Electrophysiological evidence for differential processing of numerical quantity and order in humans.

It is yet unclear whether the processing of number magnitude and order rely on common or different functional processes and neural substrates. On the one hand, recent neuroimaging studies show that quantity and order coding activate the same areas in the parietal and prefrontal cortices. On the other hand, evidence from developmental and neuropsychological studies suggest dissociated mechanisms for processing quantity and order information. To clarify this issue, the present study investigated the spatio-temporal course of quantity and order coding operations using event-related potentials (ERPs). Twenty-four subjects performed a quantity task (classifying numbers as smaller or larger than 15) and an order task on the same material (classifying numbers as coming before or after 15), as well as a control order task on letters (classifying letters as coming before or after M). Behavioral results showed a classical distance effect (decreasing reaction times [RTs] with increasing distance from the standard) for all tasks. In agreement with previous electrophysiological evidence, this effect was significant on a P2 parietal component for numerical material. However, the difference between processing numbers close or far from the target appeared earlier and was larger on the left hemisphere for quantity processing, while it was delayed and bilateral for order processing. There was also a significant distance effect in all tasks on parietal sites for the following P3 component elicited by numbers, but this effect was larger on prefrontal areas for the order judgment. In conclusion, both quantity and order show similar behavioral effects, but they are associated with different spatio-temporal courses in parietal and prefrontal cortices.

[1]  E. Mayer,et al.  A pure case of Gerstmann syndrome with a subangular lesion. , 1999, Brain : a journal of neurology.

[2]  B. Rossion,et al.  Task modulation of brain activity related to familiar and unfamiliar face processing: an ERP study , 1999, Clinical Neurophysiology.

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

[4]  Dana Ganor-Stern,et al.  Automaticity in Processing Ordinal Information , 2004 .

[5]  S. Dehaene,et al.  THREE PARIETAL CIRCUITS FOR NUMBER PROCESSING , 2003, Cognitive neuropsychology.

[6]  Laure Zago,et al.  Distinguishing visuospatial working memory and complex mental calculation areas within the parietal lobes , 2002, Neuroscience Letters.

[7]  K. Holyoak The form of analog size information in memory , 1977, Cognitive Psychology.

[8]  A. Starr,et al.  Brain potentials during mental distance judgments. , 1988, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[9]  B. Kotchoubey,et al.  Brain responses to number sequences with and without active task requirement , 2002, Clinical Neurophysiology.

[10]  M. Delazer,et al.  Arithmetic Facts without Meaning , 1997, Cortex.

[11]  Brian Butterworth,et al.  The Mathematical Brain , 1999 .

[12]  M. Farah,et al.  Neural Specialization for Letter Recognition , 2002, Journal of Cognitive Neuroscience.

[13]  S. Dehaene,et al.  Topographical Layout of Hand, Eye, Calculation, and Language-Related Areas in the Human Parietal Lobe , 2002, Neuron.

[14]  Laure Zago,et al.  Mental calculation in a prodigy is sustained by right prefrontal and medial temporal areas , 2001, Nature Neuroscience.

[15]  Elizabeth K. Warrington,et al.  Arithmetic Skills in Patients with Unilateral Cerebral Lesions , 1986, Cortex.

[16]  T. Allison,et al.  Human extrastriate visual cortex and the perception of faces, words, numbers, and colors. , 1994, Cerebral cortex.

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

[18]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.

[19]  Domenico Passafiume,et al.  Calculation Disturbances in Adults with Focal Hemispheric Damage , 1982, Cortex.

[20]  Stanislas Dehaene,et al.  Two mental calculation systems: A case study of severe acalculia with preserved approximation , 1991, Neuropsychologia.

[21]  R. Schubotz,et al.  Instruction differentiates the processing of temporal and spatial sequential patterns: evidence from slow wave activity in humans , 1999, Neuroscience Letters.

[22]  A. Ardila,et al.  Angular gyrus syndrome revisited: Acalculia, finger agnosia, right-left disorientation and semantic aphasia , 2000 .

[23]  Jerwen Jou,et al.  Multiple number and letter comparison: directionality and accessibility in numeric and alphabetic memories. , 2003, The American journal of psychology.

[24]  D. A. Taylor,et al.  Representation of linear orders. , 1984, Journal of experimental psychology. Learning, memory, and cognition.

[25]  Elizabeth K. Warrington,et al.  The WAIS as a lateralizing and localizing diagnostic instrument: A study of 656 patients with unilateral cerebral lesions , 1986, Neuropsychologia.

[26]  K. Wynn Children's acquisition of the number words and the counting system , 1992, Cognitive Psychology.

[27]  S. Dehaene,et al.  Is numerical comparison digital? Analogical and symbolic effects in two-digit number comparison. , 1990, Journal of experimental psychology. Human perception and performance.

[28]  ● Pytorch,et al.  Attention! , 1998, Trends in Cognitive Sciences.

[29]  Stanislas Dehaene,et al.  Cerebral Pathways for Calculation: Double Dissociation between Rote Verbal and Quantitative Knowledge of Arithmetic , 1997, Cortex.

[30]  Wim Fias,et al.  The mental representation of ordinal sequences is spatially organized , 2003, Cognition.

[31]  G. Denes,et al.  A specific deficit for numbers in a case of dense acalculia. , 1991, Brain : a journal of neurology.

[32]  T A Polk,et al.  The neural development and organization of letter recognition: evidence from functional neuroimaging, computational modeling, and behavioral studies. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  G Pfurtscheller,et al.  The role of the right parietal region in a movement time estimation task. , 1991, Neuroreport.

[34]  D. LeBihan,et al.  Modulation of Parietal Activation by Semantic Distance in a Number Comparison Task , 2001, NeuroImage.

[35]  Lars Nyberg,et al.  Brain Regions Differentially Involved in Remembering What and When: a PET Study , 1997, Neuron.

[36]  Peter Ullsperger,et al.  Processing of multi-dimensional stimuli: P300 component of the event-related brain potential during mental comparison of compound digits , 1995, Biological Psychology.

[37]  L. Cohen Number processing in pure alexia: The effect of hemispheric asymmetries and task demands , 1995 .

[38]  Marie-Pascale Noël,et al.  The isolation of numerals at the semantic level , 1998 .

[39]  Stanislas Dehaene,et al.  The Organization of Brain Activations in Number Comparison: Event-Related Potentials and the Additive-Factors Method , 1996, Journal of Cognitive Neuroscience.

[40]  S. Dehaene,et al.  Abstract representations of numbers in the animal and human brain , 1998, Trends in Neurosciences.

[41]  A. Paivio Perceptual comparisons through the mind’s eye , 1975, Memory & cognition.

[42]  Richard J. Brown Neuropsychology Mental Structure , 1989 .

[43]  Stanislas Dehaene,et al.  Cerebral networks for number processing: Evidence from a case of posterior callosal lesion , 1996 .

[44]  L. Fasotti,et al.  The internal representation of arithmetical word problem sentences: Frontal and posterior-injured patients compared , 1992, Brain and Cognition.

[45]  Stanislas Dehaene,et al.  Levels of Representation in Number Processing , 1998 .

[46]  M. Sugishita,et al.  Isolated acalculia due to left parietal lesion. , 1994, Archives of neurology.

[47]  M. Posner,et al.  Brain mechanisms of quantity are similar in 5-year-old children and adults. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Monica Rosselli,et al.  Calculation deficits in patients with right and left hemisphere damage , 1989, Neuropsychologia.

[49]  D G Gadian,et al.  Calculation difficulties in children of very low birthweight: a neural correlate. , 2001, Brain : a journal of neurology.

[50]  Patrick Dupont,et al.  The Quantitative Nature of a Visual Task Differentiates between Ventral and Dorsal Stream , 2002, Journal of Cognitive Neuroscience.

[51]  S Dehaene,et al.  Attention, automaticity, and levels of representation in number processing. , 1995, Journal of experimental psychology. Learning, memory, and cognition.

[52]  R. Moyer Comparing objects in memory: Evidence suggesting an internal psychophysics , 1973 .

[53]  A. Damasio,et al.  Troubled letters but not numbers. Domain specific cognitive impairments following focal damage in frontal cortex. , 1990, Brain : a journal of neurology.

[54]  Michael McCloskey,et al.  Localizing Arithmetic Processes in the Brain: Evidence from a Transient Deficit During Cortical Stimulation , 1997, Journal of Cognitive Neuroscience.

[55]  A. Kleinschmidt,et al.  Dissociating neural correlates of cognitive components in mental calculation. , 2001, Cerebral cortex.

[56]  Stephen M. Rao,et al.  The evolution of brain activation during temporal processing , 2001, Nature Neuroscience.

[57]  Margot J. Taylor Non-spatial attentional effects on P1 , 2002, Clinical Neurophysiology.

[58]  Arthur P. Shimamura,et al.  Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients , 1990, Neuropsychologia.

[59]  E. Miller,et al.  Coding of Cognitive Magnitude Compressed Scaling of Numerical Information in the Primate Prefrontal Cortex , 2003, Neuron.

[60]  Andrew W. Ellis,et al.  Modes of word recognition in the left and right cerebral hemispheres , 1988, Brain and Language.

[61]  H. Heinze,et al.  On the interaction of numerical and size information in digit comparison: a behavioral and event-related potential study , 1998, Neuropsychologia.

[62]  John Jonides,et al.  Order Information in Working Memory: fMRI Evidence for Parietal and Prefrontal Mechanisms , 2000, Journal of Cognitive Neuroscience.

[63]  A. Kleinschmidt,et al.  A Supramodal Number Representation in Human Intraparietal Cortex , 2003, Neuron.

[64]  E. Spelke,et al.  Sources of mathematical thinking: behavioral and brain-imaging evidence. , 1999, Science.

[65]  ROBERT S. MOYER,et al.  Time required for Judgements of Numerical Inequality , 1967, Nature.

[66]  J. Donoghue,et al.  Frontal and parietal lobe activation during transitive inference in humans. , 2002, Cerebral cortex.

[67]  J. Grafman,et al.  The calculating brain: an fMRI study , 2000, Neuropsychologia.

[68]  J W Aldridge,et al.  Memory representation of alphabetic position and interval information. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[69]  Daniel N. Bub,et al.  Different modes of word recognition in the left and right visual fields , 1988, Brain and Language.

[70]  Martha J. Farah,et al.  Cognitive Neuropsychology: Patterns of Co-occurrence Among the Associative Agnosias: Implications for Visual Object Representation , 1991 .

[71]  S. Dehaene,et al.  The mental representation of parity and number magnitude. , 1993 .

[72]  K. Fuson Children's Counting and Concepts of Number , 1987 .

[73]  J. Parkman,et al.  Temporal aspects of digit and letter inequality judgments. , 1971, Journal of experimental psychology.

[74]  M. Metz-Lutz,et al.  Calculation and number processing: assessment battery; role of demographic factors. , 1994, Journal of clinical and experimental neuropsychology.

[75]  M S Gazzaniga,et al.  The disconnection syndrome. Basic findings reaffirmed. , 1994, Brain : a journal of neurology.

[76]  A. Mecklinger,et al.  Mental comparison of visually presented two-digit numbers: a P300 study. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[77]  Bruno Rossion,et al.  Early lateralization and orientation tuning for face, word, and object processing in the visual cortex , 2003, NeuroImage.

[78]  G. R. Potts,et al.  Mental comparison of size and magnitude: size congruity effects. , 1984, Journal of experimental psychology. Learning, memory, and cognition.

[79]  Doreen Kimura,et al.  The relation between oral movement control and speech , 1989, Brain and Language.

[80]  S. Dehaene,et al.  Event-related fMRI analysis of the cerebral circuit for number comparison. , 1999, Neuroreport.

[81]  D. Besner,et al.  The mind's eye and the comparative judgement of number , 1979, Neuropsychologia.

[82]  Jamie I. D. Campbell Handbook of mathematical cognition , 2004 .

[83]  C. B. Cave,et al.  Evidence for two types of spatial representations: hemispheric specialization for categorical and coordinate relations. , 1989, Journal of experimental psychology. Human perception and performance.

[84]  Brian Butterworth,et al.  A Dissociation of Number Meanings , 1997 .

[85]  G. Orban,et al.  Parietal Representation of Symbolic and Nonsymbolic Magnitude , 2003, Journal of Cognitive Neuroscience.

[86]  G. Egan,et al.  The Functional Neuroanatomy of Simple Calculation and Number Repetition: A Parametric PET Activation Study , 2000, NeuroImage.

[87]  H. Wiese Numbers, language, and the human mind , 2003 .

[88]  M. Kutas,et al.  Neurophysiological evidence for visual perceptual categorization of words and faces within 150 ms. , 1998, Psychophysiology.

[89]  J. Grafman,et al.  Metabolic abnormalities detected by 1H-MRS in dyscalculia and dysgraphia , 1999, Neurology.

[90]  G. Glover,et al.  Dissociating Prefrontal and Parietal Cortex Activation during Arithmetic Processing , 2000, NeuroImage.

[91]  S. Dehaene,et al.  Differential Contributions of the Left and Right Inferior Parietal Lobules to Number Processing , 1999, Journal of Cognitive Neuroscience.

[92]  J. Hamilton,et al.  The Symbolic Distance Effect for Alphabetic Order Judgements: A Subjective Report and Reaction Time Analysis , 1978 .

[93]  W Fias,et al.  Irrelevant digits affect feature-based attention depending on the overlap of neural circuits. , 2001, Brain research. Cognitive brain research.

[94]  E. Warrington,et al.  The abstraction of numerical relations: A role for the right hemisphere in arithmetic? , 1997, Journal of the International Neuropsychological Society.

[95]  Xavier Seron,et al.  Dissociation Between Order and Quantity Meanings in a Patient with Gerstmann Syndrome , 2002, Cortex.

[96]  M. Corballis Can commissurotomized subjects compare digits between the visual fields? , 1994, Neuropsychologia.

[97]  J. Jou,et al.  Why is the alphabetically middle letter in a multiletter array so hard to determine? Memory processes in linear-order information processing. , 1997, Journal of experimental psychology. Human perception and performance.

[98]  Paul B. Buckley,et al.  Comparisons of digits and dot patterns. , 1974, Journal of experimental psychology.