Impaired neural networks for approximate calculation in dyscalculic children: a functional MRI study

Karin Kucian, Thomas Loenneker, Thomas Dietrich, Mengia Dosch, Ernst Martin, Michael von Aster, Karin Kucian, Thomas Loenneker, Thomas Dietrich, Mengia Dosch, Ernst Martin, Michael von Aster

Abstract

Background: Developmental dyscalculia (DD) is a specific learning disability affecting the acquisition of mathematical skills in children with otherwise normal general intelligence. The goal of the present study was to examine cerebral mechanisms underlying DD.

Methods: Eighteen children with DD aged 11.2 +/- 1.3 years and twenty age-matched typically achieving schoolchildren were investigated using functional magnetic resonance imaging (fMRI) during trials testing approximate and exact mathematical calculation, as well as magnitude comparison.

Results: Children with DD showed greater inter-individual variability and had weaker activation in almost the entire neuronal network for approximate calculation including the intraparietal sulcus, and the middle and inferior frontal gyrus of both hemispheres. In particular, the left intraparietal sulcus, the left inferior frontal gyrus and the right middle frontal gyrus seem to play crucial roles in correct approximate calculation, since brain activation correlated with accuracy rate in these regions. In contrast, no differences between groups could be found for exact calculation and magnitude comparison. In general, fMRI revealed similar parietal and prefrontal activation patterns in DD children compared to controls for all conditions.

Conclusion: In conclusion, there is evidence for a deficient recruitment of neural resources in children with DD when processing analog magnitudes of numbers.

Figures

Figure 1
Figure 1
Paradigm. The paradigm used during fMRI examination consisted of approximate and exact calculation, approximate and exact control conditions as well as magnitude comparison. Each condition was presented in three blocks of 80 s.
Figure 2
Figure 2
Brain activation of children with DD and control children. Brain activation patterns of children with DD (N = 18) and control children (N = 20) during each condition are depicted on the SPM standard brain template. The activated brain regions shown had been subjected to a FWE or FDR correction with a minimum number of 10 voxels, with one exception in Figure 2C, where the shown cluster comprises only 5 voxels. A, B, C: approximate calculation – approximate control condition. D, E: exact calculation – exact control condition. F, G: magnitude comparison – rest.
Figure 3
Figure 3
Stronger activation in control children compared to children with DD. Control children exhibited stronger activation in the insula and parahippocampal gyrus on the right hemisphere during approximate calculation compared to children with DD. Activated brain regions were uncorrected at p < 0.001 with a minimum number of 10 voxels represented on the SPM glass brain.
Figure 4
Figure 4
ROI-analysis. Mean t-values in each defined ROI for approximate calculation in control children (black) and children with DD (striped) are shown. Significant group differences are marked with two stars (** p < 0.05) and trends with one star (* p < 0.1).

References

    1. Butterworth B. The development of arithmetical abilities. J Child Psychol Psychiatry. 2005;46:3–18. doi: 10.1111/j.1469-7610.2004.00374.x.
    1. Kaufmann L, Lochy A, Drexler A, Semenza C. Deficient arithmetic fact retrieval-storage or access problem? A case study. Neuropsychologia. 2004;42:482–496. doi: 10.1016/j.neuropsychologia.2003.09.004.
    1. Temple CM. Procedural dyscalculia and number fact dyscalculia: Double dissociation in developmental dyscalculia. Cogn Neuropsychol. 1991;8:155–176.
    1. Landerl K, Bevan A, Butterworth B. Developmental dyscalculia and basic numerical capacities: a study of 8-9-year-old students. Cognition. 2004;93:99–125. doi: 10.1016/j.cognition.2003.11.004.
    1. WHO . ICD-10. International Statistical Classification of Diseases and Related Health Problems 10th Revision; Chapter V: Mental and behavioral disorders (F81.2) Geneva, World Health Organization; 2005.
    1. Shalev RS, Auerbach J, Manor O, Gross-Tsur V. Developmental dyscalculia: prevalence and prognosis. Eur Child Adolesc Psychiatry. 2000;9 Suppl 2:II58–64. doi: 10.1007/s007870070009.
    1. Lewis C, Hitch GJ, Walker P. The prevalence of specific arithmetic difficulties and specific reading difficulties in 9- to 10-year-old boys and girls. J Child Psychol Psychiatry. 1994;35:283–292.
    1. Shalev RS, Manor O, Gross-Tsur V. Developmental dyscalculia: a prospective six-year follow-up. Dev Med Child Neurol. 2005;47:121–125. doi: 10.1017/S0012162205000216.
    1. Ardila A, Rosselli M. Acalculia and dyscalculia. Neuropsychol Rev. 2002;12:179–231. doi: 10.1023/A:1021343508573.
    1. Monuteaux MC, Faraone SV, Herzig K, Navsaria N, Biederman J. ADHD and dyscalculia: Evidence for independent familial transmission. J Learn Disabil. 2005;38:86–93.
    1. Reiss AL, Eliez S, Schmitt JE, Patwardhan A, Haberecht M. Brain imaging in neurogenetic conditions: realizing the potential of behavioral neurogenetics research. Ment Retard Dev Disabil Res Rev. 2000;6:186–197. doi: 10.1002/1098-2779(2000)6:3<186::AID-MRDD6>;2-9.
    1. Rosenberg PB. Perceptual-motor and attentional correlates of developmental dyscalculia. Ann Neurol. 1989;26:216–220. doi: 10.1002/ana.410260206.
    1. Shalev RS. Developmental dyscalculia. J Child Neurol. 2004;19:765–771.
    1. Alarcon M, DeFries JC, Light JG, Pennington BF. A twin study of mathematics disability. J Learn Disabil. 1997;30:617–623.
    1. Schweiter M, Weinhold Zulauf M, von Aster MG. Die Entwicklung räumlicher Zahlenrepräsentationen und Rechenfertigkeiten bei Kindern. Zeitschrift für Neuropsychologie. 2005;16:105–113. doi: 10.1024/1016-264X.16.2.105.
    1. Dellatolas G, von Aster MG, Willadino-Braga L, Meier M, Deloche G. Number processing and mental calculation in school children aged 7 to 10 years: a transcultural comparison. Eur child Adolesc Psychiatry. 2000;9:102–110. doi: 10.1007/s007870070003.
    1. Shalev RS, Gross-Tsur V. Developmental dyscalculia. Pediatr Neurol. 2001;24:337–342. doi: 10.1016/S0887-8994(00)00258-7.
    1. Shalev RS, Manor O, Kerem B, Ayali M, Badichi N, Friedlander Y, Gross-Tsur V. Developmental dyscalculia is a familial learning disability. J Learn Disabil. 2001;34:59–65.
    1. Burbaud P, Degreze P, Lafon P, Franconi JM, Bouligand B, Bioulac B, Caille JM, Allard M. Lateralization of prefrontal activation during internal mental calculation: a functional magnetic resonance imaging study. J Neurophysiol. 1995;74:2194–2200.
    1. Dehaene S, Spelke E, Pinel P, Stanescu R, Tsivkin S. Sources of mathematical thinking: behavioral and brain-imaging evidence. Science. 1999;284:970–974. doi: 10.1126/science.284.5416.970.
    1. Menon V, Rivera SM, White CD, Glover GH, Reiss AL. Dissociating prefrontal and parietal cortex activation during arithmetic processing. NeuroImage. 2000;12:357–365. doi: 10.1006/nimg.2000.0613.
    1. Pesenti M, Thioux M, Seron X, De Volder A. Neuroanatomical substrates of arabic number processing, numerical comparison, and simple addition: a PET study. J Cogn Neurosci. 2000;12:461–479. doi: 10.1162/089892900562273.
    1. Rickard TC, Romero SG, Basso G, Wharton C, Flitman S, Grafman J. The calculating brain: an fMRI study. Neuropsychologia. 2000;38:325–335. doi: 10.1016/S0028-3932(99)00068-8.
    1. Schmithorst VJ, Brown RD. Empirical validation of the triple-code model of numerical processing for complex math operations using functional MRI and group Independent Component Analysis of the mental addition and subtraction of fractions. NeuroImage. 2004;22:1414–1420. doi: 10.1016/j.neuroimage.2004.03.021.
    1. Dehaene S, Piazza M, Pinel P, Cohen JD. Three Parietal Circuits for Number Processing. Cogn Neuropsychol. 2003;20:487–506. doi: 10.1080/02643290244000239.
    1. Dehaene S. Varieties of numerical abilities. Cognition. 1992;44:1–42. doi: 10.1016/0010-0277(92)90049-N.
    1. Dehaene S, Cohen JD. Towards an anatomical and functional model of number processing. Mathematical Cognition. 1995;1:83–120.
    1. Stanescu-Cosson R, Pinel P, van De Moortele PF, Le Bihan D, Cohen L, Dehaene S. Understanding dissociations in dyscalculia: a brain imaging study of the impact of number size on the cerebral networks for exact and approximate calculation. Brain. 2000;123 ( Pt 11):2240–2255. doi: 10.1093/brain/123.11.2240.
    1. Lemer C, Dehaene S, Spelke E, Cohen L. Approximate quantities and exact number words: dissociable systems. Neuropsychologia. 2003;41:1942–1958. doi: 10.1016/S0028-3932(03)00123-4.
    1. Takayama Y, Sugishita M, Akiguchi I, Kimura J. Isolated acalculia due to left parietal lesion. Arch Neurol. 1994;51:286–291.
    1. Dehaene S, Cohen L. Cerebral pathways for calculation: double dissociation between rote verbal and quantitative knowledge of arithmetic. Cortex. 1997;33:219–250.
    1. Cohen L, Dehaene S, Chochon F, Lehéricy S, Naccache L. Language and calculation within the parietal lobe: a combined cognitive, anatomical and fMRI study. Neuropsychologia. 2000;38:1426–1440. doi: 10.1016/S0028-3932(00)00038-5.
    1. Venkatraman V, Ansari D, Chee MW. Neural correlates of symbolic and non-symbolic arithmetic. Neuropsychologia. 2005;43:744–753. doi: 10.1016/j.neuropsychologia.2004.08.005.
    1. Molko N, Cachia A, Riviere D, Mangin JF, Bruandet M, Le Bihan D, Cohen L, Dehaene S. Functional and structural alterations of the intraparietal sulcus in a developmental dyscalculia of genetic origin. Neuron. 2003;40:847–858. doi: 10.1016/S0896-6273(03)00670-6.
    1. van Harskamp NJ, Rudge P, Cipolotti L. Are multiplication facts implemented by the left supramarginal and angular gyri? Neuropsychologia. 2002;40:1786–1793. doi: 10.1016/S0028-3932(02)00036-2.
    1. Rivera SM, Menon V, White CD, Glaser B, Reiss AL. Functional brain activation during arithmetic processing in females with fragile X Syndrome is related to FMR1 protein expression. Hum Brain Mapp. 2002;16:206–218. doi: 10.1002/hbm.10048.
    1. Levin HS, Scheller J, Rickard T, Grafman J, Martinkowski K, Winslow M, Mirvis S. Dyscalculia and dyslexia after right hemisphere injury in infancy. Arch Neurol. 1996;53:88–96.
    1. Levy LM, Reis IL, Grafman J. Metabolic abnormalities detected by 1H-MRS in dyscalculia and dysgraphia. Neurology. 1999;53:639–641.
    1. Molko N, Cachia A, Riviere D, Mangin JF, Bruandet M, LeBihan D, Cohen L, Dehaene S. Brain anatomy in Turner syndrome: evidence for impaired social and spatial-numerical networks. Cereb Cortex. 2004;14:840–850. doi: 10.1093/cercor/bhh042.
    1. Isaacs EB, Edmonds CJ, Lucas A, Gadian DG. Calculation difficulties in children of very low birthweight: a neural correlate. Brain. 2001;124:1701–1707. doi: 10.1093/brain/124.9.1701.
    1. Kucian K, Loenneker T, Dietrich T, Martin E, von Aster MG. Development of Neural Networks for Number Processing: an fMRI Study in Children and Adults [abstract] NeuroImage. 2005;26:46.
    1. WMA . The World Medical Association’s Declaration of Helsinki: Ethical Principles for Medical Research Involving Human Subjects. Washington, WMA General Assembly; 2002.
    1. von Aster MG. ZAREKI (Neuropsychological Test Battery for Number Processing and Calculation in Children) Lisse, Frankfurt am Main, Swets & Zeitlinger; 2001.
    1. Kaufman AS, Kaufman NL. In: Kaufman-assessment battery for children (K-ABC) al. DFPM, editor. Frankfurt a.M., Swets & Zeitlinger; 1994.
    1. Wechsler D. In: Hamburg-Wechsler-Intelligenztest für Kinder III (HAWIK-III) / Übersetzung und Adaption der WISC-III von David Wechsler. al. UT, editor. Bern, Hans Huber; 1999.
    1. Klassencockpit . MS_Deutsch_61, MS_Mathematik_61. Rorschach, Kantonaler Lehrmittelverlag St. Gallen; 2004.
    1. Marx H. Knuspels Leseaufgaben. Gruppenlesetest für Kinder Ende des ersten bis vierten Schuljahres. Göttingen, Hogrefe; 1998.
    1. Landerl K, Wimmer H, Moser E. Salzburger Lese- und Rechtschreibtest. Verfahren zur Differentialdiagnose von Störungen des Lesens und Schreibens für die 1. bis 4. Schulstufe. Bern, Huber; 1997.
    1. SPSS for Windows, Statistical Product and Service Solution. 11.5. Chicago, USA, SPSS Inc.; 2002.
    1. Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage. 2002;15:870–878. doi: 10.1006/nimg.2001.1037.
    1. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, Kochunov PV, Nickerson D, Mikiten SA, Fox PT. Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp. 2000;10:120–131. doi: 10.1002/1097-0193(200007)10:3<120::AID-HBM30>;2-8.
    1. Talairach J, Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging. Stuttgart, Thieme Medical Publisher; 1988.
    1. Cohen J. Statistical Power Analysis for the Behavioral Sciences. 2. Hillsdale, NJ, Lawrence Erlbaum; 1988.
    1. D'Amico EJ, Neilands TB, Zambarano R. Power analysis for multivariate and repeated measures designs: a flexible approach using the SPSS MANOVA procedure. Behav Res Methods Instrum Comput. 2001;33:479–484.
    1. Kwon H, Menon V, Eliez S, Warsofsky IS, White CD, Dyer-Friedman J, Taylor AK, Glover GH, Reiss AL. Functional neuroanatomy of visuospatial working memory in fragile X syndrome: relation to behavioral and molecular measures. Am J Psychiatry. 2001;158:1040–1051. doi: 10.1176/appi.ajp.158.7.1040.
    1. Shalev RS, Manor O, Amir N, Wertman-Elad R, Gross-Tsur V. Developmental dyscalculia and brain laterality. Cortex. 1995;31:357–365.
    1. Berl MM, Vaidya CJ, Gaillard WD. Functional imaging of developmental and adaptive changes in neurocognition. NeuroImage. 2006;30:679–691. doi: 10.1016/j.neuroimage.2005.10.007.
    1. Martins IP, Ferreira J, Borges L. Acquired procedural dyscalculia associated to a left parietal lesion in a child. Child Neuropsychol. 1999;5:265–273.
    1. Dehaene S, Bossini S, Giraux P. The mental representation of parity and number magnitude. J Exp Psychol. 1993;122:371–396.
    1. Berch DB, Foley EJ, Hill RJ, McDonough Ryan P. Extracting Parity and Magnitude from Arabic Numerals: Developmental Changes in Number Processing and Mental Representation. J Exp Child Psychol. 1999;74:286–308. doi: 10.1006/jecp.1999.2518.
    1. Bachot J, Gevers W, Fias W, Roeyers H. Number sense in children with visuospatial disabilities: orientation of the mental number line. Psychology Science. 2005;47:172–183.
    1. Rubinsten O, Henik A. Automatic activation of internal magnitudes: a study of developmental dyscalculia. Neuropsychology. 2005;19:641–648. doi: 10.1037/0894-4105.19.5.641.
    1. Koontz KL, Berch DB. Identifying Simple Numerical Stimuli: Processing Inefficiencies Exhibited by Arithmetic Learning Disabled Children. Mathematical Cognition. 1996;2:1–24. doi: 10.1080/135467996387525.
    1. Kawashima R, Taira M, Okita K, Inoue K, Tajima N, Yoshida H, Sasaki T, Sugiura M, Watanabe J, Fukuda H. A functional MRI study of simple arithmetic--a comparison between children and adults. Brain Res Cogn Brain Res. 2004;18:227–233. doi: 10.1016/j.cogbrainres.2003.10.009.
    1. Rivera SM, Reiss AL, Eckert MA, Menon V. Developmental Changes in Mental Arithmetic: Evidence for Increased Functional Specialization in the Left Inferior Parietal Cortex. Cereb Cortex. 2005
    1. Burbaud P, Camus O, Guehl D, Bioulac B, Caille J, Allard M. Influence of cognitive strategies on the pattern of cortical activation during mental subtraction. A functional imaging study in human subjects. Neurosci Lett. 2000;287:76–80. doi: 10.1016/S0304-3940(00)01099-5.
    1. Gura T. Educational research: big plans for little brains. Nature. 2005;435:1156–1158. doi: 10.1038/4351156a.

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