NeuroImage 62 (2012) 1520–1528

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NeuroImage
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Common substrate for mental arithmetic and finger representation in the

parietal cortex
Michael Andres a, b, c,⁎, Nicolas Michaux a, b, Mauro Pesenti a, b
a
Institut de Recherche en Sciences Psychologiques, Université catholique de Louvain, Place Cardinal Mercier 10, 1348 Louvain-la-Neuve, Belgium
b
Institute of Neuroscience, Université catholique de Louvain, Avenue Hippocrate 10, 1200 Brussels, Belgium
c
Department of Experimental Psychology, Ghent University, Henri Dunantlaan 2, 9000 Gent, Belgium

a r t i c l e i n f o a b s t r a c t

Article history: The history of mathematics provides several examples of the use of fingers to count or calculate. These obser-
Accepted 20 May 2012 vations converge with developmental data showing that fingers play a critical role in the acquisition of arith-
Available online 24 May 2012 metic knowledge. Further studies evidenced specific interference of finger movements with arithmetic
problem solving in adults, raising the question of whether or not finger and number manipulations rely on
Keywords:
common brain areas. In the present study, functional magnetic resonance imaging (fMRI) was used to inves-
Counting
Memory retrieval
tigate the possible overlap between the brain areas involved in mental arithmetic and those involved in fin-
Calculation ger discrimination. Solving subtraction and multiplication problems was found to increase cerebral activation
Embodied cognition bilaterally in the horizontal part of the intraparietal sulcus (hIPS) and in the posterior part of the superior
parietal lobule (PSPL). Finger discrimination was associated with increased activity in a bilateral occipito-
parieto-precentral network extending from the extrastriate body area to the primary somatosensory and
motor cortices. A conjunction analysis showed common areas for mental arithmetic and finger representa-
tion in the hIPS and PSPL bilaterally. Voxelwise correlations further showed that finger discrimination and
mental arithmetic induced a similar pattern of activity within the parietal areas only. Pattern similarity
was more important for the left than for the right hIPS and for subtraction than for multiplication. These find-
ings provide the first evidence that the brain circuits involved in finger representation also underlie arithmetic
operations in adults.
© 2012 Elsevier Inc. All rights reserved.

Introduction et al., 2011; Domahs et al., 2008). In adults, behavioural studies reported
faster numerical judgements when target numbers were primed by
The use of fingers to count objects or calculate goes back to the finger configurations congruent with the finger-counting habits of the
Ancient Times (e.g., Cicero, Epistole ad Atticum, V, 21, 13, 106–43 BCN) participants (Badets et al., 2010; Di Luca & Pesenti, 2008; Di Luca et al.,
and is further illustrated in famous counting systems (e.g., Beda 2006, 2010). A trace of finger-counting habits was also found in electro-
Venerabilis, De temporum ratione, 672–735 ACN) commonly used across physiological studies showing increased corticospinal excitability (CSE)
Europe in the Middle Ages (Butterworth, 1999; Williams and Williams, in hand muscles during various numerical tasks (Andres et al., 2007;
1995). The success of these counting systems across times and cultures Sato et al., 2007).
is likely to result from their capacity to pass the bottleneck of pre- There is now a large agreement that the parietal cortex plays an
existing representations in the brain of each individual (De Cruz, important role in mental calculation, as shown by numerous neuro-
2006). In this view, fingers constitute a useful means for acquiring psychological (e.g., Takayama et al., 1994) and brain imaging studies
and communicating arithmetic knowledge because they provide a phys- (for a recent meta-analysis, see Arsalidou and Taylor, 2011). Several
ical counterpart for mental operations and they rely on pre-existing rep- studies showed that arithmetic factors, such as problem size (De
resentations in the sensorimotor system. Several developmental studies Smedt et al., 2011; Stanescu-Cosson et al., 2000), number of operands
have confirmed the intimate relationship between numbers and fingers. (Menon et al., 2000) and strategy (Delazer et al., 2003, 2005; Grabner
Children's score in finger discrimination tests is the best predictor of et al., 2009), influence the blood-oxygen level-dependent (BOLD) sig-
their later arithmetical skills (Noël, 2005) and finger counting proved nal in the horizontal part of the intraparietal sulcus (hIPS) and in the
to be very important while learning to add or subtract numbers (Costa posterior part of superior parietal lobule (PSPL), a region extending
from the posterior segment of the IPS to the precuneus. In contrast
⁎ Corresponding author at: Department of Experimental Psychology, Ghent University,
to subtraction and addition that may require calculation procedures,
Henri Dunantlaan 2, 9000 Gent, Belgium. the multiplication of single digits generally leads to direct retrieval
E-mail address: andres.meh@gmail.com (M. Andres). of the problem and its answer from long-term memory (Campbell,

1053-8119/$ – see front matter © 2012 Elsevier Inc. All rights reserved.
doi:10.1016/j.neuroimage.2012.05.047
 M. Andres et al. / NeuroImage 62 (2012) 1520–1528 1521

1987; Galfano et al., 2003; LeFevre et al., 1996), with the contribution however, whether the predicted overlap between the brain circuits
of the middle and superior temporal gyrii (MTG and STG; Lampl et al., underlying finger discrimination and those involved in mental arith-
1994; Prado et al., 2011; Sandrini et al., 2003; Zhou et al., 2007) and/ metic will differ between operations. If the influence of finger use on
or the angular gyrus (ANG; Delazer et al., 2003; Grabner et al., 2009, arithmetic operations is strictly related to procedural aspects of cou-
2011). Recent evidence from fMRI-guided TMS studies showed that nting in childhood, then finger circuits should overlap exclusively
the integrity of the hIPS is required to perform both subtraction and with those involved in subtraction. The finding of a similar overlap
multiplication problems, challenging the view that the brain net- for subtraction and multiplication would mean that the influence of
works underlying these operations are entirely separated (Andres finger use on arithmetic operations is not limited to the procedural
et al., 2011; Salillas et al., 2012). Finally, mental arithmetic has been aspects of counting but entails a representation of the numbers
shown to recruit several areas in the frontal lobe (Arsalidou and and/or intermediary results on the fingers regardless of arithmetic
Taylor, 2011), among which areas in the ventral and dorsal parts of operation.
the premotor cortex (Pesenti et al., 2000; Piazza et al., 2006). Interest- In order to address these issues, we used fMRI to measure the
ingly, the parietal and frontal areas activated during mental arithmetic BOLD signal in the brain of healthy adults who had to solve subtrac-
are very close to those activated by executed or imagined finger move- tion and multiplication problems or to discriminate the position of
ments, suggesting that number processing is anchored in the processes the fingers on the left and right hand. The similarity between the pat-
underlying finger representation (Haaland et al., 2004; Harrington tern of activity observed during finger discrimination and that ob-
et al., 2000; Pelgrims et al., 2009, 2011). However, so far, this apparent served during each arithmetic operation was further explored by
anatomical similarity only stems from indirect comparisons of results computing voxelwise correlations between tasks.
coming from different studies using different methods.
Moreover, the functional mechanism that accounts for the poten- Material and methods
tial overlap between mental arithmetic and finger representation in
the human brain remains to be specified. First, it is unclear whether Participants
the processes and/or representations related to finger discrimination
form an intrinsic component of number processing, or whether they Eighteen French-speaking males (mean ± S.D.: 21.3 ± 2.5 years)
complement the core number system by providing helpful tools to gave their informed consent to participate to this study. All partici-
manipulate numbers, such as other slave systems involved in visuo- pants were right-handed according to the Edinburgh Handedness
spatial or linguistic aspects of number processing (Dehaene et al., Inventory (mean EHI score ([right−left]/[right+left])±S.D.: 0.81±
2003). Second, it is essential to determine how much the potential 0.16; Oldfield, 1971). They had no history of neurological or psychiatric
overlap between mental arithmetic and finger representation is relat- disorders, had normal or corrected-to-normal vision, and they were un-
ed to the somatic representation of the body in order to specify aware of the purpose of the study. The experiment was non-invasive
the embodied nature of their interactions. In line with this, previous and was performed in accordance with the ethical standards laid down
fMRI studies showed that activations in the primary motor (M1) in the 1964 Helsinki Declaration. The experimental protocol was ap-
and somatosensory cortex (S1) were sensitive to the hand used to proved by the Biomedical Ethical Committee of the Université catholique
perform finger movements, whereas activations of the hIPS and de Louvain.
PSPL occurred irrespective of hand laterality (Haaland et al., 2004;
Harrington et al., 2000). A third question concerns the influence of Tasks and stimuli
representational and procedural aspects of finger counting on the im-
plementation of arithmetic operations in finger circuits. Representa- The three experimental tasks were matched with specific control
tional aspects were evidenced in behavioural studies showing that tasks in terms of visual display and response requirements (see
numbers or results of arithmetic operations implicitly activate a men- Fig. 1). In the finger discrimination task (adapted from Kinsbourne
tal configuration of fingers (Badets et al., 2010; Di Luca & Pesenti, and Warrington, 1962), the participants held a wooden block of irreg-
2008; Di Luca et al., 2006, 2010). Procedural aspects refer to the role ular shape in each hand, with half of the fingers flexed in the holes
of fingers in instantiating the one-to-one correspondence between and the other half extended over the bumps of the blocks; the
counted items and any ordered series (Andres et al., 2007). Whereas thumb was positioned on the lateral face of the block to allow a stable
representational aspects do not necessarily imply a different imple- grip (Fig. 1A). In each trial, the palm view of a left or right hand was
mentation of each operation in finger circuits, procedural aspects displayed on the screen in black on a white background. During the
predict that the involvement of finger circuits will differ across op- experimental blocks, one finger was red and the participants were
erations as a function of the level of practice with finger counting. instructed to answer aloud “yes” if their corresponding finger was
In children, single-digit multiplication problems are mostly solved by flexed into a hole of the wooden block and “no” if it was extended
memory retrieval from the fourth grade (Cooney et al., 1988), whereas over a bump, without moving or looking at their fingers (Fig. 1B). All
subtraction often involves computational strategies with a great em- fingers but the thumb were tested in each experimental block, using
phasis on finger-based calculation procedures in the early stages of ac- a pseudo-random order, so that the same finger was not coloured in
quisition (Fuson, 1988; pp. 278–279). Adults report almost exclusive red in two consecutive trials. In the control task, all fingers on the draw-
reliance on retrieval for multiplication (i.e., 98% and 95% for small ing had the same colour, either black or red, and the participants had to
and large problems respectively), whereas this strategy is much less decide whether it was red by answering aloud “yes” or “no” (Fig. 1C).
used for subtraction (i.e., 73% and 42% for small and large problems re- Different wooden blocks were placed in the left and right hands at
spectively; Campbell and Xue, 2001). The status of addition is less clear the beginning of each run in order to prevent the participants from re-
with a rate of memory retrieval in-between multiplication and subtrac- lying on learned associations between finger names and expected an-
tion (i.e., 88% and 64% for small and large addition problems respec- swers. The left and right hands were tested in separate series of trials
tively; Campbell and Xue, 2001). A dual-task experiment showed that to avoid confusion between finger discrimination and left–right orien-
concurrent finger movements slow down addition and subtraction, tation during the task. During the arithmetic tasks, one Arabic digit
whereas multiplication remains unaffected, even after matching prob- ranging from 3 to 9 was displayed on the screen and the participants
lems for response speed and accuracy (Michaux et al., submitted for had to subtract it from 11 or 13, or to multiply it by 3 or 4, depending
publication). This difference was attributed to the fact that multiplica- on the run (Fig. 1C); the control task required reading single uppercase
tion is less sensitive to finger interference because answers can be re- letters (C, D, F, G, H, J). The wooden blocks were removed from the
trieved from long-term memory without computation. It is unclear, hands of the participants during the arithmetic tasks. In total, the
1522 M. Andres et al. / NeuroImage 62 (2012) 1520–1528

Fig. 1. A. Photograph of the wooden blocks used in the finger discrimination task. During the task, the participants held a different block in each hand, palms up, with the thumb in a
lateral position. B. Illustration of the participant's grip on the wooden block, with half of the fingers placed over the bumps (upper position) and the others in the holes of the block
(down position). C. Time course of each experimental task and its reference. In arithmetic tasks, they had to multiply the Arabic digit by 3 or 4, or to subtract it from 11 or 13. In the
finger discrimination task, the participants were instructed to decide whether the red finger was in a down position by saying “yes” or “no”. Control tasks consisted in letter reading
or colour judgements (see Procedure for further details).

participants performed 15 trials for each finger of the two hands, 12 tri- flip angle = 8°, field of view = 220 × 197 mm, 150 contiguous axial
als for each digit (or letter) in each arithmetic (or reading) task, except slices of 1 mm, voxel size= 0.81× 0.95 × 1 mm, SENSE factor = 1.4).
for 3 and 4 (or C and D) that were presented 6 times in each arithmetic Functional images were then acquired as series of blood-oxygen-
(or reading) task. sensitive T2*-weighted echo-planar image volumes (GRE-EPI). Each
run consisted of 132 volumes and was preceded by 4 dummy scans
Procedure to allow for magnetic saturation effects. Acquisition parameters were:
TE= 50 ms, TR= 2500 ms, flip angle = 90°, FOV= 220 × 220 mm, 36
The participants practiced all tasks outside the magnet room in slices acquired in an ascending interleaved sequence, slice thickness =
order to get familiar with the instructions and response requirements. 3.5 mm with no interslice gap, SENSE factor (parallel imaging) = 2.5.
In particular, they were trained to produce audible responses while
keeping bucco-laryngo-facial movements to a minimum. In the magnet Data analysis
room, the participants were lying in the scanner with both arms resting
along the body, palms up, and viewed the stimuli projected on a screen, A first analysis of variance (ANOVA) was performed on error rates
in the rear of the scanner, via a tilted mirror mounted on the head coil. and median response latencies (RLs) of correct trials with TASK (sub-
Each experimental task and its control were tested twice in 6 runs traction, multiplication vs. finger) as a within-subject factor. A second
counterbalanced across participants. We used a block-design paradigm ANOVA was performed on the median RLs in the finger discrimina-
with short series of 17,500 ms, interleaved with 10,000 ms fixation pe- tion task with HAND SIDE (left vs. right) and FINGERS (index, middle,
riods, to optimize the signal-to-noise ratio while controlling for speech- ring vs. pinkie) as within-subject factors. This ANOVA was not con-
related head motion artefacts (Birn et al., 2004). Each run consisted of ducted on error rates due to empty cells. Paired-sample t-tests were
12 series alternating between an experimental task and its control. used for post-hoc comparisons (p b .05, Bonferroni adjustment for
Each series involved 5 trials where hand drawings or digits/letters multiple comparisons). Average RLs are reported with standard er-
were displayed for 150 ms with a 3500-ms intertrial interval. The partic- rors (S.E.) corrected for within-subject designs (Loftus and Masson,
ipants were reminded of the instructions at the beginning of each run. 1994).
Stimulus display was controlled by E-prime 2.0 (Psychology Software The functional data were processed and analyzed using Statistical
Tools, Pittsburgh, USA) and the verbal responses were recorded by a Parametric Mapping (SPM5, Welcome Department of Cognitive Neu-
digital recorder (for more details about this procedure, see Andres rology, London, UK, http://www.fil.ion.ucl.ac.uk/spm). The functional
et al., 2011). images were (1) corrected for slice acquisition delays, (2) re-aligned
to the first scan of the first run (closest to the anatomical scan) to cor-
Imaging protocol rect for within- and between-run motion, (3) coregistered with the
anatomical image, (4) normalized to the MNI template using an affine
For each participant, a high-resolution anatomical image was fourth degree ß-spline interpolation transformation and a voxel size
first acquired with a 3.0 Tesla magnetic resonance imager and an of 2 × 2 × 2 mm 3 after the skull and bones had been removed with a
8-channel phased array head coil (Achieva, Philips Medical Systems, mask based on the individual anatomical images, and (5) spatially
Andover, MA, USA) using a T1-weighted 3D turbo fast field-echo se- smoothed using an 8-mm FWHM Gaussian kernel. Condition-related
quence with an inversion recovery prepulse (TE = 4.6 ms, TR = 9.1 ms, BOLD signal changes were estimated for each participant by a general
 M. Andres et al. / NeuroImage 62 (2012) 1520–1528 1523

linear model in which the responses evoked by each condition were 20 ms, t(17) = 5.02, p b .001; Fig. 2A). In the finger discrimination
modelled by a standard hemodynamic response function. The con- task, a main effect of FINGER (F(3,51) = 7.55, p b .001) was found, with
trasts of interest were computed at the individual level to identify slower responses for the middle finger (746 ± 13 ms) when compared
the cerebral areas significantly activated by subtraction or multiplica- to the index (683 ± 11 ms, t(17) = 3.77, p b .01) and the pinkie (661 ±
tion. The significant cerebral activations for the critical contrasts (fin- 9 ms, t(17) = 4.29, p b .01), and for the ring finger (721 ± 14 ms) when
ger discrimination minus colour judgement; subtraction minus letter compared to the pinkie (t(17) = 3.69, p b .01). Performance was as
reading; multiplication minus letter reading; multiplication minus fast and accurate for the left (701±8.3 ms and 2.1±0.6%) and right
subtraction; subtraction minus multiplication) were examined at the hands (705±8.3 ms and 4.6±1.2%; Fb 1).
group level in random-effect analyses with the statistical threshold
set at p b 0.05 corrected for the false discovery rate (pFDR). In order to
reveal the brain areas commonly activated in finger and arithmetic fMRI results
tasks, the contrasts computed at the group level were entered in a
conjunction analysis using the minimum statistic (MS) compared to The contrast between mental arithmetic and letter reading showed
the conjunction null (CN; Nichols et al., 2005). bilateral activations in the hIPS, in the PSPL, and right-sided activa-
Voxelwise correlations were then computed between task-related tions in the orbital part of the inferior frontal gyrus (IFG; Fig. 2B and
changes of the BOLD signal in the areas revealed by the conjunction Table 1). The direct contrast between multiplication and subtraction
analysis. If two tasks recruit the same neuronal populations, a positive revealed further activations in the left and right superior temporal
correlation is expected because the pattern of voxels showing low gyrii (STG). No area was significantly more activated during subtrac-
and high activity increases should be similar for both tasks; dissimilar tion than multiplication. The contrast between finger discrimination
patterns of peak voxels between tasks should be reflected by a null and colour judgement showed a bilateral occipito-parieto-precentral
or negative correlation (Dormal et al., 2010; Downing et al., 2007; network (Fig. 2C and Table 1). Increased activity was observed bilater-
Peelen and Downing, 2007; Peelen et al., 2006, 2007). The clusters re- ally in the EBA, the hIPS, the PSPL and the frontal eye fields (FEF). Clus-
vealed by the conjunction analysis were intersected with a 5-mm- ters of activation were also found in the left inferior precentral sulcus
radius sphere centred on peak voxels, using the MarsBAR toolbox (PrCS), the right IFG and the right middle frontal gyrus (MFG). The di-
(http://marsbar.sourceforge.net; Brett et al., 2002), and t-values rect contrasts between the left and right hands, and vice-versa, re-
were extracted for each contrast and each participant from a set of vealed additional activations in the contralateral M1 and S1.
normalized but unsmoothed data. First, we measured (1) the correla- The conjunction analysis showed common activations for finger
tion between the t-values of the contrast [finger discrimination–colour discrimination, subtraction and multiplication in the hIPS and PSPL,
judgement] and the t-values of the contrast [subtraction–letter reading] bilaterally, and in the right IFG (Fig. 2D). In order to investigate further
and (2) the correlation between the t-values of the contrast [finger the functional overlap between finger discrimination and each arith-
discrimination–colour judgement] and the t-values of the contrast metic task, we measured voxelwise correlations in each area identified
[multiplication–letter reading] across the voxels of each cluster. Pearson in the conjunction analysis. Table 2 provides the Pearson coefficients
coefficients were computed at the individual level and the mean coeffi- for the correlation between the t-values of the [finger discrimination–
cient of each correlation was tested against 0 using a one-sample t-test colour judgement] contrast and the t-values of the [subtraction–letter
with SUBJECT as a random factor (for statistical procedures, see Lorch reading] contrast, and for the correlation between the t-values of the
and Myers, 1990). Because the finger task was correlated both with [finger discrimination–colour judgement] contrast and the t-values of
the subtraction task and with the multiplication task, p-values were ad- the [multiplication–letter reading] contrast for the four parietal clusters.
justed to control for Type 1 error with α = 0.05/2. Second, as a control, In the hIPS and PSPL, positive correlations were found between the ac-
we measured voxelwise correlations between tasks in 5-mm spheres tivation patterns elicited by finger discrimination and each arithmetic
centred on the peak voxel in the left and right extrastriate body areas task (all r ranging between .3 and .6; all p b .004). Voxelwise correlations
(EBA), which were activated during finger discrimination but not dur- between task-related patterns in the EBA, chosen as a control site be-
ing mental arithmetic. The between-task correlations measured for cause of its specific contribution to finger discrimination, showed only
each area revealed by the conjunction analysis were directly compared weak and nonsignificant correlations (all r between −.08 and .2, all
to the between-task correlations measured for the EBA of the same p > .1, corrected for multiple comparisons). In the left hemisphere,
hemisphere using paired-sample t-tests with SUBJECT as a random factor. correlations between finger- and arithmetic-related patterns were sig-
A Bonferroni correction was applied to take into account that each EBA nificantly larger in the hIPS and PSPL than in the EBA (all p b .004,
was compared to multiple areas (2 in the left hemisphere, i.e. the hIPS corrected for multiple comparisons; Table 2). In the right hemisphere,
and PSPL, and 3 in the right hemisphere, i.e. the hIPS, PSPL and IFG). a significant difference was observed between the PSPL and the EBA
Third, the coefficients obtained for homologue parietal areas were (all p b .021, corrected for multiple comparisons) but not between the
entered in a repeated-measure ANOVA with CORRELATION (finger- hIPS and the EBA (all p >.1). The ANOVA with HEMISPHERE (left vs. right),
subtraction vs. finger-multiplication), SITE (hIPS vs. PSPL) and HEMISPHERE AREA (hIPS vs. PSPL) and CORRELATION (finger-subtraction vs. finger-
(left vs. right) as within-subject factors, and SUBJECT as a random factor, multiplication) as within-subject factors revealed a main effect of AREA
in order to investigate the effect of these factors on the size of the coef- (F(1,17)= 8.34, pb .01), with larger correlations in the PSPL than in the
ficients. A Bonferroni correction was applied where needed in post-hoc hIPS, and an interaction between AREA and HEMISPHERE (F(1,17) =5.49,
comparisons. pb .032), indicating that the difference between the two areas mainly
concerned the right hemisphere (right PSPL vs. right hIPS: t(17)=3.3,
Results pb .05). No significant difference was found between activation patterns
in the PSPL and the hIPS of the left hemisphere (t(17)=1.56, p >.1). Re-
Behavioural results sults also showed a main effect of CORRELATION (F(1,17)=8.23, pb .001),
indicating that the activation pattern observed during finger dis-
The error rates did not differ between subtraction (mean ± S.E.: crimination was more similar to the one observed during subtraction
3.5 ± 1.1%), multiplication (3.9 ± 0.5%) and finger discrimination than during multiplication across all parietal areas. Finally, correla-
(3.3 ± 0.6%; F b 1). A significant effect of TASK was found on RLs tions between activation patterns in the right IFG (finger-subtraction:
(F(2,34) = 14.84, p b .001), showing that performance was slower in r =.21 ±.07; finger-multiplication: r =.22±.08) failed to be significant
the subtraction task (905 ± 23 ms) than in the multiplication (792 ± and did not differ from the correlations measured for the right EBA, cho-
24 ms, t(17) = 3.20, p b .016) and finger discrimination tasks (695 ± sen as a control site (all p >.1).
1524 M. Andres et al. / NeuroImage 62 (2012) 1520–1528

Fig. 2. A. Mean RLs and S.E. as a function of task (S = subtraction, M = multiplication, F = finger discrimination) and finger. B. Brain areas showing increased activity in mental
arithmetic tasks compared to letter reading (pFDR b .05). C. Brain regions showing increased activity in finger discrimination compared to colour judgements. D. Overlapping acti-
vations in finger discrimination and arithmetic tasks. Diagrams represent the percent of signal change in peak voxels (MNI coordinates) for each experimental task (black) and
its reference (grey).

Discussion a finger discrimination task. The behavioural results showed that sub-
traction was performed more slowly than multiplication or finger
The present study tested the hypothesis that the cerebral network discrimination, whereas the error rate was equal in the three tasks.
involved in mental arithmetic overlaps with the one involved in finger Discriminating the position of the middle and ring fingers took longer
discrimination. To do so, whole brain activity was measured while par- than discriminating the position of the index and pinkie, which is
ticipants solved subtraction and multiplication problems or performed reminiscent of the greater difficulties of brain-damaged patients
 M. Andres et al. / NeuroImage 62 (2012) 1520–1528 1525

Table 1 other areas along the IPS and the PrCS were activated during finger
Summary of the activations observed during subtraction, multiplication and finger discrimination, irrespective of the tested hand. This parieto-precentral
discrimination (pFDR b .05; minimum cluster size k = 100 voxels).
network has been repeatedly associated with the execution or mental im-
Contrast Brain area x y z T-value k agery of hand and finger movements (Haaland et al., 2004; Harrington
Arithmetic–letter reading Left PSPL − 28 − 72 42 5.80 664 et al., 2000; Pelgrims et al., 2009, 2011).
Left hIPS − 32 − 58 42 5.58 In the parietal cortices, the areas involved in mental arithmetic
Right PSPL 32 − 70 42 5.13 377 and finger discrimination overlapped in the hIPS and PSPL of both
Right IFG 42 20 −2 4.80 282
hemispheres. In all areas but the right hIPS, the patterns of activity
Right hIPS 48 − 40 48 4.06 200
Multiplication–subtraction Left STG − 60 − 14 0 5.87 1616 observed during finger discrimination and arithmetic were highly
Right STG 60 −2 −2 5.53 1047 correlated, indicating that brain activity was distributed similarly
Finger task–colour task Left PSPL − 20 − 68 62 11.61 5914 across voxels during these tasks. The AREA by HEMISPHERE interaction in-
Left hIPS − 38 − 44 50 11.08 dicated larger between-task correlations for the PSPL than for the
Left EBA − 48 − 68 −2 7.03
hIPS but only in the right hemisphere. The absence of evidence for a
Right hIPS 44 − 40 52 10.87 5966
Right PSPL 30 − 72 40 9.16 strong correlation between the activation patterns related to finger
Right EBA 54 − 60 −8 7.06 335 discrimination and arithmetic, in the right hIPS, might reflect a left
Left FEF − 28 −4 50 6.37 681 hemisphere specialization for precise numerical representations dur-
Right IFG 38 26 −4 6.35 534
ing the development of finger-counting abilities (Andres et al., 2005,
Right FEF 26 −2 56 5.08 874
Right MFG 50 32 30 4.65 548 2008; Piazza et al., 2007). Although both operations induced activa-
Left PrCS − 46 4 34 3.97 283 tions in the parietal areas underlying finger discrimination, voxelwise
Right hand–left hand Left M1/ S1 − 46 − 22 62 7.39 895 correlations showed that the pattern of activation induced by finger
Left hand–right hand Right M1/ S1 42 − 20 62 6.46 188 discrimination in the hIPS and PSPL was more similar to the one ob-
x, y, z = MNI stereotaxic coordinates of the peak voxels; k = cluster size (number of served during subtraction than during multiplication. The similarity of
voxels); EBA = extrastriate body area, FEF = frontal eye fields, hIPS = intraparietal sulcus activation patterns is not linked to a speed confound since the slowest
(horizontal part), IFG = inferior frontal gyrus (orbital part), M1 = primary motor cortex,
(i.e., subtraction) and fastest (i.e., finger discrimination) tasks turned
MFG = middle frontal gyrus, PrCS = pre-central sulcus (inferior part), PSPL = posterior su-
perior parietal lobule, S1 = primary somatosensory cortex, STG = superior temporal gyrus. out to be more correlated with each other.
These results have several implications for the understanding of
the functional interactions between numbers and fingers in arithmet-
with finger agnosia to recognize central than lateral fingers (Benton, ic operations. First, they show that fingers do not just provide a com-
1959; Kinsbourne and Warrington, 1962). The ability to discriminate plementary tool to perform arithmetic operations since overlapping
the position of fingers was not enhanced for the right dominant hand in activations extended in the hIPS that is assumed to house the core
our participants. Such an observation was also made in a brain-damaged representation of numbers (Dehaene et al., 2003). This neural overlap
patient with finger agnosia (Mayer et al., 1999) and, although no data should therefore be considered as reflecting an intrinsic component
are available for left-handed people, it could indicate that the processes of number processing (for a similar proposal, see Di Luca and Pesenti,
and/or representations underlying the performance of this task are not 2011). Second, because neural overlap was found in parietal areas
influenced by handedness. whose contribution to finger discrimination was not specific to the
Brain imaging results revealed increased activity in the hIPS and left or the right hand, it is reasonable to assume that this overlap is
PSPL bilaterally during subtraction and multiplication, with additional not related to somatic representations. Third, the higher pattern simi-
activations in the left and right STG during multiplication. This finding larity between finger discrimination and subtraction, when compared
converges with the results of previous studies showing that solving to multiplication, suggests that the neural overlap is partially deter-
subtraction problems requires manipulating number representations mined by the strategy used to solve arithmetic problems. The multipli-
with the joint contribution of the hIPS and PSPL (Eger et al., 2003; cation and subtraction problems used in the present study typically lead
Knops et al., 2009a; Piazza et al., 2007; Prado et al., 2011). Although to a rate of memory retrieval of respectively 95% and 42% in occidental
the presentation of simple multiplication problems was also associat- cultures (Campbell and Xue, 2001). Our behavioural results confirmed
ed to increased activity in these parietal areas (Andres et al., 2011; that multiplication problems were solved through fast and automatic
Rickard et al., 2000; Salillas et al., 2012; Zago et al., 2001), it was processes, such as memory retrieval, whereas subtraction problems
shown that these problems induce automatic activation of the answer required more time-consuming computational strategies. In line with
in long-term memory with the potential support of additional areas this, dual-task experiments showed that finger movements slowed
in the MTG and STG (Andres et al., 2011; Prado et al., 2011; Zhou et al., down arithmetic operations solved by counting whereas operations
2007) and/or the ANG (Delazer et al., 2003; Grabner et al., 2009, 2011; solved by memory retrieval remained unaffected (Imbo et al., 2011;
Price and Ansari, 2011). Finger discrimination increased activity in sen- Michaux et al., submitted for publication). Another dual-task experi-
sorimotor areas containing a topographic representation of the body, ment showed that multiplication but not subtraction was delayed by
such as the bilateral EBA (Downing et al., 2007) and the contralateral concurrent phonological rehearsal, corroborating the idea that these
M1 (Dechent and Frahm, 2003) and S1 (Schweizer et al., 2008). Several two operations rely on partially distinct processes and/or representa-
tions (Lee and Kang, 2002). Our brain imaging results therefore suggest
that the role of fingers in arithmetic operations depends on procedural
Table 2 aspects of finger counting. However, procedural aspects are not suffi-
Mean correlations (and S.E.) between the patterns of activation induced by finger dis- cient to account for the implementation of arithmetic operations in fin-
crimination and mental arithmetic in the hIPS and the PSPL. Asterisks indicate a signif-
ger circuits. Indeed, although the pattern similarity was less important,
icant difference when compared to the EBA taken as a control site for its specific
contribution to finger discrimination (*p b .05, corrected for multiple comparisons). multiplication also led to overlapping activations with finger discrimi-
Same abbreviations as in Table 1. nation in the hIPS and PSPL. Because finger-counting strategies do not
directly contribute to solving multiplication problems, such overlap is
Finger and subtraction Finger and multiplication
best explained by the implicit activation of finger configurations rep-
Left hemisphere Right hemisphere Left hemisphere Right hemisphere
resenting the manipulated numbers and/or the intermediate results.
PSPL 0.59 ± 0.07* 0.61 ± 0.06* 0.44 ± 0.09* 0.56 ± 0.07* Below, we propose an explanation that emphasizes procedural aspects
hIPS 0.59 ± 0.08* 0.41 ± 0.06 0.45 ± 0.01* 0.31 ± 0.09 of finger counting, while suggesting that the use of a stable counting se-
EBA 0.11 ± 0.10 0.22 ± 0.10 − 0.08 ± 0.11 0.08 ± 0.10
quence could contribute to derive digital representations of numbers.
1526 M. Andres et al. / NeuroImage 62 (2012) 1520–1528

In the finger discrimination task, the absence of visual feedback difficult to reconcile with its role in attention orientation. Several
put strong demands on the ability to represent the relative position of brain imaging studies corroborated the finding of increased activity in
the fingers, as evidenced by increased RLs for the middle fingers that the hIPS and PSPL during basic multiplication (Andres et al., 2011;
have more neighbours than the others. The pattern of activation in Chochon et al., 1999; Dehaene et al., 1996; Kiefer and Dehaene, 1997;
this task was analogue to the one observed in the contrast between Rickard et al., 2000), sometimes with an extension to the parieto-
complex and simple finger movements in other fMRI studies (Haaland occipital junction (POJ) known for its role in eye–hand coordination
et al., 2004; Harrington et al., 2000). These studies showed that activity (Prado et al., 2005; Zago et al., 2001). The companion role of the PSPL
along the IPS increased each time a new finger was moved, irrespective and POJ in solving basic multiplication problems was also evidenced
of hand laterality, whereas M1 and S1 were activated in response to with fMRI in a patient whose lesions in the left perisylvian areas
contralateral movements regardless of finger changes. The parietal cor- prevented her to solve this operation normally (Cohen et al., 2000). A
tex was found to react to finger transitions, whatever the total number first explanation could be that the PSPL contributes to narrow down
of fingers involved in the sequence, indicating that its contribution was the range of potential answers to multiplication problems by shifting at-
mainly determined by the need to individuate fingers. Cell recordings in tention along a mental number line, as for addition and multiplication
the monkey homologue of the hIPS showed that neuronal activity in (Dehaene and Cohen, 1991). A recent developmental study showed
this area predicts a transition between two different movements, with that 5-to-7-year-old children are indeed able to approximate the an-
incremental increases reflecting the number of times a movement is swer of non-symbolic multiplication problems above chance level, be-
repeated before a transition (Sawamura et al., 2002). Altogether, these fore they receive formal schooling in this operation (McCrink and
results suggest that the parietal network underlying finger discrimina- Spelke, 2010). Alternatively, it has been proposed that the robust parie-
tion is endowed with suitable properties for keeping track of incremen- tal activations observed during basic multiplication problems reflects
tal changes during arithmetic operations. We therefore propose that, magnitude-based strategies that can facilitate their solving (Chochon
during development, the wiring of number and finger circuits in the pa- et al., 1999), for example to reverse the order of the operands or to de-
rietal cortex enables the implementation of a successor function that compose a multiplication into a series of additions (Campbell, 1994;
improves the representation of the number sequence and helps keeping LeFevre et al., 1996). In this view, the PSPL would contribute to shifting
track of incremental changes during arithmetic operations. This inter- attention between operands or zooming in and out the different parts of
pretation fits with electrophysiological results showing an increase of a decomposed problem. The FEF were not activated during arithmetic
CSE in hand muscles whenever items have to be put in correspondence tasks in our study but previous studies suggest that these areas also con-
with the elements of an ordered series, being the number sequence or tribute to represent numbers on a visuospatial medium (Knops et al.,
the alphabet (Andres et al., 2007). Importantly, the implementation of 2009a; Rusconi et al., 2011). Further research is required, however, to
a successor function in the parietal cortex would not only contribute determine the exact nature of the processes shared by finger discrimi-
to keep track of incremental changes but it also provides a medium nation and mental arithmetic in the hIPS and PSPL.
to represent numbers on fingers. Because finger counting relies on a Finally, a cluster of activation was found in the inferior part of the left
stable sequence (i.e. from the thumb to the pinkie in most occidental PrCS during finger discrimination but not during mental arithmetic, in
cultures; Lindemann et al., 2011), the relative position of each finger contrast with several previous results (Arsalidou and Taylor, 2011). Fur-
can be used to infer the cardinality of a number. The digital representa- ther studies are required to explain this discrepancy, for example, by
tions derived from the mapping of the number sequence onto fingers using a larger set of arithmetic problems. It is worth noting that activa-
can in turn support other functions in mental arithmetic, such as the tion in the left PrCS might have been underestimated in the finger dis-
creation/consolidation of arithmetic facts or the decomposition of a crimination task as well, because the colour judgement task, used as a
problem in intermediate steps (Domahs et al., 2008). The latter func- reference, also involved finger drawings. A recent study tested the in-
tions could explain the overlap between finger discrimination and volvement of the left and right premotor/motor cortex as a function of
multiplication in the parietal cortex. Along the same lines, the finger in- the preferred counting direction of the participants (Tschentscher et
dividuation process underlying one-to-one correspondence is likely to al., 2012). Viewing numbers between 1 and 5, with both hands at rest,
support exact arithmetic operations with small and large numbers, led to higher activation in the right premotor/motor cortex of left-
but we do not exclude a more specific contribution to small arithmetic starters when compared to right-starters, showing that the preferred
problems whose answer can be readily represented through configural starting hand influenced the activations induced by small numbers in
representations (Kaufmann et al., 2008; Thompson et al., 2004). In order the contralateral hemisphere. No difference was observed for numbers
to address this issue, future fMRI studies should investigate whether ranging from 6 to 10. These results suggest that future studies should
the BOLD signal in finger-related areas correlates with problem size in take into account the relationship between hand preference for finger-
arithmetic tasks. based calculation and hemispheric lateralization of motor activity in
The hIPS activation extends in areas whose role in visuomotor func- order to decipher the role of the premotor/motor cortex in mental arith-
tions, such as pointing or grasping, is well established both in human metic. In the present study, the only common focus of activation in the
and non-human primates (Binkofski et al., 1999; Simon et al., 2002). frontal lobe was located in the right IFG. It has been argued that this
The same areas have also been related to movement preparation and area controls the search within working memory contents (Lepsien et
motor intention (Göbel et al., 2004; Rushworth et al., 2003; Thoenissen al., 2005). A previous study showed that this area was equally activated
et al., 2002). In contrast, the PSPL is known to interact with the FEF to when numbers, syllables or locations were manipulated vs. rehearsed in
support eye movements and attention shifts (for a meta-analysis, see working memory (Zago et al., 2008). Our multi-voxel pattern analysis
Grosbras et al., 2005). The correlation between the pattern of activation suggests that numbers and fingers do not activate the same parts of
observed in the PSPL during finger discrimination and arithmetic could the IFG, meaning that the recruitment of this area is not completely in-
therefore indicate that the two tasks share common resources for atten- dependent of the contents stored in working memory.
tion allocation over the mental representation of fingers and numbers
(Hubbard et al., 2005). It has been shown that computing the result of Conclusion
an arithmetic problem is analogue to shifting attention to the left or
right side of a mental number line (Knops et al., 2009b; McCrink et al., The present study adds further evidence to the view that the brain
2007; Pinhas and Fischer, 2008). Indeed, a common neural code was areas involved in finger representation might offer a support for
found for leftward saccades and subtraction and for rightward saccades arithmetic operations. Results showed that finger discrimination and
and addition in the PSPL (Knops et al., 2009a). The involvement of the mental arithmetic share common parietal and frontal areas in the
PSPL in multiplication problems solved by memory retrieval is more adult brain. In contrast with the EBA and S1/M1, these areas do not
 M. Andres et al. / NeuroImage 62 (2012) 1520–1528 1527

contribute to somatic representations, as evidenced by a similar increase Dechent, P., Frahm, J., 2003. Functional somatotopy of finger representations in human
primary motor cortex. Hum. Brain Mapp. 18, 272–283.
of activity while representing the left or right hand. Voxelwise correla- Dehaene, S., Cohen, L., 1991. Two mental calculation systems: a case study of severe
tions were used to explore further the neural overlap between finger acalculia with preserved approximation. Neuropsychologia 29, 1045–1074.
discrimination and arithmetic tasks, and similar patterns of activity Dehaene, S., Tzourio, N., Frak, V., Raynaud, L., Cohen, L., Mehler, J., Mazoyer, B., 1996.
Cerebral activations during number multiplication and comparison: a PET study.
were found in the hIPS and PSPL but not in the IFG. Correlations were Neuropsychologia 34, 1097–1106.
higher in the left than in the right hIPS and they were also influenced Dehaene, S., Piazza, M., Pinel, P., Cohen, L., 2003. Three parietal circuits for number pro-
by arithmetic operation. The parietal areas involved in finger discrimina- cessing. Cogn. Neuropsychol. 20, 487–506.
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drill-evidence from an fMRI study. Neuroimage 25 (3), 838–849.
ditional areas in the temporal cortex. Future research should clarify the
De Smedt, B., Holloway, I.D., Ansari, D., 2011. Effects of problem size and arithmetic
nature of the neural mechanisms shared by finger discrimination and operation on brain activation during calculation in children with varying levels
mental arithmetic in the hIPS and PSPL with a special emphasis on the of arithmetical fluency. Neuroimage 57 (3), 771–781.
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This work was supported by grants from the Fonds National pour
in Arabic numeral processing. Q. J. Exp. Psychol. 59, 1648–1663.
la Recherche Scientifique (grant 1.B099.09, FRS-FNRS, Belgium), and Domahs, F., Krinzinger, H., Willmes, K., 2008. Mind the gap between both hands: evidence
the Fonds Spéciaux de Recherche of the Université catholique de for internal finger-based number representations in children's mental calculation.
Louvain (grant FSR09-CWS/09.285). M.A. was a post-doctoral researcher, Cortex 44, 359–367.
Dormal, V., Andres, M., Dormal, G., Pesenti, M., 2010. Mode-dependent and mode-
N.M. is a research fellow and M.P. a research associate at the Fonds Na- independent representations of numerosity in the right intraparietal sulcus.
tional pour la Recherche Scientifique (FRS-FNRS, Belgium). We are grate- Neuroimage 52 (4), 1677–1686.
ful to Pierre Leclef for his contribution to the acquisition of fMRI data, to Downing, P.E., Wiggett, A.J., Peelen, M.V., 2007. Functional magnetic resonance imaging
investigation of overlapping lateral occipitotemporal activations using multi-voxel
Cécile Grandin for the medical supervision, to the Radiodiagnosis Unit pattern analysis. J. Neurosci. 27, 226–233.
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