to one another (for recent reviews, see de Hevia et al., 2006b; Fias and Fischer, 2005; Hubbard et al., 2005). Historically, the first source of support came more than a century ago, when Galton’s investigations on mental imagery suggested that the internal representation of numbers may evoke a stable, linear space (Galton, 1880). The so-called ‘number forms’ reflect a series of visuo-spatial properties associated with

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Fig. 1. A ‘number form’. Illustration of the mental image evoked by a subject when thinking about numbers (from Galton, 1880).

numerical information, such as spatial orientation, color, and brightness, which give rise to particular configurations occupied by numbers (Galton, 1880) (see Fig. 1). Although originally anecdotal, the intuition that the mental representation of numbers contains a series of visuo-spatial properties has later found systematic support (Seron et al., 1992). It has, at present, a major impact on cognitive models of numerical processing (Dehaene, 1992; Dehaene et al., 2003). In fact, some individuals report the deployment of a visuo-spatial internal space when they represent numerical information, and perform mental arithmetic. Interestingly, they claim that these mental images are not the product of mathematical instruction at school, reflecting instead the spontaneous process of visualizing numbers (Sagiv et al., 2006; Seron et al., 1992). In the past few decades, empirical evidence lent further support to the hypothesis that numerical representations are spatially coded into a non-verbal ‘mental number line’. This view, in turn, leads to considering such a representation the core of number meaning (Dehaene, 1992). Visuo-spatial processing is intuitively involved in various aspects of number processing and calculation: For instance, the meaning of a digit in a multi-digit number is coded following spatial information, given its association to its relative position within the number. Similarly, in order to solve a complex written multiplication, one has to know the correct location of the intermediate results. In this review the behavioral, neuropsychological, and neuroimaging evidence concerning the close relationship between numerical abilities and visuo-spatial processes is considered. 1. Numbers and visuo-spatial processing 1.1. The mental number line hypothesis There is wide evidence supporting the view that the representation of numerical magnitude is mapped onto an analogue ‘mental number line’. Early reports suggested that the representation of numbers is analogue, with subjects adding portions of the number line when performing a mental addition (Moyer and Landauer, 1967; Restle, 1970). Nowadays, the hypothesis of a spatial numerical representation is central to models of numerical cognition (in particular, the ‘Triple Code’ model, Dehaene, 1992; Dehaene et al., 2003), which postulate that among the verbal– auditory (e.g., ‘twenty-seven’), and the Arabic-visual (e.g., ‘27’)

codes, in which numbers can be mentally represented, subjects also activate an analogue-quantity code, which contains the semantic information of a number. At this level, the numerical representation is non-verbal, and only approximate, consisting of variable distributions of activation along the spatial ‘mental number line’ (Dehaene et al., 2003). The ‘mental number line’, in the form of a mental continuum logarithmically compressed (see Gallistel and Gelman, 2000, 1992, for the view of an analogue linear representation of magnitude), provides the information of numerical magnitude (Dehaene et al., 2003; Restle, 1970). This proposal was initially supported by two psychophysical effects that characterize the comparison judgment between two numerical values. First, the ‘distance effect’ (i.e., subjects are faster and more accurate in comparing two numbers the farther apart they are), and second, the ‘size effect’ (i.e., by keeping the numerical distance between two numbers constant, the performance is faster, and more accurate, with smaller than with larger numbers) (Moyer and Landauer, 1967). These effects characterize judgments of inequality within other continuous dimensions, such as brightness, or the length of a line, suggesting that the internal representation of numerical magnitude is not digital, but analogue (Moyer and Landauer, 1967), and that, as a consequence, the subjective difference between two numerical magnitudes obeys the Weber–Fechner law (Dehaene, 2003; Nieder and Miller, 2003). The distance and size effects have been described also with nonsymbolic numbers, such as dot patterns, both in adults and children (Buckley and Gillman, 1974; Temple and Posner, 1998), suggesting that the number line contains an abstract representation of magnitude. Moreover, there is evidence that the numerical discrimination abilities present in non-verbal animals (Gallistel and Gelman, 2000, for a review), and in pre-verbal human infants, as young as 6-month-old (Feigenson et al., 2004, for a review), are governed by the same properties (i.e., the success of discrimination depends on the ratio between the two quantities). These findings support the hypothesis that the number line is a natural endowed capacity of representing and discriminating numbers (Spelke and Dehaene, 1999). Accordingly, the ‘mental number line’ representation provides the capacity of understanding a numerical quantity in an approximate way. Furthermore, a growing body of empirical findings suggests that this internal code consists of an oriented spatial medium, in such a way that increasing numerical magnitudes are represented in ascending order, and, as a consequence, each number is associated with a specific spatial location (Dehaene et al., 1993). 1.2. Experimental paradigms and effects The spatial orientation of the representational continuum – within the hypothesis of the ‘mental number line’ representation – is qualified as left-to-right oriented by the observation of a stimulus–response compatibility effect that emerges in numerical classification tasks: The ‘SNARC’ effect (Spatial Numerical Association of Response Codes) refers to the fact that subjects respond faster to smaller numbers with the left than with the right hand, and to larger numbers with the right hand (Dehaene et al., 1993; Fias et al., 1996) (Fig. 2). This phenomenon suggests that the numerical representation accessed in these tasks contains spatial information. The SNARC effect may be regarded as a sort of Simon effect (Gevers et al., 2005; Keus and Schwarz, 2005; but see Mapelli et al., 2003), in the form of a dimensional overlap between the (implicit) relative position of the magnitude on the ‘mental number line’ (in representational space), and the location of the manual response to the left and right sides (in physical egocentric space).

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Fig. 2. (A) The classical experimental setting in which the SNARC effect is observed. In a numerical classification task, smaller magnitude numbers elicit left-sided responses, larger magnitude numbers right-sided responses. (B) Expected differences in RT (dRT) between right, and left hand responses, as a function of the digit to be classified.

The implicit association of numbers to spatial locations can be demonstrated in subjects who do not consciously experience the phenomenon. Importantly, the SNARC effect may be triggered automatically, being present whether or not the numerical magnitude is intentionally processed: It has been obtained when participants simply need to categorize numbers by their identity (Dehaene and Akhavein, 1995; Zhou et al., 2008); it also emerges in parity judgment tasks, where subjects are required to classify numbers as even or odd (Dehaene et al., 1993; Fias et al., 1996; Ito and Hatta, 2004); in phoneme detection tasks, where numbers are classified as containing a specific phoneme in the corresponding number word (Fias et al., 1996); or in orientation judgments, where subjects need to process the spatial orientation of a figure superimposed on a single Arabic digit (Fias et al., 2001). The SNARC effect has been systematically replicated in a variety of conditions: It can be obtained for different notations (Arabic vs. verbal; Fias, 2001), and with non-symbolic number (dice dot patterns; Nuerk et al., 2005). The effect has also been described for different modalities of presentation (visual vs. auditory, see Nuerk et al., 2005), and it extends to two-digit numbers (Brysbaert, 1995; Dehaene et al., 1990; Zhou et al., 2008). Overall, these observations support the view that the ‘mental number line’ is to be conceived as an amodal, and abstract visuo-spatial representation of the numerical magnitude. The mapping of numbers into specific spatial locations has been observed to be a flexible and context-dependent process. In particular, it has been shown that the association of a number with a spatial location is not absolute, depending instead on the relative magnitude; thus, the same number considered in different numerical intervals would be associated with different spatial positions (e.g., the number ‘4’ in intervals [0–4] vs. [4–9], Dehaene et al., 1993; Fias et al., 1996). Furthermore, the advantage of responding to small numbers with the left hand and to large numbers with the right hand is related neither to handedness, nor to hemispheric lateralization (Dehaene et al., 1993). The direction along which magnitudes are arranged into the horizontal dimension, however, seems to be shaped by reading

habits: left-to-right vs. right-to-left (Dehaene et al., 1993; Zebian, 2005). In fact, in the work by Dehaene et al. (1993), Iranian participants show a weaker SNARC effect than French participants, the former approaching a significant reversed SNARC effect. Similarly, in Lebanese participants, comparing two visually presented Arabic digits, an advantage when numbers are presented oriented from right-to-left (e.g., 9 1), in contrast to a left-to-right orientation (e.g., 1 9) has been found (Zebian, 2005). However, contrasting evidence is also on record: Japanese participants, whose reading habits predict an association between a top location with a small number and a low location with a large number, exhibit the reverse pattern of association during a parity judgment task (Ito and Hatta, 2004). Moreover, the preferred spatial orientation might also depend on the specific numerical notation in which numbers are presented. For instance, native speakers of Chinese showed a horizontal left-to-right advantage for Arabic digits, whereas for numbers written with Chinese characters, which appear predominantly with a vertical top-tobottom directionality, a top-small and bottom-large association was found to facilitate processing (Hung et al., 2008). The evidence that the specific orientation of this numerical continuum is shaped by cultural constraints suggests that the spatial properties are acquired during school years, with the acquisition of reading and writing habits as the main determinants. In fact, the SNARC effect, assessed by the parity judgment task, has been found to emerge in children after 3rd grade (9–10 year-old) (Berch et al., 1999). Notwithstanding the apparent late appearance of spatial properties in numerical processing, as indexed by the SNARC effect, it should be noted that the automatic access to magnitude information from Arabic symbols, as assessed by a numerical-Stroop paradigm, emerges from age 10 (Girelli et al., 2000). It is thus likely that the spatial organization of numerical magnitude may be present even earlier in development. Importantly, once the spatial mapping of numbers has been established, the spatial information is implicit in the processing of a number (Dehaene et al., 1993; Fias, 2001; Fias et al., 1996). One may suggest that the initial mapping of numbers onto space might be partially triggered by the exposure to measurement devices, such as rulers, or that it critically depends on extensive experience with number in the visual modality (Cooper, 1984; Simon, 1997). This view has been recently challenged in a study with congenitally or early blind participants, who show a SNARC effect as strong as a sighted control group, in a series of bimanual classification tasks of verbal numbers presented auditorily (Castronovo and Seron, 2007). As discussed earlier, the SNARC effect has typically been found in numerical classification tasks requiring bimanual responses, leading to an association between smaller numbers with the left side and larger numbers with the right side of space (e.g., Dehaene et al., 1993; Dehaene et al., 1990; Fias, 2001; Fias et al., 1996). However, although the spatial arrangement might have a left-toright orientation by default, mainly determined by scanning habits (Chokron and Imbert, 1993), the assignment of a spatial code to a number has proved to be a flexible phenomenon. For instance, when numbers are visualized on a clock face, a reversed SNARC effect can be obtained: If subjects are simply asked to classify numbers as hours of the day coming before or after six o’clock, faster responses to small numbers with the right hand, and to large ¨ numbers with the left hand, can be obtained (Bachtold et al., 1998). Although it is worth noticing that in this study participants were explicitly required to evoke the corresponding mental image of an analogical clock, this finding suggests that the spontaneous mapping of numbers into an internal visuo-spatial representation may be subject to the specific context into which numbers are manipulated. Additional evidence supports the view that the left-

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to-right oriented ‘mental number line’ is not the only representation which leads to visuo-spatial associations. In fact, when subjects use all their fingers in a task that requires to identify Arabic digits (each digit is assigned to a unique finger), they show an advantage for small numbers responded to with the right hand, provided that the specific digit-finger mapping imposed in the task mirrors the personal finger counting strategies (Di Luca et al., 2006). These studies provide evidence of further spatial frames onto which numbers might be mapped, such as a finger counting map, which may even overcome the canonical left-to-right orientation of the ‘mental number line’. In addition, the spatial representation of the ‘mental number line’ is not confined to the horizontal dimension. In fact, the specific mapping of the responses has proved to be related to the emergence of spatial–numerical compatibility effects. When participants are required to perform the numerical classification task with key responses arranged in a top-down fashion, a vertical SNARC effect is observed, where smaller (larger) numbers are preferentially associated to low (high) locations (Ito and Hatta, 2004; Schwarz and Keus, 2004). Moreover, the response advantage driven by the numerical information is not specific to bimanual responses, being also present with responses involving eye movements (Fischer et al., 2003): When subjects are required to detect a stimulus in the right or left sides of the computer screen, there is an advantage in detecting left-sided stimuli when a smallmagnitude digit (i.e., 1, 2) is previously presented in the centre of the screen, while right-sided stimuli are primed by a largermagnitude digit (i.e., 8, 9) (Fischer et al., 2003). These shifts of attention towards the left or the right sides of space are also found along the vertical dimension, with saccadic responses towards bottom locations being faster for smaller numbers, saccadic responses towards top locations faster for larger numbers (Schwarz and Keus, 2004). Similar lateralized effects, which emerge in the processing of numerical information, have been observed in a variety of different experimental paradigms, such as naming (Brysbaert, 1995; Zebian, 2005), unimanual pointing (Fischer, 2003; Ishihara et al., 2006), and numerical classification tasks with pedal responses (Schwarz ¨ and Muller, 2006). In these studies, participants show effects of congruency between the numerical and the spatial information. In naming tasks, subjects show faster responses when the numerical

display reflects the preferred orientation [left-to-right ‘1 9’ (Brysbaert, 1995), or right-to-left ‘9 1’ (Zebian, 2005)]. Similarly, in the performance of pointing tasks participants are faster in pointing towards a left location when a smaller-magnitude number has been presented, and towards a right location with the preceding presentation of a larger-magnitude number (Fischer, 2003; Ishihara et al., 2006). Finally, the SNARC effect is present also when participants provide bipedal responses in a numerical ¨ classification task (Schwarz and Muller, 2006). Recently, it has been shown that the spontaneous mapping of information into representational space is not confined to numerical information. In particular, a stimulus–response compatibility effect has been described in the classification of ordered non-numerical stimuli, whether or not the order information is the attended dimension: When subjects classify a letter of the alphabet (or a month of the year), as coming before or after a specific letter (month), SNARC-like effects are observed: Letters coming before the letter (month) of reference are classified faster with the left hand than with the right hand, the reverse being true for letters (months) coming after the letter (month) of reference. Critically, the spatial-congruency effects are present even when these stimuli are classified according to a property unrelated to the ordinal meaning, such as in a phoneme monitoring task (Gevers et al., 2003; Gevers et al., 2004; but see Dehaene et al., 1993, for a null effect). This evidence undermines the hypothesis that the mapping of the ‘mental number line’ representation into a spatial dimension derives from the meaning of quantity, rather than from the ordinal meaning. It has been also suggested, however, that numerical magnitudes are mapped onto a continuous space, whereas for other ordered sequences the spatial mapping corresponds to categorical (left/ right) positions (Ishihara et al., 2006; Zorzi et al., 2006). Even if this were the case, it still remains unclear whether a continuous spatial mapping is specific to the numerical domain, since it has been observed that other continua, such as the pitch height, show spatial compatibility effects along both the vertical and the horizontal dimensions (Rusconi et al., 2006). In particular, when participants are asked to compare the pitch of variable frequency tones with a fixed reference, by providing bimanual responses, they show faster responses in responding to higher tones with the top, and the right keys, and to lower tones with the bottom, and the left, keys;

Fig. 3. (A) Illustration of the bisection paradigm with numerical material. Participants are asked to set the subjective midpoint of horizontal lines, flanked by digits. (B) Mean spatial biases exhibited in the bisection task: rightward biases are observed when the larger digit is on the right-hand side, leftward biases when the larger digit is on the lefthand side of the line (reprinted from de Hevia et al., 2006b, with permission).

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moreover, the same effects are observed when participants classify stimuli on the basis of the musical instrument producing the sounds, suggesting an automatic spatial mapping of tones (Rusconi et al., 2006). A number of studies focus on the behavioral effects observed when numerical and visuo-spatial processing are concurrently engaged in a given task. Several numerical effects have been described using a variety of visuo-spatial paradigms, in which the numerical information is irrelevant, but still affects the performance in a visuo-spatial task. For instance, the task of manual bisection of a segment has been used by means of flanking each side of horizontal lines by numbers, resulting in the observation of systematic spatial biases towards the larger magnitude number (de Hevia et al., 2006a; Fischer, 2001) (Fig. 3). The effect of numbers on the perception of a line has been interpreted as if subjects represent numerical flankers demarcating a specific portion of the ‘mental number line’ (Fischer, 2001), or as if subjects exhibit spatial biases towards the larger magnitude, as a result of an overestimation of the lateral extent closer to the larger digit (de Hevia et al., 2006a). Similarly, left- or rightward spatial biases have been reported when the stimulus to bisect is a string of identical smaller or larger numbers, respectively, in Arabic as well as in verbal notation, interpreted on the basis of the SNARC effect (Calabria and Rossetti, 2005; Fischer, 2001). This automatic activation of left/right spatial codes can actually guide our attention towards the left- or righthand sides of space, as it has been shown in detection tasks using irrelevant digits as fixation points (Fischer et al., 2003). Moreover, motor performance is modulated by numerical magnitude information: Motor planning and execution towards the left- or the right-hand sides of space are influenced by number magnitude (Fischer, 2003; Ishihara et al., 2006). Besides the automatic activation of left-oriented vs. rightoriented spatial codes, numerical magnitude can influence spatial processing by inducing a sort of ‘cognitive’ illusions (de Hevia et al., 2006a). In particular, underestimations and overestimations of a spatial extension have been described by using a length reproduction task, in which participants are required to reproduce the space between two, previously presented, small or large Arabic numbers, respectively (de Hevia et al., 2007). In this study, participants underestimate the spatial gap between two smaller magnitude numbers (e.g., ‘1 1’). Conversely, the spatial extent is overestimated when two large magnitude numbers (e.g., ‘9 9’) are used as flankers (de Hevia et al., 2007). This observation is consistent with the idea that a given numerical magnitude is internally represented by a spatial extension (Restle, 1970). Recently, aperture and closure grasping movements have been found to be influenced by the magnitude information of numerical stimuli (Andres et al., 2004). In this study, participants are required to perform a closure or opening grip, depending on the parity of a visually presented digit. Electromyographic recordings of hand muscles indicate that smaller digits speed up grip closure, larger digits grip opening (Andres et al., 2004). These interference effects may be interpreted in the context of an integrative view: Estimations of magnitude, time, and space are computed by a general magnitude system, which represents the essential information guiding the sensorimotor transformations required for action (Walsh, 2003). 1.3. Neuropsychological evidence The idea that number and space are intimately related to one another found early support from neuropsychological studies, showing that the parietal lobe, a long known basic neural underpinning of spatial processing (Critchley, 1953; Jewesbury,

1969), is also involved in numerical processing. Parietal damage is frequently associated to acalculia, a deficit of the numerical domain of cognition, which may be independent of other cognitive ´ disorders (Hecaen et al., 1961; Henschen, 1919). A striking instance of the putative relationship between processing of space and number may be provided by the Gerstmann’s syndrome, a four-symptom disorder, typically associated with damage to the inferior parietal lobule (angular gyrus) of the left hemisphere. The syndrome comprises acalculia, agraphia, finger agnosia, and left-right disorientation (Gerstmann, 1940). The syndrome has a definite value for anatomical localization, suggesting a lesion of the inferior-posterior parietal lobe of the left hemisphere (Morris et al., 1984; Roeltgen et al., 1983; Strub and Geschwind, 1983). The functional unity of the syndrome, however, and the hypothesis of a single pathological mechanism underlying the four components of it have been long criticized (reviews and discussion in Benton, 1992; Critchley, 1966; Morris et al., 1984). The main argument, mainly developed in the 1960s by the north-American neuropsychologist Arthur Benton on the basis of the investigation of large series of brain-damaged patients (e.g., Benton, 1961), is that the four symptoms of the syndrome may occur in isolation. The association, accordingly, has a relevant anatomical value, suggesting a focal left posterior parietal lesion, but is not functionally relevant: the syndrome is anatomical, not functional (Vallar, 2000). Critically for the present review, the hypothesis that the tetrad of symptoms characterizing the Gerstmann syndrome share a common underlying deficit of visuo-spatial nature (reviews in Critchley, 1966; Vallar, 2007) has been revived in recent years. On the basis of the investigation of individual left-brain damaged patients with Gerstmann syndrome, suggestions have been made that the core impairment may concern difficulties in deriving the relative position of an object along the horizontal axis (Gold et al., 1995), or the mental transformation of visual images (e.g., rotation, translation) (Mayer et al., 1999; see also Carota et al., 2004). Moreover, the performance of 5- and 7-year-old children in tests assessing finger representation, left–right orientation, constructional abilities, and handwriting, is an excellent predictor of ¨ arithmetical skills, but not of verbal performance (Noel, 2005). More recent evidence for a fundamental association between number and space comes from studies assessing number processing in brain-damaged patients suffering from the syndrome of unilateral spatial neglect, that is more frequent and severe after a right hemispheric lesion, involving the left, contralateral, part of space (Vallar, 1998). The deficit consists of the inability to explore the side of space contralateral to the side of the lesion, and to report stimuli presented in that portion of space (Bisiach and Vallar, 2000). Critical to the present review is the fact that unilateral spatial neglect extends to the scanning of mental images generated by the patient (Bisiach and Luzzatti, 1978). With regard to numerical processing, when right-brain-damaged patients with neglect are asked to compare numbers with a reference one, shown centrally at fixation, their latencies are increased for those located to the immediate ‘left’ of the reference, along the ‘‘mental number line, such as ‘‘4’’ vs. a reference number ‘‘5’’. This imagery deficit extends to the left-sided positions of the hours onto an imagined clockface, with slower latencies to hours such as ‘‘9’’, and is not found in right-brain-damaged patients without neglect (Vuilleumier et al., 2004). These findings support the hypothesis that the number comparison task invokes an internal space of magnitude, oriented from left-to-right. In patients with left spatial neglect, the left side of such a representation may be not available for numerical processing. In sum, a unilateral impairment of spatial representation and attention (in the absence of primary numerical deficits or acalculia) may affect performance in some numerical

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tasks. This suggests that spatial representations may contribute to aspects of numerical processing. The task recently exploited for the assessment of the ‘‘mental number line’’ representation is the numerical bisection task, which consists in detecting the midpoint of a numerical interval (e.g., which is the central number between ‘‘2’’ and ‘‘8’’?). This task is supposed to rely explicitly on the representation of the ‘‘mental number line’’ (Dehaene, 1992; but see Nuerk et al., 2002). Accordingly, performance should primarily reflect visuo-spatial internal representations. Some studies (Zorzi et al., 2006; Zorzi et al., 2002) have argued that, when assessed by this task, the performance of brain-damaged patients with left neglect parallels the rightward error found in the bisection of physical lines (Heilman and Valenstein, 1979; Schenkenberg et al., 1980), by showing a displacement of the numerical centre towards the right side, namely the larger number. Double dissociations between the bisection of physical lines vs. numerical imagined lines are also on record, however, with patients being selectively impaired only in one of these tasks (Doricchi et al., 2005; Rossetti et al., 2004). These findings extend to the spatial representations of numbers the distinction between left neglect for objects in extra-personal space vs. in internally generated visuo-spatial mental images (Anderson, 1993; Bisiach and Luzzatti, 1978; Guariglia et al., 1993). Notwithstanding a defective processing of the left side of the representation of the ‘mental number line’, right-brain-damaged patients with left neglect may show a SNARC effect, as assessed by a task in which numbers are classified according to their parity with left-right unimanual responses (Priftis et al., 2006). This finding suggests that a left-to-right visuo-spatial numerical representation is still preserved in brain-damaged patients with left neglect. These patients, however, show impairment when the task requires a more explicit processing (Priftis et al., 2006). More generally, these findings are in line with the view that the core deficit of the neglect syndrome concerns perceptual awareness of left-sided, contralesional, representations (e.g., Berti, 2002). Furthermore, manipulations that transiently ameliorate a number of manifestations of the syndrome of spatial neglect (i.e., the prism adaptation procedure, see review in Rossetti and Rode, 2002) also improve the performance of patients with left neglect in the number bisection task (Rossetti et al., 2004). This finding suggests that sensorimotor transformations operating in the visuo-spatial domain are able to exert an influence on higher cognitive abilities, such as the internal representations of numerical magnitude, and further support their spatial nature. 1.4. Neuro-anatomical basis: lesion and neuroimaging data The view of a functional interaction between numerical and spatial processes, suggested by the previously reviewed evidence, is further supported by the partial overlapping of the posterior

parietal areas devoted to the processing of either types of information. Neuropsychological studies suggest that deficits in numerical processing may involve verbal vs. quantity numerical representations. Damage to the parietal lobe is usually associated to a deficit in quantitative tasks that tackle the internal manipulation of quantity, such as magnitude comparison, estimations of numerosity, and bisection of numerical intervals, while other language-related abilities, such as counting, and retrieval of arithmetic facts, are well preserved (Dehaene and Cohen, 1997; Delazer and Benke, 1997; Delazer et al., 2006a,b; Lemer et al., 2003). As evidence for such a dissociation, an aphasic patient affected by a left fronto-temporal atrophy was more impaired in multiplication fact retrieval (highly dependent on rote verbal memory), than in subtraction (primarily solved via non-verbal quantity meaning). The patient compared and calculated with large nonsymbolic quantities (arrays of dots) better than with tasks requiring verbal counting (Lemer et al., 2003). On the other hand, a patient who presented with a Gerstmann’s syndrome following a left parietal ischemic lesion, was more deteriorated in the manipulation of non-symbolic quantities and in subtraction, than in multiplication and counting procedures (Lemer et al., 2003). These dissociations between quantity and verbal numerical processes support the view of a basic distinction, within numerical processing, between a verbal system involving the left frontal and temporal (language) regions, and a non-verbal quantity system, based on the left and right intraparietal regions (Dehaene et al., 2003). The participation of specific brain regions to numerical processing may be modulated by practice. In fact, one study (Delazer et al., 2003) has shown, during a training session of multiplication facts, a shift of the focus of activation from the intraparietal sulcus to the angular gyrus (see however Rickard et al., 2000, for contrasting evidence on the activation of the angular gyrus in an arithmetic task). In the last decade, a large number of brain imaging studies have attempted to localize the brain regions involved in the processing of numerical information. Early functional-anatomical models suggested a role of the bilateral posterior parietal regions for the representation of numerical information (Dehaene and Cohen, 1995). More recent studies have refined, and further specified, the regions involved in the processing of number magnitude. PET studies show posterior parietal activations in simple numerical tasks, such as single digits multiplication, comparison, naming, and subtraction (Dehaene et al., 1996; Pesenti et al., 2000; Zago et al., 2001). fMRI studies reveal that manipulation of numerical information leads to an activation of the posterior-inferior parietal lobule (Chochon et al., 1999; Pinel et al., 2001). The specialized role of the posterior parietal cortex for numerical processing is supported by studies showing that the intraparietal sulcus (IPS) is activated when participants are engaged in subtraction

Fig. 4. Bilateral parietal network involved in numerical processing. A bilateral-intraparietal system may be devoted to the more abstract representation of quantity (grey), the left angular gyrus to verbal numerical representations (black), and a bilateral posterior-superior parietal system to spatial and non-spatial attention (cross-hatched). (Adapted from Dehaene et al., 2003).

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problems with Arabic numbers, among a variety of tasks including pointing, visual saccades, phoneme detection, and attention (Simon et al., 2002). In fact, a domain-specific localization hypothesis for numerical processing has been proposed, according to which the horizontal segment of the intraparietal sulcus (IPS), frequently related to visuo-spatial processing, is involved in the coding of numerical magnitude (Dehaene et al., 2003) (Fig. 4). In line with this view, a bilateral region in the horizontal IPS is activated in a greater extent when participants are involved in a detection task with Arabic numbers, in comparison to the presentation of letters or colors (Eger et al., 2003; but see contrasting evidence in Fias et al., 2007, and in Shuman and Kanwisher, 2004). Moreover, the horizontal IPS appears to be sensitive to the numerical distance effect, with the numerical comparison of closer digits leading to a higher degree of parietal activation than that of digits farther apart (Pinel et al., 2001). Similar activations have been obtained with passive viewing tasks (Piazza et al., 2004, 2007). The activation of the IPS is stronger in approximate than in exact calculation problems, supporting its role in the representation of numerical quantity (Dehaene et al., 1999). In line with these findings, more IPS activation is observed during subtraction than during multiplication (Chochon et al., 1999). The left IPS is activated by comparison judgments between symbolic (Arabic numbers), and non-symbolic (lines and angles) magnitudes (Fias et al., 2003). A recent study has shown a bilateral activation of the IPS for the estimation of discrete non-symbolic numerosities, both in sequential (temporal) and in simultaneous (visuo-spatial) presentations, compared to the estimation of analogue quantity (i.e., extension) (Castelli et al., 2006). These findings suggest the existence of a number-specific region in the parietal lobe. Additional converging evidence for the role of the posterior parietal regions, bilaterally, in basic number processing comes from recent studies using the rTMS technique. In particular, the participants’ performance in the standard numerical comparison task is disrupted after bilateral stimulation of the angular ¨ gyrus (Gobel et al., 2001), and of the left inferior parietal lobule (Sandrini et al., 2004). Finally, stimulation of the right parietal cortex affects performance in a numerical bisection task, shifting ¨ rightwards the numerical midpoint (Gobel et al., 2006; Oliveri et al., 2004). In monkeys trained to perform a numerical matching task, cells both in the lateral prefrontal cortex and in the IPS selectively respond to numerosity (Nieder and Miller, 2004). Importantly, IPS neurons require less time than those in the prefrontal cortex to become selective to numerosity, and their response adjustment is increasingly imprecise as numerosity increases. This response change follows the Weber-fraction, and thus mirrors the internal representation of magnitude (Nieder and Miller, 2004; Nieder and Miller, 2003). Finally, the level of abstraction of these numerosityselective neurons is demonstrated by the finding that, although in the monkey’s cortex the codification of number is segregated for spatial (simultaneous) and temporal (sequential) visual presentations, a common neural population ultimately encodes a more abstract quantity representation, irrespective of their numerical format (Nieder et al., 2006). To further investigate the possibility of numerosity ‘tuning’ in humans, the fMRI adaptation paradigm has been employed (Piazza et al., 2004; Shuman and Kanwisher, 2004). In these studies, the fMRI response, in brain areas supposed to process the quantity dimension, is expected to be lower for repeated stimuli, due to neural adaptation, than for stimuli changing in quantity. Consistent with the hypothesis that the horizontal segment of the IPS processes number, activation is attenuated with repeated presentation of the same numerical quantity conveyed by an Arabic

symbol, or by a number word (Naccache and Dehaene, 2001). Similar adaptation effects occur during the presentation of dots arrays with the same quantity, leading to an increased activity in the IPS bilaterally, when new numerosities are presented (Piazza et al., 2004). Moreover, a cross-notational adaptation effect between symbolic (digits) and non-symbolic (arrays of dots) number has been found (Piazza et al., 2007). Recent evidence from 4-year-old children (Cantlon et al., 2006) further supports the hypothesis that the IPS is implicated in a notation-independent representation of numerical magnitude (Dehaene et al., 1998). However, while the evidence is accumulating in support for the activation of the IPS in number processing, the hypothesis that its horizontal segment is specific for numbers has been recently challenged. In particular, when presenting non-symbolic numerical information, a significant involvement of the IPS is found, although not higher than the activation observed in the same area for color judgments. These results suggest that the IPS participates in processes concerned not only with number processing, but also with the analysis of other types of information. These results challenge the hypothesis of a single, domain-specific, region in the IPS that underlies both symbolic and non-symbolic number processing (Shuman and Kanwisher, 2004). In fact, parallel to the behavioral evidence of SNARC-like effects for non-numerical ordinal information (Gevers et al., 2003, 2004), a recent fMRI study using a comparison task has shown that the anterior region of the horizontal IPS is equally involved in the processing of numbers and letters (Fias et al., 2007). This evidence suggests that the IPS region may represent numerical ordinality, and not only cardinality (Fias et al., 2007; Nieder, 2005). 2. Calculation and visuo-spatial processes 2.1. The hypothesis of a visuo-spatial medium for arithmetic The importance of visuo-spatial metaphors in grasping mathematical concepts has been stressed by many authors (e.g., ´˜ Bryant and Squire, 2001; Lakoff and Nunez, 2000). In fact, a number of studies have emphasized the fact that participants spontaneously rely on visuo-spatial processes when they engage in arithmetic and numerical processing (e.g., Dehaene, 1992; Restle, 1970; Seron et al., 1992). For instance, the suggestion has been made that visuo-spatial imagery consists of one of several strategies among which subjects may choose to solve arithmetic problems (Siegler and Lemaire, 1997). Visuo-spatial representations may be one resource, among other numerical codes, that subjects may preferentially use to ¨ maintain numerical information in an active state (Noel and Seron, 1993; Seron et al., 1992). The distinction between auditory and visual calculators, neatly introduced by Smith (1983), in describing strategies and performances of famous mathematics prodigies, has been confirmed by a recent case-study of a prodigy turning to visual strategies when calculating (Pesenti et al., 2001). At the same time, other authors have attached a more fundamental role to visuo-spatial imagery in calculation (Hayes, 1973; Heathcote, 1994; Restle, 1970). Furthermore, visualizing mathematical concepts helps their acquisition: For instance, in formal school teaching, the number line diagram has been successfully employed to improve and train subjects in ‘less than’ and ‘more than’ kind of relations (Griffin et al., 1994). In the study of calculation processing, models of numerical cognition assume the existence of a long-term memory store of arithmetical facts, containing known sums, products, and the like (e.g., 2 Â 4), which are retrieved by participants without following the corresponding calculation algorithm (e.g., Ashcraft, 1992). This semantic network is thought to rely on language-based mechan-

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isms, since simple arithmetic facts are supposed to be acquired in school by verbal rote learning (Dehaene, 1992). However, multidigit operations (e.g., 34 Â 25) are supposed to require, besides retrieval of arithmetical facts, the mental manipulation of a spatial image of the operation in Arabic format (Dehaene, 1992). Its maintenance in a short-term representational medium, while the dedicated solution algorithm is applied, is also required. Furthermore, whether or not the calculation problem needs to be solved by writing it down, mastering the spatial information contained in numbers is crucial, for instance, to know the value of digits which, syntactically organized, form a complex number (e.g., units, decades, hundreds), and to know which number must operate with which other number in a calculation problem (e.g., in multiplication, addition, and subtraction). Thus, cognitive models of numerical processing consider the contribution of visuo-spatial and visuo-constructive abilities in arithmetical operations (Dehaene, 1992; McCloskey et al., 1985), and propose the involvement of both verbal and visuo-spatial working memory during complex calculation (Dehaene and Cohen, 1995). The involvement of mental imagery in arithmetic has been considered crucial in order to hold the problem operands, and the interim results, active in a visuo-spatial working memory system during calculation (Hayes, 1973; Hitch, 1978). For instance, it has been suggested that visual imagery is used as a strategy to solve arithmetic problems, since it allows the maintenance of notations that would be performed on paper in written arithmetic (Hayes, 1973). The view that calculation is partially mediated by mental visual images raised interest in the contribution of working memory in calculation and counting processes. In particular, a significant quantity of errors in complex addition may be the consequence of a failure in maintaining crucial information in working memory, such as the ‘carries’, and the interim results (Hitch, 1978). However, the latter observations do not focus on the specific system(s) of working memory (WM) crucial for arithmetic processing (review in Baddeley, 2007). The question as to whether the visuo-spatial component of working memory, the visuo-spatial sketch pad (VSSP), plays a role in arithmetic has been investigated in behavioral studies, by means of interfering with its WM capacity during calculation. 2.2. Experimental paradigms and effects The relationship between the visuo-spatial component of memory and calculation skills has been the object of a few experimental studies, and has mainly been investigated by means of the dual task-paradigm. This methodology has been used to identify which WM components are engaged in performing cognitive tasks (e.g., Logie et al., 1989). The logic of this method consists of engaging participants in a primary cognitive task, while a secondary task, known to place load on the WM components, is concurrently performed. The observed pattern of interference (or lack thereof) provides information about the differential engagement of specific WM subsystems in a given cognitive task. Adopting this rationale, Logie et al. (1994) required subjects to perform a cumulative addition task, consisting of adding a series of two-digit numbers presented in the visual or auditory modality, while the verbal and visuo-spatial WM components were loaded by a secondary task. Spatial suppression, obtained by asking participants to perform a spatial tapping task (i.e., hand movement), produces an interference effect. However, the interference effects are minor in size, and limited to the condition in which numbers are presented in the visual modality. These results suggest a minor involvement of the VSSP in mental arithmetic (Logie et al., 1994). Further support for the importance of visual imagery in calculation comes from the observation that multi-digit addition

problems containing visually similar digits are more prone to errors than addition problems with dissimilar digits. This finding suggests that visual WM is implied in the encoding stage of numerical information (Heathcote, 1994). In this study, visuospatial suppression disrupts calculation performance, the more so in complex problems involving carrying. Visuo-spatial representation may be critical for maintaining the information of the carries (Heathcote, 1994). The role of the VSSP in complex arithmetic has been further investigated by manipulating the visual similarity of the addends ¨ in multi-digit addition (Noel et al., 2001). This study did not find any disrupting effect on the overall performance of participants, as a group; however, emphasizing the role of individual differences in arithmetic performance (LeFevre and Kulak, 1994), and in ¨ manipulating number representation (Noel and Seron, 1993), evidence has been provided, in the performance profile of each participant, for a sensitivity, in the individual subject, to the manipulation of the visual features of the stimuli. Accordingly, some individuals may preferentially rely on the visualization of the ¨ numerical information in computing calculations (Noel et al., 2001; see also Hatta et al., 1989), particularly those for whom the visual form constitutes a preferred code of number representation ¨ (Noel and Seron, 1993). Recent empirical evidence suggests that the recruitment of visuo-spatial codes in arithmetic depends upon contextual factors, such as the problem’s format. Previous findings indicate that the presentation format affects level of performance for arithmetic facts ¨ (Campbell, 1994; Noel and Seron, 1997), and this seems to apply also to complex written calculation. Trbovich and LeFevre (2003) manipulated the vertical and horizontal alignment of addition problems to be solved by participants, while retaining a memory load. Indeed, the vertical presentation of the operands, which mirrors the arrangement of operands in written arithmetic, was expected to elicit the same unit-to-decade addition algorithm used to solve written calculation, thus requiring more visual resources than horizontally presented operands. As expected, the results indicate a cost of the visual load limited to the problems presented in vertical format, suggesting a selective recruitment of the VSSP component of WM in this condition (Trbovich and LeFevre, 2003). Besides written calculation, the role of visuo-spatial processing in simple arithmetic has been investigated using a dual-task paradigm, for either phonological or visuo-spatial suppression (Lee and Kang, 2002). In particular, specific predictions derived from the hypothesis of different forms of number representation involved in different operations, as postulated by the ‘Triple Code’ model (Dehaene and Cohen, 1997; Dehaene et al., 1996). According to this model, an auditory-verbal code is preferentially used for multiplications learned by verbal rote during school-years, whereas subtraction depends on the manipulation of quantity meaning, thus implying the activation of semantic representations, conceived as a mental number line (Dehaene, 1992). This hypothesis predicts an operation-specific relationship between arithmetic performance and working memory subsystems, as indeed reported by Lee and Kang (2002): Phonological suppression affects multiplication but not subtraction, whereas visuo-spatial suppression interferes with subtraction but not multiplication (Lee and Kang, 2002). These findings lend support to the hypothesis of discrete, operation-specific, numerical representations in simple arithmetic (Dehaene et al., 1999). It is worth noticing that brain-damaged patients with spatial neglect may present with no signs of acalculia and, specifically, be unimpaired in arithmetic tasks, such as simple arithmetic fact retrieval with one- and two-digit numbers (Vuilleumier et al., 2004), and numerical comparison and subtraction tasks (Zorzi et al., 2002). Furthermore, patients may be impaired exploring

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explicitly a spatially organized numerical representation, showing left-sided neglect in a mental bisection task, but no effects of neglect on the SNARC effect (Priftis et al., 2006). To account for these findings, one might imply that numerical visuo-spatial representations are invoked only implicitly when supporting subtraction and/or addition problems, or the SNARC effect. 2.3. Neuropsychological evidence Intuitively, one may consider visuo-spatial processing as intrinsically related to number processing and calculation, all the more so when treating multi-digit numbers. Difficulties of visuo-spatial nature would thus manifest themselves in the assembly and organization of numbers, or in the spatial layout of written calculation. In the neuropsychological literature, the role of visual and spatial processes in the occurrence of numerical deficits was in fact recognized very early on, although mainly grounded on anecdotal and scattered clinical observations (e.g., Kleist, 1934; Peritz, 1918; Singer and Low, 1933). The link between numerical abilities and space was formalized ´ by Hecaen who introduced the term ‘‘spatial acalculia’’, with reference to difficulties in dealing with written digits in a specific order and position, including calculation deficits associated with ´ spatial neglect (Hecaen et al., 1961). Typical errors associated with spatial acalculia include incorrect alignment of digits in columns, confusions with reversals (32 for 23), or with visually similar digits (6 for 9), and difficulties in maintaining the decimal place (for a ´ review, see Hartje, 1987) (Fig. 5). Since the seminal paper by Hecaen et al. (1961), the ‘spatial’ category of acalculia refers to calculation deficits considered to be secondary to visuo-spatial disorders. On the basis of this assumption, acalculia has been investigated in group studies of right-brain-damaged patients (Ardila and Roselli, 1994; Basso et al., 2000; Dahmen et al., 1982; Rosselli and Ardila, 1989). Most of these studies have confirmed the presence of spatially related difficulties in multi-digit written calculation in righthemisphere-damaged patients, namely: Problems with carrying and borrowing, organization of interim products, and failure in the correct alignment of digits. These reports, however, do not provide any interpretation concerning the functional origin of these errors. Only recently, efforts have been made to identify which components of multi-digit calculation rely on spatial cognition and, in turn, to verify whether ‘‘spatial’’ errors may be related to calculation-specific spatial disturbances, rather than to a generic ` ` spatial deficit (Grana et al., 2006). In particular, Grana et al. (2006) report a right-hemisphere-damaged patient who systematically fails on multiplication procedures. Specifically, while knowing ‘what’, ‘when’, and ‘how’ to carry out the various steps required to

solve a multi-digit multiplication, the patient does not know ‘‘where’’. The patient’s difficulties are traced back to the impairment of a visuo-spatial store, containing a layout representation specific to multiplication. This system may support neurologically unimpaired calculators in overcoming the WM demands of complex calculation, by representing the information of where ` each sub-step should be placed (Grana et al., 2006). The role for such a memory-based visuo-spatial store resource, or representation, in calculation had been previously suggested (Dehaene and Cohen, 1995), but was awaiting for experimental support. Other neuropsychological syndromes, like posterior cortical atrophy, which includes other complex visual disorders and leftto-right disorientation (Benson et al., 1988), provide further support for the close relationship between visuo-spatial deficits and impairment of calculation abilities. A recent case study presents a detailed neuropsychological examination of numerical and arithmetical abilities in a patient with a severe atrophy of the bilateral posterior parietal regions, more pronounced on the right side (Delazer et al., 2006a,b). The patient’s severe impairment in visuo-spatial processing was accompanied by a series of numerical deficits in tasks assessing counting large series of dots arrays, numerical bisection, approximation, and estimation. Moreover, while the recitation of the counting sequence was well preserved (as predicted by the preserved language abilities), the patient was severely impaired in the subtraction and division arithmetical abilities (both mental and written) (Delazer et al., 2006a,b). Aside from the neuropsychological evidence in adult patients with acquired brain damage, hints for the differential contribution of verbal and non-verbal competence to numerical cognition comes from the investigation of number abilities in children with genetic disorders, and specifically those whose cognitive impairment is characterized by visuo-spatial deficits (i.e., Williams syndrome and Turner Syndrome). In particular, since Williams syndrome (WS) is marked by a relative strength in language, coupled with a severe deficit in visuo-spatial abilities, attention has recently been directed to the deficit in numerical cognition, typically associated with these disorders (Ansari et al., 2003; Paterson et al., 2006). Critically, the impairment in visuo-spatial cognition prevents the normal development of exact number representation, regardless of adequate language abilities (Ansari et al., 2003). Indeed, in the context of an overall delay in cardinality understanding, language predicts the success of WS children in numerical tasks better than visuo-spatial abilities, which is opposite to what occurs for normally developing unimpaired children, whose visuo-spatial abilities predict their performance in numerical tasks. Overall, these studies point to the role that visuo-spatial cognition plays in the normal development of numerical understanding, strengthening the view that basic number competence is driven by a non-verbal system of representations (Dehaene et al., 1999; Gelman and Butterworth, 2005). 2.4. Neural correlates The observation that number processing and calculation rely on brain areas devoted to visuo-spatial processes has been highlighted in numerous neuroimaging studies (e.g., Chochon et al., 1999; Dehaene et al., 1999; Dehaene et al., 1996; Gruber et al., 2001; Pesenti et al., 2001; Simon et al., 2002; Zago et al., 2001; Zago and Tzourio-Mazoyer, 2002). Complex calculation includes a wide range of cognitive components, from number-specific processes, such as accessing the quantity meaning of numbers, to processes shared by arithmetical and non-arithmetical tasks, such as attention, and the active maintenance of the numerical information in spatial WM (Simon et al., 2002). The brain areas that are engaged in complex calculation comprise a network of prefrontal, premotor, and parietal cortices (e.g., Gruber et al., 2001).

Fig. 5. Examples of spatial errors in written calculation: misalignment of partial ` product in complex multiplication (adapted from Grana et al., 2006).

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Few neuroimaging studies, aiming at characterizing the WM systems engaged during the resolution of a complex calculation, have shown that visuo-spatial working memory is massively exploited in arithmetic performance (Pesenti et al., 2000; Zago et al., 2001; Zago and Tzourio-Mazoyer, 2002). For instance, when comparing the brain activations during a complex calculation task and a non-numerical visuo-spatial task, a bilateral involvement of the posterior parietal regions is found (Zago and Tzourio-Mazoyer, 2002). In particular, the task of multiplying a pair of two-digit numbers relies, among other areas, on a bilateral fronto-parietal network (supposed to be engaged on holding multi-digit numbers in visuo-spatial WM), as well as on the inferior temporal gyrus bilaterally (possibly involved in mental imagery) (Zago et al., 2001). Moreover, it has been shown that, during the development of arithmetical abilities, significant changes in neural responses are observed (Rivera et al., 2005). In this study, 8-to-20-year-old participants performed a verification task with a series of two-digit addition and subtraction problems: Older participants exhibit more activation in the left supramarginal gyrus and the IPS, whereas in younger subjects there is more activity in the prefrontal cortex. These findings suggest a developmental process of functional specialization of the posterior parietal cortex for mental arithmetic (Rivera et al., 2005). With regard to the role of visuo-spatial WM, the upper part of the right supramarginal gyrus may be a relevant region (Becker et al., 1999). The role of the inferior parietal lobule (angular and supramarginal gyri) in calculation has been repeatedly suggested (Dehaene et al., 1999; Gruber et al., 2001; Menon et al., 2000; Zago and Tzourio-Mazoyer, 2002). Particularly, a bilateral increase of activation in the angular gyrus of the inferior parietal cortex, in response to increasing arithmetic complexity, has been reported (Menon et al., 2000). Activation of the right supramarginal gyrus is associated with both complex calculation on visually presented numbers, and non-numerical tasks that tap visuo-spatial WM (Zago and Tzourio-Mazoyer, 2002). These observations concur to suggest that the storage of numbers, such as the carries, needed for mental calculation, is accomplished by holding information in a visuo-spatial short-term representational medium (Pesenti et al., 2000; Zago and Tzourio-Mazoyer, 2002). 3. Conclusions Following very early suggestions, starting from the end of the XIX century (Galton, 1880; Moyer and Landauer, 1967; Restle, 1970), there is converging evidence to the effect that numerical and arithmetical abilities involve visuo-spatial resources, for the purpose of processing and temporary storage. Overall, neuropsychological reports, neuroimaging and behavioral findings support the view that visuo-spatial processes and numerical representation are intimately related. This relationship may constitute an early and fundamental link which, although partially shaped by our cultural constraints, remains an essential component of our cognitive architecture. Acknowledgements Supported in part by a MUR Prin 2005 Grant to G.V. and L.G. M.D.dH. was supported by a Spanish MEC-Fulbright Postdoctoral Fellowship. References
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