The Role of Finger Representations and Saccades for Number Processing: An fMRI Study in Children

A possible functional role of finger representations for the development of early numerical cognition has been the subject of recent debate; however, until now, only behavioral studies have directly supported this view. Working from recent models of number processing, we focused on the neural networks involved in numerical tasks and their relationship to the areas underlying finger representations and saccades in children aged 6–12 years. We were able to differentiate three parietal circuits that were related to distinct aspects of number processing. Abstract magnitude processing was subserved by an association area also activated by saccades and visually guided finger movements. Addition processes led to activation in an area only engaged during saccade encoding, whereas counting processes resulted in the activation of an area only activated during visually guided finger movements, namely in the anterior intraparietal sulcus. Apart from this area, a large network of specifically finger-related brain areas including the ventral precentral sulcus, supplementary motor area, dorso-lateral prefrontal cortex, insula, thalamus, midbrain, and cerebellum was activated during (particularly non-symbolic) exact addition but not during magnitude comparison. Moreover, a finger-related activation cluster in the right ventral precentral sulcus was only present during non-symbolic addition and magnitude comparison, but not during symbolic number processing tasks. We conclude that finger counting may critically mediate the step from non-symbolic to symbolic and exact number processing via somatosensory integration processes and therefore represents an important example of embodied cognition.

[1]  Guilherme Wood,et al.  A developmental fMRI study of nonsymbolic numerical and spatial processing , 2008, Cortex.

[2]  Michael Andres,et al.  Actions, Words, and Numbers , 2008 .

[3]  Mark Hallett,et al.  The role of the human ventral premotor cortex in counting successive stimuli , 2007, Experimental Brain Research.

[4]  V. Michel,et al.  Recruitment of an Area Involved in Eye Movements During Mental Arithmetic , 2009, Science.

[5]  L. Barsalou,et al.  Embodiment in Attitudes, Social Perception, and Emotion , 2005, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[6]  J. Raven Coloured progressive matrices : sets A, Ab, B , 1956 .

[7]  Michael Andres,et al.  Mode-dependent and mode-independent representations of numerosity in the right intraparietal sulcus , 2010, NeuroImage.

[8]  Mauro Pesenti,et al.  Place and summation coding for canonical and non-canonical finger numeral representations , 2010, Cognition.

[9]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[10]  M. Noël,et al.  Does finger training increase young children's numerical performance? , 2008, Cortex.

[11]  S. Dehaene,et al.  A Magnitude Code Common to Numerosities and Number Symbols in Human Intraparietal Cortex , 2007, Neuron.

[12]  P. Pietrini,et al.  Conjoint and extended neural networks for the computation of speech codes: the neural basis of selective impairment in reading words and pseudowords. , 2001, Cerebral cortex.

[13]  John H. Martin Neuroanatomy: Text and Atlas , 1989 .

[14]  Richard F. Thompson,et al.  Number Coding in Association Cortex of the Cat , 1970, Science.

[15]  E. Brannon,et al.  Monotonic Coding of Numerosity in Macaque Lateral Intraparietal Area , 2007, PLoS biology.

[16]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[17]  Luigi Cattaneo,et al.  Numbers within Our Hands: Modulation of Corticospinal Excitability of Hand Muscles during Numerical Judgment , 2007, Journal of Cognitive Neuroscience.

[18]  M. Brass,et al.  The role of the inferior frontal junction area in cognitive control , 2005, Trends in Cognitive Sciences.

[19]  Frank Domahs,et al.  Embodied numerosity: Implicit hand-based representations influence symbolic number processing across cultures , 2010, Cognition.

[20]  Karin Landerl,et al.  Subitizing and counting in typical and atypical development. , 2011, Developmental science.

[21]  Michael W. L. Chee,et al.  Neural correlates of symbolic and non-symbolic arithmetic , 2005, Neuropsychologia.

[22]  Margaret Wilson,et al.  Six views of embodied cognition , 2002, Psychonomic bulletin & review.

[23]  Masami Ishihara,et al.  Touch perception reveals the dominance of spatial over digital representation of numbers , 2008, Proceedings of the National Academy of Sciences.

[24]  Frank Domahs,et al.  Mind the gap between both hands: Evidence for internal finger-based number representations in children's mental calculation , 2008, Cortex.

[25]  M. Thioux,et al.  Neuroanatomical Substrates of Arabic Number Processing, Numerical Comparison, and Simple Addition: A PET Study , 2000, Journal of Cognitive Neuroscience.

[26]  Satrajit S. Ghosh,et al.  Evaluating the validity of volume-based and surface-based brain image registration for developmental cognitive neuroscience studies in children 4 to 11years of age , 2010, NeuroImage.

[27]  S. Dehaene Origins of Mathematical Intuitions , 2009, Annals of the New York Academy of Sciences.

[28]  Karl J. Friston,et al.  Subtractions, conjunctions, and interactions in experimental design of activation studies , 1997, Human brain mapping.

[29]  Tomáš Paus,et al.  Brain Development during Childhood and Adolescence , 2011 .

[30]  Daniel Ansari,et al.  Symbol processing in the left angular gyrus: Evidence from passive perception of digits , 2011, NeuroImage.

[31]  H. Gräfin von Einsiedel,et al.  The role of lateral premotor-cerebellar-parietal circuits in motor sequence control: a parametric fMRI study. , 2002, Brain research. Cognitive brain research.

[32]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.

[33]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[34]  M. Noël,et al.  Finger gnosia: a predictor of numerical abilities in children? , 2005, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[35]  Xavier Seron,et al.  Finger–digit compatibility in Arabic numeral processing , 2006, Quarterly journal of experimental psychology.

[36]  Volkmar Glauche,et al.  Localization of human intraparietal areas AIP, CIP, and LIP using surface orientation and saccadic eye movement tasks , 2008, Human brain mapping.

[37]  Michael Andres,et al.  Contribution of Hand Motor Circuits to Counting , 2007, Journal of Cognitive Neuroscience.

[38]  Avishai Henik,et al.  Meta-Analyses of Developmental fMRI Studies Investigating Typical and Atypical Trajectories of Number Processing and Calculation , 2011, Developmental neuropsychology.

[39]  G. Fink,et al.  REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys , 2005, Journal of anatomy.

[40]  Martin H. Fischer,et al.  Finger counting habits modulate spatial-numerical associations , 2008, Cortex.

[41]  Martin H. Fischer,et al.  When Digits Help Digits: Spatial–Numerical Associations Point to Finger Counting as Prime Example of Embodied Cognition , 2011, Front. Psychology.

[42]  Stephen M. Rao,et al.  Specialized Neural Systems Underlying Representations of Sequential Movements , 2000, Journal of Cognitive Neuroscience.

[43]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[44]  M. K. Wolf,et al.  Lacunar and Other Subcortical Infarctions , 1997, Neurology.

[45]  K. Willmes,et al.  Sensitivity, Reproducibility, and Reliability of Self-Paced Versus Fixed Stimulus Presentation in an fMRI Study on Exact, Non-Symbolic Arithmetic in Typically Developing Children Aged Between 6 and 12 Years , 2011, Developmental neuropsychology.

[46]  Margot J. Taylor,et al.  Is 2+2=4? Meta-analyses of brain areas needed for numbers and calculations , 2011, NeuroImage.

[47]  Michael L. Anderson Embodied Cognition: A field guide , 2003, Artif. Intell..

[48]  M. Fitzgerald Neuroanatomy : basic and applied , 1985 .

[49]  D. V. von Cramon,et al.  Interval and ordinal properties of sequences are associated with distinct premotor areas. , 2001, Cerebral cortex.

[50]  D Yves von Cramon,et al.  Premotor cortex in observing erroneous action: an fMRI study. , 2003, Brain research. Cognitive brain research.

[51]  R. J. Seitz,et al.  A fronto‐parietal circuit for object manipulation in man: evidence from an fMRI‐study , 1999, The European journal of neuroscience.

[52]  J. Piaget The Child's Conception of Number , 1953 .

[53]  Wim Fias,et al.  Number Processing Pathways in Human Parietal Cortex , 2009, Cerebral cortex.

[54]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[55]  J. Tanji,et al.  Numerical representation for action in the parietal cortex of the monkey , 2002, Nature.

[56]  Elizabeth M. Brannon,et al.  The Development of Ordinal Numerical Competence in Young Children , 2001, Cognitive Psychology.

[57]  Mauro Pesenti,et al.  Masked priming effect with canonical finger numeral configurations , 2008, Experimental Brain Research.

[58]  Andreas Nieder,et al.  Basic mathematical rules are encoded by primate prefrontal cortex neurons , 2010, Proceedings of the National Academy of Sciences.

[59]  Marc Sato,et al.  On the relationship between handedness and hand-digit mapping in finger counting , 2008, Cortex.

[60]  Rainer Goebel,et al.  Genetic Contribution to Variation in Cognitive Function: An fMRI Study in Twins , 2009, Science.

[61]  Xavier Seron,et al.  About numerical representations: Insights from neuropsychological, experimental, and developmental studies. , 2005 .