Skip to main content

Advertisement

Log in

Cognitive resource allocation for neural activity underlying mathematical cognition: a multi-method study

  • Original Article
  • Published:
ZDM Aims and scope Submit manuscript

Abstract

Mathematical cognition requires the allocation of computation resources, where math-specific computations are assumed to take place in the parietal cortex and math-supportive computations in the frontal cortex. Because the pupil dilation has a higher temporal resolution than functional MRI (fMRI), the study investigated to which extent the pupil dilation can help to identify cognitive resource allocation for neural activity underlying math-specific and math-supportive cognition. Combining pupillometry and event-related fMRI, we administered a multiplication verification paradigm to 15 healthy participants asking them to solve easy, moderate, and difficult multiplication tasks. The results revealed that (1) behavioral and pupil dilation data increased parametrically with task difficulty; (2) mental multiplication with increasing difficulty recruited a fronto-parietal circuit comprising left pre-supplementary motor area, left precentral gyrus, right dorsolateral prefrontal cortex, and bilateral intraparietal sulcus (IPS); and (3) pupil dilation was sensitive to cognitive resource allocation for neural activity underlying math-specific cognition in the bilateral IPS, implicating a strong reliance on numerical quantity processing during multiplication. In conclusion, the pupil dilation could be used in mathematics education as an easily acquired peripheral physiological indicator (without relying on fMRI) that might lead to a better understanding of dynamical changes in learning arithmetic abilities as a function of training, experience, and development. On a broader level, its application allows to obtain useful insights into learning disabilities such as dyscalculia, and further improve rehabilitation programs with appropriate intervention structures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aleman, A., & Van’t Wout, M. (2008). Repetitive transcranial magnetic stimulation over the right dorsolateral prefrontal cortex disrupts digit span task performance. Neuropsychobiology, 57(1–2), 44–48.

    Article  Google Scholar 

  • Andres, M., Seron, X., & Olivier, E. (2007). Contribution of hand motor circuits to counting. Journal of Cognitive Neuroscience, 19(4), 563–576.

    Article  Google Scholar 

  • Ansari, D. (2008). Effects of development and enculturation on number representation in the brain. Nature Review Neuroscience, 9(4), 278–291.

    Article  Google Scholar 

  • Ashcraft, M. H. (1992). Cognitive arithmetic: A review of data and theory. Cognition, 44(1–2), 75–106.

    Article  Google Scholar 

  • Beatty, J. (1982). Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychological Bulletin, 91, 276–292.

    Article  Google Scholar 

  • Beatty, J., & Lucero-Wagoner, B. (2000). The pupillary system. In T. Cacioppo, L. Tassinary, & G. Berntson (Eds.), Handbook of psychophysiology (pp. 142–162). New York: Cambridge University Press.

    Google Scholar 

  • Behrmann, M., Geng, J. J., & Shomstein, S. (2004). Parietal cortex and attention. Current Opinion in Neurobiology, 14(2), 212–217.

    Article  Google Scholar 

  • Buchel, C., Holmes, A. P., Rees, G., & Friston, K. J. (1998). Characterizing stimulus-response functions using nonlinear regressors in parametric fMRI experiments. Neuroimage, 8(2), 140–148.

    Article  Google Scholar 

  • Butterworth, B. (1999). A head for figures. Science, 284(5416), 928–929.

    Article  Google Scholar 

  • Carpenter, T. P., & Moser, J. M. (1983). The acquisition of addition and subtraction concepts. In R. Lesh & M. Landau (Eds.), Acquisition of mathematics, concepts and processes (pp. 7–44). New York: Academic Press.

    Google Scholar 

  • Cohen, L., & Dehaene, S. (1996). Cerebral networks for number processing: Evidence from a case of posterior callosal lesion. Neurocase, 2, 155–174.

    Article  Google Scholar 

  • Cohen Kadosh, R., Lammertyn, J., & Izard, V. (2008). Are numbers special? An overview of chronometric, neuroimaging, developmental and comparative studies of magnitude representation. Progress in Neurobiology, 84(2), 132–147.

    Article  Google Scholar 

  • Committeri, G., Galati, G., Paradis, A. L., Pizzamiglio, L., Berthoz, A., & LeBihan, D. (2004). Reference frames for spatial cognition: Different brain areas are involved in viewer-, object-, and landmark-centered judgments about object location. Journal of Cognitive Neuroscience, 16(9), 1517–1535.

    Article  Google Scholar 

  • Dehaene, S. (1997). The number sense. Oxford: Oxford University Press.

    Google Scholar 

  • Dehaene, S., & Cohen, L. (1995). Towards an anatomical and functional model of number processing. Mathematical Cognition, 1(1), 83–120.

    Google Scholar 

  • Dehaene, S., Dehaene-Lambertz, G., & Cohen, L. (1998). Abstract representations of numbers in the animal and human brain. Trends in Neurosciences, 21(8), 355–361.

    Article  Google Scholar 

  • Dehaene, S., Molko, N., Cohen, L., & Wilson, A. J. (2004). Arithmetic and the brain. Current Opinion in Neurobiology, 14(2), 218–224.

    Article  Google Scholar 

  • Dehaene, S., Piazza, M., Pinel, P., & Cohen, L. (2003). Three parietal circuits for number processing. Cognitive Neuropsychology, 20(3–6), 487–506.

    Article  Google Scholar 

  • Dehaene, S., Spelke, E., Pinel, P., Stanescu, R., & Tsivkin, S. (1999). Sources of mathematical thinking: Behavioral and brain-imaging evidence. Science, 284, 970–974.

    Article  Google Scholar 

  • Dehaene, S., Tzourio, N., Frak, V., Raynaud, L., Cohen, L., Mehler, J., et al. (1996). Cerebral activations during number multiplication and comparison: A PET study. Neuropsychologia, 34(11), 1097–1106.

    Article  Google Scholar 

  • Delazer, M., Domahs, F., Bartha, L., Brenneis, C., Lochy, A., Trieb, T., et al. (2003). Learning complex arithmetic—An fMRI study. Brain Research Cognitive Brain Research, 18(1), 76–88.

    Article  Google Scholar 

  • Delazer, M., Domahs, F., Lochy, A., Bartha, L., Brenneis, C., & Trieb, T. (2004). The acquisition of arithmetic knowledge—An fMRI study. Cortex, 40(1), 166–167.

    Article  Google Scholar 

  • Delazer, M., Ischebeck, A., Domahs, F., Zamarian, L., Koppelstaetter, F., Siedentopf, C. M., et al. (2005). Learning by strategies and learning by drill—Evidence from an fMRI study. Neuroimage, 25(3), 838–849.

    Article  Google Scholar 

  • Di Luca, S., Grana, A., Semenza, C., Seron, X., & Pesenti, M. (2006). Finger-digit compatibility in Arabic numeral processing. The Quarterly Journal of Experimental Psychology (Colchester), 59(9), 1648–1663.

    Article  Google Scholar 

  • Eger, E., Sterzer, P., Russ, M. O., Giraud, A. L., & Kleinschmidt, A. (2003). A supramodal number representation in human intraparietal cortex. Neuron, 37(4), 719–725.

    Article  Google Scholar 

  • Fayol, M., Barrouillet, P., & Marinthe, C. (1998). Predicting arithmetical achievement from neuro-psychological performance: A longitudinal study. Cognition, 68(2), B63–B70.

    Article  Google Scholar 

  • Feigenson, L., Carey, S., & Hauser, M. (2002). The representations underlying infants’ choice of more: Object files versus analog magnitudes. Psychological Science, 13(2), 150–156.

    Article  Google Scholar 

  • Felgenson, L., Carey, S., & Spelke, E. (2002). Infant’s discriminations of numbers vs. continuous extent. Cognitive Psychology, 44, 33–66.

    Article  Google Scholar 

  • Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., & Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences of the United States of America, 102(27), 9673–9678.

    Article  Google Scholar 

  • Friston, K. J., Holmes, A. P., & Worsley, K. J. (1999). How many subjects constitute a study? Neuroimage, 10, 1–5.

    Article  Google Scholar 

  • Fuson, K. C. (1988). Children’s counting and concepts of number. New York: Springer.

    Google Scholar 

  • Galati, G., Committeri, G., Sanes, J. N., & Pizzamiglio, L. (2001). Spatial coding of visual and somatic sensory information in body-centred coordinates. European Journal of Neuroscience, 14(4), 737–746.

    Article  Google Scholar 

  • Geary, D. C. (2000). From infancy to adulthood: The development of numerical abilities. European Child and Adolescent Psychiatry, 9(Suppl 2), II11–II16.

    Google Scholar 

  • Genovese, C. R., Lazar, N. A., & Nichols, T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage, 15(4), 870–878.

    Article  Google Scholar 

  • Goebel, R., Esposito, F., & Formisano, E. (2006). Analysis of functional image analysis contest (FIAC) data with brain voyager QX: From single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Human Brain Mapping, 27(5), 392–401.

    Article  Google Scholar 

  • Grabner, R. H., Ansari, D., Koschutnig, K., Reishofer, G., Ebner, F., & Neuper, C. (2009). To retrieve or to calculate? Left angular gyrus mediates the retrieval of arithmetic facts during problem solving. Neuropsychologia, 47(2), 604–608.

    Google Scholar 

  • Grabner, R. H., Ansari, D., Reishofer, G., Stern, E., Ebner, F., & Neuper, C. (2007). Individual differences in mathematical competence predict parietal brain activation during mental calculation. Neuroimage, 38(2), 346–356.

    Article  Google Scholar 

  • Granger, C. (1969). Investigating causal relations by econometric models and cross-spectral methods. Econometrica, 37, 424–438.

    Article  Google Scholar 

  • Granholm, E., Asarnow, R. F., Sarkin, A. J., & Dykes, K. L. (1996). Pupillary responses index cognitive resource limitations. Psychophysiology, 33(4), 457–461.

    Article  Google Scholar 

  • Gruber, O., Indefrey, P., Steinmetz, H., & Kleinschmidt, A. (2001). Dissociating neural correlates of cognitive components in mental calculation. Cerebral Cortex, 11(4), 350–359.

    Article  Google Scholar 

  • Hauser, M. D., Carey, S., & Hauser, L. B. (2000). Spontaneous number representation in semi-free-ranging rhesus monkeys. Proceedings of the Royal Society of London Series B: Biological Sciences, 267(1445), 829–833.

    Article  Google Scholar 

  • Hess, E. H., & Polt, J. M. (1964). Pupil size in relation to mental activity during simple problem-solving. Science, 143, 1190–1192.

    Article  Google Scholar 

  • Hesse, W., Moller, E., Arnold, M., & Schack, B. (2003). The use of time-variant EEG Granger causality for inspecting directed interdependencies of neural assemblies. Journal of Neuroscience Methods, 124(1), 27–44.

    Article  Google Scholar 

  • Hillis, A. E., Barker, P. B., Beauchamp, N. J., Gordon, B., & Wityk, R. J. (2000). MR perfusion imaging reveals regions of hypoperfusion associated with aphasia and neglect. Neurology, 55(6), 782–788.

    Google Scholar 

  • Isaacs, E. B., Edmonds, C. J., Lucas, A., & Gadian, D. G. (2001). Calculation difficulties in children of very low birthweight: A neural correlate. Brain, 124(Pt 9), 1701–1707.

    Article  Google Scholar 

  • Ischebeck, A., Zamarian, L., Egger, K., Schocke, M., & Delazer, M. (2007). Imaging early practice effects in arithmetic. Neuroimage, 36(3), 993–1003.

    Article  Google Scholar 

  • Ischebeck, A., Zamarian, L., Siedentopf, C., Koppelstatter, F., Benke, T., Felber, S., et al. (2006). How specifically do we learn? Imaging the learning of multiplication and subtraction. Neuroimage, 30(4), 1365–1375.

    Article  Google Scholar 

  • Just, M. A., & Carpenter, P. (1992). A capacity theory of comprehension: Individual differences in working memory. Psychological Review, 99, 122–149.

    Article  Google Scholar 

  • Just, M. A., Carpenter, P., & Miyake, A. (2003). Neuroindices of cognitive workload: Neuroimaging, pupillo-metric and event-related potential studies of brain work. Theoretical Issues in Ergonomics Science, 4(1), 56–88.

    Article  Google Scholar 

  • Kahneman, D., & Beatty, J. (1966). Pupil diameter and load on memory. Science, 154(756), 1583–1585.

    Article  Google Scholar 

  • Kazui, H., Kitagaki, H., & Mori, E. (2000). Cortical activation during retrieval of arithmetical facts and actual calculation: A functional magnetic resonance imaging study. Psychiatry and Clinical Neurosciences, 54(4), 479–485.

    Article  Google Scholar 

  • Kiefer, M., & Dehaene, S. (1997). The time course of parietal activation in single-digit multiplication: Evidence from event-related potentials. Mathematical Cognition, 3, 1–30.

    Article  Google Scholar 

  • Kong, J., Wang, C., Kwong, K., Vangel, M., Chua, E., & Gollub, R. (2005). The neural substrate of arithmetic operations and procedure complexity. Brain Research Cognitive Brain Research, 22(3), 397–405.

    Article  Google Scholar 

  • Krueger, F. (2000). Coding of temporal relations in semantic memory. Cognitive load and task-evoked pupillary response. Berlin: Waxman.

    Google Scholar 

  • Krueger, F., & Grafman, J. (2008). Disorders of mathematics: Implications for adult functioning. In E. Lorraine, L. E. Schreiber, & J. Wasserstein (Eds.), Adult learning disorders: Contemporary issues (pp. 191–218). New York, NY: Psychology Press.

    Google Scholar 

  • Krueger, F., Landgraf, S., van der Meer, E., Desphande, G., & Hu, X. (2010). Effective connectivity of the multiplication network: A functional MRI and multivariate Granger causality mapping study. Human Brain Mapping (in press).

  • Krueger, F., Nuthmann, A., & van der Meer, E. (2001). Pupillometric indices of temporal representation in semantic memory. Zeitschrift für Psychologie, 209, 402–415.

    Article  Google Scholar 

  • Krueger, F., Spampinato, M. V., Pardini, M., Pajevic, S., Wood, J. N., Weiss, G. H., et al. (2008). Integral calculus problem solving: An fMRI investigation. Neuroreport, 19(11), 1095–1099.

    Article  Google Scholar 

  • Le Clec, H. G., Dehaene, S., Cohen, L., Mehler, J., Dupoux, E., Poline, J. B., et al. (2000). Distinct cortical areas for names of numbers and body parts independent of language and input modality. Neuroimage, 12(4), 381–391.

    Article  Google Scholar 

  • Loewenfeld, I. (1993). The pupil: Anatomy, physiology, and clinical applications. Ames: Iowa State University Press.

    Google Scholar 

  • McCloskey, M., Caramazza, A., & Basili, A. (1985). Cognitive mechanisms in number processing and calculation: Evidence from dyscalculia. Brain and Cognition, 4(2), 171–196.

    Article  Google Scholar 

  • Mellet, E., Petit, L., Mazoyer, B., Denis, M., & Tzourio, N. (1998). Reopening the mental imagery debate: Lessons from functional anatomy. Neuroimage, 8(2), 129–139.

    Article  Google Scholar 

  • Menon, V., Rivera, S. M., White, C. D., Glover, G. H., & Reiss, A. L. (2000). Dissociating prefrontal and parietal cortex activation during arithmetic processing. Neuroimage, 12(4), 357–365.

    Article  Google Scholar 

  • Molko, N., Cachia, A., Riviere, D., Mangin, J. F., Bruandet, M., Le Bihan, D., et al. (2003). Functional and structural alterations of the intraparietal sulcus in a developmental dyscalculia of genetic origin. Neuron, 40, 847–858.

    Article  Google Scholar 

  • Montojo, C. A., & Courtney, S. M. (2008). Differential neural activation for updating rule versus stimulus information in working memory. Neuron, 59(1), 173–182.

    Article  Google Scholar 

  • Naccache, L., & Dehaene, S. (2001). The priming method: Imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. Cerebral Cortex, 11(10), 966–974.

    Article  Google Scholar 

  • Nichols, T., Brett, M., Andersson, J., Wager, T., & Poline, J. B. (2005). Valid conjunction inference with the minimum statistic. Neuroimage, 25(3), 653–660.

    Article  Google Scholar 

  • Nuthmann, A., & van der Meer, E. (2005). Time’s arrow and pupillary response. Psychophysiology, 42, 306–317.

    Article  Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113.

    Article  Google Scholar 

  • Pesenti, M., Thioux, M., Seron, X., & De Volder, A. (2000). Neuroanatomical substrates of Arabic number processing, numerical comparison, and simple addition: A PET study. Journal of Cognitive Neuroscience, 12(3), 461–479.

    Article  Google Scholar 

  • Pesenti, M., Zago, L., Crivello, F., Mellet, E., Samson, D., Duroux, B., et al. (2001). Mental calculation in a prodigy is sustained by right prefrontal and medial temporal areas. Nature Neuroscience, 4(1), 103–107.

    Article  Google Scholar 

  • Piazza, M., Mechelli, A., Butterworth, B., & Price, C. J. (2002). Are subsidizing and counting implemented as separate or functionally overlapping processes? Neuroimage, 15(2), 435–446.

    Article  Google Scholar 

  • Pinel, P., Dehaene, S., Riviere, D., & LeBihan, D. (2001). Modulation of parietal activation by semantic distance in a number comparison task. Neuroimage, 14(5), 1013–1026.

    Article  Google Scholar 

  • Raisig, S., Welke, T., Hagendorf, H., & van der Meer, E. (2007). Investigating dimensional organization in scripts using the pupillary response. Psychophysiology, 44(6), 864–873.

    Article  Google Scholar 

  • Rickard, T. C., Romero, S. G., Basso, G., Wharton, C., Flitman, S., & Grafman, J. (2000). The calculating brain: An fMRI study. Neuropsychologia, 38(3), 325–335.

    Article  Google Scholar 

  • Rivera, S. M., Reiss, A. L., Eckert, M. A., & Menon, V. (2005). Developmental changes in mental arithmetic: Evidence for increased functional specialization in the left inferior parietal cortex. Cerebral Cortex, 15(11), 1779–1790.

    Article  Google Scholar 

  • Rueckert, L., Lange, N., Partiot, A., Appollonio, I., Litvan, I., Le Bihan, D., et al. (1996). Visualizing cortical activation during mental calculation with functional MRI. Neuroimage, 3(2), 97–103.

    Article  Google Scholar 

  • Sato, M., Cattaneo, L., Rizzolatti, G., & Gallese, V. (2007). Numbers within our hands: Modulation of corticospinal excitability of hand muscles during numerical judgment. Journal of Cognitive Neuroscience, 19(4), 684–693.

    Article  Google Scholar 

  • Seymour, S. E., Reuter-Lorenz, P. A., & Gazzaniga, M. S. (1994). The disconnection syndrome. Basic findings reaffirmed. Brain, 117(Pt 1), 105–115.

    Article  Google Scholar 

  • Siegle, G. J., Steinhauer, S. R., Stenger, V. A., Konecky, R., & Carter, C. S. (2003). Use of concurrent pupil dilation assessment to inform interpretation and analysis of fMRI data. Neuroimage, 20(1), 114–124.

    Article  Google Scholar 

  • Simon, O., Mangin, J. F., Cohen, L., Le Bihan, D., & Dehaene, S. (2002). Topographical layout of hand, eye, calculation, and language-related areas in the human parietal lobe. Neuron, 33(3), 475–487.

    Article  Google Scholar 

  • Spelke, E., & Dehaene, S. (1999). Biological foundations of numerical thinking. Response to T.J. Simon (1999). Trends in Cognitive Science, 3(10), 365–366.

    Article  Google Scholar 

  • Stanescu-Cosson, R., Pinel, P., van De Moortele, P. F., Le Bihan, D., Cohen, L., & Dehaene, S. (2000). 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(Pt 11), 2240–2255.

    Article  Google Scholar 

  • Steinhauer, S. R., & Hakerem, G. (1992). The pupillary response in cognitive psychophysiology and schizophrenia. Annals of the New York Academy of Sciences, 658, 182–204.

    Article  Google Scholar 

  • Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme Medical Publishers.

    Google Scholar 

  • Temple, C. M., & Marriott, A. J. (1998). Arithmetic ability and disability in Turner’s syndrome: A cognitive neuropsychological analysis. Developmental Neuropsychology, 14, 47–67.

    Article  Google Scholar 

  • Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory: A meta-analysis. Cognitive, Affective & Behavioral Neuroscience, 3(4), 255–274.

    Article  Google Scholar 

  • Wechsler-Clearfield, M., & Mix, K. S. (1999). Number versus contour length in infant’s discrimination of small visual sets. Psychological Science, 10, 408–411.

    Article  Google Scholar 

  • Wojciulik, E., & Kanwisher, N. (1999). The generality of parietal involvement in visual attention. Neuron, 23(4), 747–764.

    Article  Google Scholar 

  • Xu, F. (2003). Numerosity discrimination in infants: Evidence for two systems of representations. Cognition, 89(1), B15–B25.

    Article  Google Scholar 

  • Xu, K., Anderson, T. R., Neyer, K. M., Lamparella, N., Jenkins, G., Zhou, Z., et al. (2007). Nucleotide sequence variation within the human tyrosine kinase B neurotrophin receptor gene: Association with antisocial alcohol dependence. Pharmacogenomics Journal, 7(6), 368–379.

    Article  Google Scholar 

  • Zago, L., Pesenti, M., Mellet, E., Crivello, F., Mazoyer, B., & Tzourio-Mazoyer, N. (2001). Neural correlates of simple and complex mental calculation. Neuroimage, 13(2), 314–327.

    Article  Google Scholar 

  • Zago, L., Petit, L., Turbelin, M. R., Andersson, F., Vigneau, M., & Tzourio-Mazoyer, N. (2008). How verbal and spatial manipulation networks contribute to calculation: An fMRI study. Neuropsychologia, 46(9), 2403–2414.

    Article  Google Scholar 

  • Zhou, X. Q., He, R., Liu, Z., & Wang, C. Q. (2002). Clinical analysis of 7 patients with Gerstmann syndrome secondary to cerebral vascular disease. Zhongguo Yi Xue Ke Xue Yuan Xue Bao, 24(5), 510–511.

    Google Scholar 

Download references

Acknowledgments

SL was funded by the Konsul-Karl-und-Dr-Gabriele-Sandmann Stiftung, Berlin Germany, and the Université Pierre et Marie Curie, EC3C No. 158, Paris VI, France.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Krueger.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Landgraf, S., van der Meer, E. & Krueger, F. Cognitive resource allocation for neural activity underlying mathematical cognition: a multi-method study. ZDM Mathematics Education 42, 579–590 (2010). https://doi.org/10.1007/s11858-010-0264-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11858-010-0264-7

Keywords

Navigation