Time-resolved and spatio-temporal analysis of complex cognitive processes and their role in disorders like developmental dyscalculia
Corresponding Author
István Ákos Mórocz
Department of Radiology, Harvard Medical School, Brigham and Women's Hospital, Boston, MA 02445
Department of Neurobiology, Weizmann Institute of Sciences, Rehovot, Israel
The Edmond J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Israel
Department of Radiology, Harvard Medical School, Brigham and Women's Hospital, Boston, MA 02445Search for more papers by this authorFirdaus Janoos
Department of Radiology, Harvard Medical School, Brigham and Women's Hospital, Boston, MA 02445
Search for more papers by this authorPeter van Gelderen
Advanced MRI, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorDavid Manor
Department of Diagnostic Imaging, Sheba Medical Center, Tel Hashomer, Israel
Search for more papers by this authorAvi Karni
The Edmond J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Israel
Department of Diagnostic Imaging, Sheba Medical Center, Tel Hashomer, Israel
Search for more papers by this authorZvia Breznitz
The Edmond J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Israel
Search for more papers by this authorMichael von Aster
Department of Child and Adolescent Psychiatry, German Red Cross Hospitals, Berlin, Germany
Search for more papers by this authorTammar Kushnir
Department of Diagnostic Imaging, Sheba Medical Center, Tel Hashomer, Israel
Search for more papers by this authorRuth Shalev
Department of Pediatric Neurology, Shaare Zedek Medical Center, Jerusalem, Israel
Search for more papers by this authorCorresponding Author
István Ákos Mórocz
Department of Radiology, Harvard Medical School, Brigham and Women's Hospital, Boston, MA 02445
Department of Neurobiology, Weizmann Institute of Sciences, Rehovot, Israel
The Edmond J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Israel
Department of Radiology, Harvard Medical School, Brigham and Women's Hospital, Boston, MA 02445Search for more papers by this authorFirdaus Janoos
Department of Radiology, Harvard Medical School, Brigham and Women's Hospital, Boston, MA 02445
Search for more papers by this authorPeter van Gelderen
Advanced MRI, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorDavid Manor
Department of Diagnostic Imaging, Sheba Medical Center, Tel Hashomer, Israel
Search for more papers by this authorAvi Karni
The Edmond J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Israel
Department of Diagnostic Imaging, Sheba Medical Center, Tel Hashomer, Israel
Search for more papers by this authorZvia Breznitz
The Edmond J. Safra Brain Research Center for the Study of Learning Disabilities, University of Haifa, Israel
Search for more papers by this authorMichael von Aster
Department of Child and Adolescent Psychiatry, German Red Cross Hospitals, Berlin, Germany
Search for more papers by this authorTammar Kushnir
Department of Diagnostic Imaging, Sheba Medical Center, Tel Hashomer, Israel
Search for more papers by this authorRuth Shalev
Department of Pediatric Neurology, Shaare Zedek Medical Center, Jerusalem, Israel
Search for more papers by this authorAbstract
The aim of this article is to report on the importance and challenges of a time-resolved and spatio-temporal analysis of fMRI data from complex cognitive processes and associated disorders using a study on developmental dyscalculia (DD). Participants underwent fMRI while judging the incorrectness of multiplication results, and the data were analyzed using a sequence of methods, each of which progressively provided more a detailed picture of the spatio-temporal aspect of this disease. Healthy subjects and subjects with DD performed alike behaviorally, though they exhibited parietal disparities using traditional “voxel-based” group analyses. Further and more detailed differences, however, surfaced with a “time-resolved” examination of the neural responses during the experiment. While performing intergroup comparisons, a third group of subjects with dyslexia but with no arithmetic difficulties was included to test the specificity of the analysis and strengthen the statistical base with overall 58 subjects. Surprisingly, the analysis showed a functional dissimilarity during an initial reading phase for the group of dyslexic but otherwise normal subjects, with respect to controls, though only numerical digits and no alphabetic characters were presented. Thus, our results suggest that “time-resolved multivariate” analysis of complex experimental paradigms has the ability to yield powerful new clinical insights about abnormal brain function. Similarly, a detailed compilation of aberrations in the functional cascade may have much greater potential to delineate the core processing problems in mental disorders. © 2012 Wiley Periodicals, Inc. Int J Imaging Syst Technol, 22, 81–96, 2012
Supporting Information
Additional Supporting Information may be found in the online version of this article.
Filename | Description |
---|---|
IMA_22009_sm_SuppInfo.pdf87.7 KB | Supporting Information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- O. Afacan,W.S. Hoge,F. Janoos,D. Brooks, andI.Á. Mórocz, Rapid fullbrain fMRI with an accelerated multi-shot 3D-EPI sequence using both UNFOLD and GRAPPA. Magn Reson Med (in press).
- G. Allen,R.B. Buxton,E.C. Wong, andE. Courchesne, Attentional activation of the cerebellum independent of motor involvement. Science 275 ( 1997), 1940–1943.
- J.R. Andrews-Hanna,J.S. Reidler,J. Sepulcre,R. Poulin, andR.L. Buckner, Functional-anatomic fractionation of the brain's default network. Neuron 65 ( 2010), 550–562.
- D. Ansari andA. Karmiloff-Smith, Atypical trajectories of number development: A neuroconstructivist perspective. Trends Cogn Sci 6 ( 2002) 511–516.
- N. Barnea-Goraly,S. Eliez,V. Menon,R. Bammer, andA.L. Reiss, Arithmetic ability and parietal alterations: A diffusion tensor imaging study in velocardiofacial syndrome. Brain Res Cogn Brain Res 25 ( 2005), 735–740.
- T. Bitan,A. Lifshitz,Z. Breznitz, andJ.R. Booth, Bidirectional connectivity between hemispheres occurs at multiple levels in language processing but depends on sex. J Neurosci 30 ( 2010), 11576–11585.
- M. Botvinick,L.E. Nystrom,K. Fissell,C.S. Carter, andJ.D. Cohen, Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402 ( 1999), 179–181.
- Z. Breznitz andM. Misra, Speed of processing of the visual-orthographic and auditory-phonological systems in adult dyslexics: The contribution of ”asynchrony” to word recognition deficits. Brain Lang 85 ( 2003), 486–502.
- J.W. Brown andT.S. Braver, Learned predictions of error likelihood in the anterior cingulate cortex. Science 307 ( 2005), 1118–21.
- G. Bush,P. Luu, andM.I. Posner, Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4 ( 2000), 215–222.
- B. Butterworth, Foundational numerical capacities and the origins of dyscalculia. Trends Cogn Sci 14 ( 2010), 534–541.
- B. Butterworth,S. Varma, andD. Laurillard, Dyscalculia: From brain to education. Science 332 ( 2011), 1049–1053.
- G. Buzsáki, Rhythms of the brain, Oxford University Press, Inc., New York, NY, 2005.
- J.I. Campbell andD.P. Tarling, Retrieval processes in arithmetic production and verification. Mem Cognit 24 ( 1996), 156–172.
- C.S. Carter,T.S. Braver,D.M. Barch,M.M. Botvinick,D. Noll, andJ.D. Cohen, Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280 ( 1998), 747–749.
- D. Chawla,G. Rees, andK.J. Friston, The physiological basis of attentional modulation in extrastriate visual areas. Nat Neurosci 2 ( 1999), 671–676.
- S.H.A. Chen andJ.E. Desmond, Cerebrocerebellar networks during articulatory rehearsal and verbal working memory tasks. Neuroimage 24 ( 2005), 332–338.
- S. Cho,S. Ryali,D.C. Geary, andV. Menon, How does a child solve 7+8? Decoding brain activity patterns associated with counting and retrieval strategies. Dev Sci 14 ( 2011), 989–1001.
- F. Chochon,L. Cohen,P.F. van de Moortele, andS. Dehaene, Differential contributions of the left and right inferior parietal lobules to number processing. J Cogn Neurosci 11 ( 1999), 617–630.
- R. Cohen-Kadosh,S. Soskic,T. Iuculano,R. Kanai, andV. Walsh, Modulating neuronal activity produces specific and long-lasting changes in numerical competence. Curr Biol 20 ( 2010), 2016–2020.
- M. Corbetta andG.L. Shulman, Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3 ( 2002), 201–215.
- S. Dehaene andL. Cohen, Towards an anatomical and functional model of number processing. Math Cogn 1 ( 1995), 83–120.
- S. Dehaene,M. Piazza,P. Pinel, andL. Cohen, Three parietal circuits for number processing. Cogn Neuropsychol 20 ( 2003), 487–506.
- S. Dehaene,E. Spelke,P. Pinel,R. Stanescu, andS. Tsivkin, Sources of mathematical thinking: Behavioral and brain-imaging evidence. Science 284 ( 1999), 970–974.
- M. Delazer andB. Butterworth, A dissociation of number meaning. Cogn Neuropsychol 14 ( 1997), 613–636.
- J. Duncan andA. Owen, Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci 23 ( 2000), 475–483.
- E. Eger,P. Sterzer,M.O. Russ,A.-L. Giraud, andA. Kleinschmidt, A supramodal number representation in human intraparietal cortex. Neuron 37 ( 2003), 719–725.
- S. Eliez,C. Blasey,V. Menon,C. White,J. Schmitt, andA. Reiss, Functional brain imaging study of mathematical reasoning abilities in velocardiofacial syndrome (del22q11.2). Genet Med 3 ( 2001), 49–55.
- L. Feigenson,S. Dehaene, andE. Spelke, Core systems of number. Trends Cogn Sci 8 ( 2004), 307–14.
- J.A. Fiez, Cerebellar contributions to cognition. Neuron 16 ( 1996), 13–15.
- J.A. Fiez andS.E. Petersen, Neuroimaging studies of word reading. Proc Natl Acad Sci USA 95 ( 1998), 914–921.
-
K. Friston, J. Ashburner, S. Kiebel, T. Nichols, and W. Penny (Editors),
Statistical parametric mapping: The analysis of functional brain images,
Academic Press,
Elsevier, Maryland Heights, MO,
2007.
10.1016/B978-012372560-8/50002-4 Google Scholar
- K. Friston,C. Chu,J. Mourão-Miranda,O. Hulme,G. Rees,W. Penny, andJ. Ashburner, Bayesian decoding of brain images. Neuroimage 39 ( 2008), 181–205.
- D.C. Geary, Mathematical learning disabilities. Adv Child Dev Behav 39 ( 2010), 45–77.
- U. Goswami andD. Szücs, Educational neuroscience: Developmental mechanisms: Towards a conceptual framework. Neuroimage 57 ( 2011), 651–658.
- B. Gottwald,B. Wilde,Z. Mihajlovic, andH.M. Mehdorn, Evidence for distinct cognitive deficits after focal cerebellar lesions. J Neurol Neurosurg Psychiatry 75 ( 2004), 1524–1531.
- C.B. Grandin,D.P. Madio,P. van Gelderen, andC.T.W. Moonen, Reduction of undesirable signal of large veins in functional MRI with PRESTO, Proc. ESMRMB 14th Ann Meeting, Vol. 54, Brussels, Belgium, 1997, pp. 14.
- C.B. Holroyd,S. Nieuwenhuis,N. Yeung,L. Nystrom,R.B. Mars,M.G.H. Coles, andJ.D. Cohen, Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals. Nat Neurosci 7 ( 2004), 497–498.
- P.D. Howe,T.S. Horowitz,I.A. Mórocz,J. Wolfe, andM.S. Livingstone, Using fmri to distinguish components of the multiple object tracking task. J Vis 9 ( 2009), 1–11.
- E.B. Isaacs,C.J. Edmonds,A. Lucas, andD.G. Gadian, Calculation difficulties in children of very low birthweight: A neural correlate. Brain 124 ( 2001), 1701–1707.
- F. Janoos, W.M. Wells, I.Á. Mórocz, and G.G. Brown, State-space analysis of working memory in schizophrenia—An fBIRN study (submitted for publication in Psychometrika).
- F. Janoos,R. Machiraju,S. Singh, andI.Á. Mórocz, Spatio-temporal models of mental processes from fMRI. Neuroimage 57 ( 2011a), 362–377.
- F. Janoos,S. Singh,R. Machiraju,W.M. Wells, andI.Á. Mórocz, Statespace models of mental processes from fMRI. Inf Process Med Imaging 22 ( 2011b), 588–599.
- S.M. Jones,J.F. Cantlon,D.J. Merritt, andE.M. Brannon, Context affects the numerical semantic congruity effect in rhesus monkeys (macaca mulatta). Behav Processes 83 ( 2010), 191–196.
- N. Kanwisher andE. Wojciulik, Visual attention: Insights from brain imaging. Nat Rev Neurosci 1 ( 2000), 91–100.
- L. Kaufmann,G. Wood,O. Rubinsten, andA. Henik, Meta-analyses of developmental fMRI studies investigating typical and atypical trajectories of number processing and calculation. Dev Neuropsychol 36 ( 2011), 763–787.
- J.G. Kerns,J.D. Cohen,I.A.W. MacDonald,R.Y. Cho,V.A. Stenger, andC.S. Carter, Anterior cingulate conflict monitoring and adjustments in control. Science 303 ( 2004), 1023–1026.
- D.C. Krawczyk, Contributions of the prefrontal cortex to the neural basis of human decision making. Neurosci Biobehav Rev 26 ( 2002), 631–664.
- F. Kruggel,S. Zysset, andD.Y. von Cramon, Nonlinear regression of functional MRI data: An item recognition task study. Neuroimage 12 ( 2000), 173–183.
- K. Kucian,T. Loenneker,T. Dietrich,M. Dosch,E. Martin, andM. von Aster, Impaired neural networks for approximate calculation in dyscalculic children: A functional MRI study. Behav Brain Funct 2 ( 2006), 31.
- K. Kucian,M. von Aster,T. Loenneker,T. Dietrich, andE. Martin, Development of neural networks for exact and approximate calculation: A fMRI study. Dev Neuropsychol 33 ( 2008), 447–473.
- H.C. Lau,R.D. Rogers,P. Haggard, andR.E. Passingham, Attention to intention. Science 303 ( 2004), 1208–1210.
- D. Lehmann,R.D. Pascual-Marqui,W.K. Strik, andT. Koenig, Core networks for visual-concrete and abstract thought content: A brain electric microstate analysis. Neuroimage 49 ( 2010), 1073–1079.
- L.M. Levy,I.L. Reis, andJ. Grafman, Metabolic abnormalities detected by 1H-MRS in dyscalculia and dysgraphia. Neurology 53 ( 1999), 639–641.
- F.-H. Lin,T. Witzel,J.B. Mandeville,J.R. Polimeni,T.A. Zeffiro,D.N. Greve,G. Wiggins,L.L. Wald, andJ.W. Belliveau, Event-related singleshot volumetric functional magnetic resonance inverse imaging of visual processing. Neuroimage 42 ( 2008), 230–247.
- M.S. Livingstone,K. Srihasam, andI.Á. Mórocz, The benefit of symbols: monkeys show linear, human-like, accuracy when using symbols to represent scalar value. Anim Cogn 13 ( 2010), 711–719.
- A.W. MacDonald,J.D. Cohen,V.A. Stenger, andC.S. Carter, Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288 ( 2000), 1835–1838.
- D.S. Manoach,N.S. White,K.A. Lindgren,S. Heckers,M.J. Coleman,S. Dubal, andP.S. Holzman, Hemispheric specialization of the lateral prefrontal cortex for strategic processing during spatial and shape working memory. Neuroimage 21 ( 2004), 894–903.
- K. Mathiak,I. Hertrich,W. Grodd, andH. Ackermann, Discrimination of temporal information at the cerebellum: Functional magnetic resonance imaging of nonverbal auditory memory. Neuroimage 21 ( 2004), 154–162.
- B. McCandliss,L. Cohen, andS. Dehaene, The visual word form area: Expertise for reading in the fusiform gyrus. Trends Cogn Sci 7 ( 2003), 293–299.
- K. McCrink andE.S. Spelke, Core multiplication in childhood. Cognition 116 ( 2010), 204–216.
- A.W.S. Metcalfe andJ.I.D. Campbell, Adults' strategies for simple addition and multiplication: Verbal self-reports and the operand recognition paradigm. J Exp Psychol Learn Mem Cogn 37 ( 2011), 661–672.
- E. Miller andJ. Cohen, An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24 ( 2001), 167–202.
- T.M. Mitchell,S.V. Shinkareva,A. Carlson,K.-M. Chang,V.L. Malave,R.A. Mason, andM.A. Just, Predicting human brain activity associated with the meanings of nouns. Science 320 ( 2008), 1191–1195.
- N. Molko,A. Cachia,D. Riviere,J.F. Mangin,M. Bruandet,D. LeBihan,L. Cohen, andS. Dehaene, Functional and structural alterations of the intraparietal sulcus in a developmental dyscalculia of genetic origin. Neuron 40 ( 2003), 847–858.
- S.O. Murray andE. Wojciulik, Attention increases neural selectivity in the human lateral occipital complex. Nat Neurosci 7 ( 2004), 70–74.
- A. Nieder, Counting on neurons: The neurobiology of numerical competence. Nat Rev Neurosci 6 ( 2005), 177–190.
- A. Nieder andS. Dehaene, Representation of number in the brain. Annu Rev Neurosci 32 ( 2009), 185–208.
- A. Nieder andE.K. Miller, A parieto-frontal network for visual numerical information in the monkey. Proc Natl Acad Sci USA 101 ( 2004), 7457–7462.
- M. Piazza, Neurocognitive start-up tools for symbolic number representations. Trends Cogn Sci 14 ( 2010), 542–551.
- N. Picard andP. Strick, Imaging the premotor areas. Curr Opin Neurobiol 11 ( 2001), 663–72.
- P. Pinel,S. Dehaene,D. Riviere, andD. LeBihan, Modulation of parietal activation by semantic distance in a number comparison task. Neuroimage 14 ( 2001), 1013–1026.
- N.F. Ramsey,J.S. van den Brink,A.M. van Muiswinkel,P.J. Folkers,C.T. Moonen,J.M. Jansma, andR.S. Kahn, Phase navigator correction in 3D fMRI improves detection of brain activation: Quantitative assessment with a graded motor activation procedure. Neuroimage 8 ( 1998), 240–248.
- S.M. Ravizza,C.A. McCormick,J.E. Schlerf,T. Justus,R.B. Ivry, andJ.A. Fiez, Cerebellar damage produces selective deficits in verbal working memory. Brain 129 ( 2006), 306–320.
- T.C. Rickard,S.G. Romero,G. Basso,C. Wharton,S.S. Flitman, andJ. Grafman, The calculating brain: An fMRI study. Neuropsychologia 38 ( 2000), 325–335.
- K.R. Ridderinkhof,M. Ullsperger,E.A. Crone, andS. Nieuwenhuis, The role of the medial frontal cortex in cognitive control. Science 306 ( 2004), 443–447.
- S. Rotzer,K. Kucian,E. Martin,M. von Aster,P. Klaver, andT. Loenneker, Optimized voxel-based morphometry in children with developmental dyscalculia. Neuroimage 39 ( 2008), 417–422.
- S. Rotzer,T. Loenneker,K. Kucian,E. Martin,P. Klaver, andM. von Aster, Dysfunctional neural network of spatial working memory contributes to developmental dyscalculia. Neuropsychologia 47 ( 2009), 2859–2865.
- F.E. Roux,S. Boetto,O. Sacko,F. Chollet, andM. Tremoulet, Writing, calculating, and finger recognition in the region of the angular gyrus: A cortical stimulation study of Gerstmann syndrome. J Neurosurg 99 ( 2003), 716–727.
- C. Ruff,T. Woodward,K. Laurens, andP. Liddle, The role of the anterior cingulate cortex in conflict processing: evidence from reverse stroop interference. Neuroimage 14 ( 2001), 1150–1158.
- H. Sawamura,K. Shima, andJ. Tanji, Numerical representation for action in the parietal cortex of the monkey. Nature 415 ( 2002), 918–922.
- J.D. Schmahmann andJ.C. Sherman, The cerebellar cognitive affective syndrome. Brain 121 (Pt 4) ( 1998), 561–579.
- R.S. Shalev andV. Gross-Tsur, Developmental dyscalculia. Pediatr Neurol 24 ( 2001), 337–342.
- M. Shuman andN. Kanwisher, Numerical magnitude in the human parietal lobe; tests of representational generality and domain specificity. Neuron 44 ( 2004), 557–569.
- O. Simon,J.F. Mangin,L. Cohen,D. LeBihan, andS. Dehaene, Topographical layout of hand, eye, calculation, and language-related areas in the human parietal lobe. Neuron 33 ( 2002), 475–487.
- D.C. Somers,A.M. Dale,A.E. Seiffert, andR.B. Tootell, Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. Proc Natl Acad Sci USA 96 ( 1999), 1663–1668.
- R. Stanescu-Cosson,P. Pinel,P.F. van De Moortele,D. LeBihan,L. Cohen, andS. Dehaene, Understanding dissociations in dyscalculia: A brain imaging study of the impact of number size on the cerebral networks for exact and approximate calculation. Brain 123 ( 2000), 2240–2255.
- M. Thioux,M. Pesenti,N. Costes,A.D. Volder, andX. Seron, Taskindependent semantic activation for numbers and animals. Brain Res Cogn Brain Res 24 ( 2005), 284–90.
- I. Toni,N.J. Shah,G.R. Fink,D. Thoenissen,R.E. Passingham, andK. Zilles, Multiple movement representations in the human brain: An event-related fMRI study. J Cogn Neurosci 14 ( 2002), 769–784.
- P. van Gelderen,N.F. Ramsey,G. Liu,J.H. Duyn,J.A. Frank,D.R. Weinberger, andC.T. Moonen, Three-dimensional functional magnetic resonance imaging of human brain on a clinical 1.5T scanner. Proc Natl Acad Sci USA 92 ( 1995), 6906–6910.
- H.T. van Schie,R.B. Mars,M.G.H. Coles, andH. Bekkering, Modulation of activity in medial frontal and motor cortices during error observation. Nat Neurosci 7 ( 2004), 549–554.
- P. Verstichel andC. Masson, ‘Acalculie progressive’: Variété d'atrophie dégénérative focale affectant le traitement de nombres. Rev Neurol 159 ( 2003), 413–420.
- M.G. von Aster andR.S. Shalev, Number development and developmental dyscalculia. Dev Med Child Neurol 49 ( 2007), 868–873.
- M.E. Walton,J.T. Devlin, andM.F.S. Rushworth, Interactions between decision making and performance monitoring within prefrontal cortex. Nat Neurosci 7 ( 2004), 1259–1265.
- WHO, ICD10. International statistical classification of diseases and related health problems 10th Revision, Chapter V: Mental and behavioral disorders (F81.2), World Health Organization, Geneva, Switzerland, 2005.
- S.M. Wilson,A.P. Saygin,M.I. Sereno, andM. Iacoboni, Listening to speech activates motor areas involved in speech production. Nat Neurosci 7 ( 2004), 701–702.
- K.J. Worsley,C.H. Liao,J. Aston,V. Petre,G.H. Duncan,F. Morales, andA.C. Evans, A general statistical analysis for fMRI data. Neuroimage 15 ( 2002), 1–15.
- L. Zago,M. Pesenti,E. Mellet,F. Crivello,B.M. Mazoyer, andN. Tzourio-Mazoyer, Neural correlates of simple and complex mental calculation. Neuroimage 13 ( 2001), 314–327.