Skip to main content

Advertisement

Log in

rTMS over the intraparietal sulcus disrupts numerosity processing

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

It has been widely argued that the intraparietal sulcus (IPS) is involved in tasks that evoke representations of numerical magnitude, among other cognitive functions. However, the causal role of this parietal region in processing symbolic and non-symbolic numerosity has not been established. The current study used repetitive Transcranial Magnetic Stimulation (rTMS) to the left and right IPS to investigate the effects of temporary deactivations of these regions on the capacity to represent symbolic (Arabic numbers) and non-symbolic (arrays of dots) numerosities. We found that comparisons of both symbolic and non-symbolic numerosities were impaired after rTMS to the left IPS but enhanced by rTMS to the right IPS. A signature effect of numerical distance was also found: greater impairment (or lesser facilitation) when comparing numerosities of similar magnitude. The reverse pattern of impairment and enhancement was found in a control task that required judging an analogue stimulus property (ellipse orientation) but no numerosity judgements. No rTMS effects for the numerosity tasks were found when stimulating an area adjacent but distinct from the IPS, the left and right angular gyrus. These data suggest that left IPS is critical for processing symbolic and non-symbolic numerosity; this processing may thus depend on common neural mechanisms, which are distinct from mechanisms supporting the processing of analogue stimulus properties.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  • Alexander I, Cowey A, Walsh V (2005) The right parietal cortex and time perception: back to Critchley and the Zeitraffer phenomenon. Cogn Neuropsychol 22:306–315

    Article  Google Scholar 

  • Andres M, Seron X, Olivier E (2005) Hemispheric lateralization of number comparison. Cogn Brain Res 25:283–290

    Article  Google Scholar 

  • Ashbridge E, Walsh V, Cowey A (1997) Temporal aspects of visual search studies by transcranial magnetic stimulation. Neuropsychologia 35:1121–1131

    Article  PubMed  CAS  Google Scholar 

  • Barth H, La Mont K, Lipton J, Spelke E (2005) Abstract number and arithmetic in preschool children. Proc Natl Acad Sci USA 102:14116–14121

    Article  PubMed  CAS  Google Scholar 

  • Barth H, La Mont K, Lipton J, Dehaene S, Kanwisher N, Spelke E (2006) Non-symbolic arithmetic in adults and young children. Cognition 98:199–222

    Article  PubMed  Google Scholar 

  • Boles DB (1986) Hemispheric differences in the judgment of number. Neuropsychologia 24:511–519

    Article  PubMed  CAS  Google Scholar 

  • Butterworth B (1999) The mathematical brain. McMillian, New York

    Google Scholar 

  • Cappelletti M, Butterworth B, Kopelman MD (2001) Spared numerical abilities in a case of semantic dementia. Neuropsychologia 39:1224–1239

    Article  PubMed  CAS  Google Scholar 

  • Castelli F, Glaser DE, Butterworth B (2006) Discrete and analogue quantity processing in the parietal lobe: a functional MRI study. PNAS 103:4693–4698

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403

    PubMed  CAS  Google Scholar 

  • Cipolotti L, Butterworth B, Denes G (1991) Specific deficit for numbers in a case of dense acalculia. Brain 114:2619–2637

    Article  PubMed  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 L, Dehaene S, Chochon F, Lehéricy S, Naccache L (2000) Language and calculation within the parietal lobe: a combined cognitive, anatomical and fMRI study. Neurospychologia 138:1426–1440

    Article  Google Scholar 

  • Crutch SJ, Warrington EK (2002) Preserved calculation skills in a case of semantic dementia. Cortex 38:389–399

    Article  PubMed  Google Scholar 

  • Culham J, Kenwisher N (2001) Neuroimaging of cognitive functions in human parietal cortex. Curr opin Neurobiol 11:157–163

    Article  PubMed  CAS  Google Scholar 

  • Dehaene S (1992) Varieties of numerical abilities. Cognition 44:42

    Article  Google Scholar 

  • Dehaene S (1996) The organization of brain activations in number comparison: event-related potentials and the additive-factors methods. J Cogn Neurosci 8:47–68

    Article  Google Scholar 

  • Dehaene S (1997) The number sense. Oxford University Press, Penguin press, New York, Cambridge, UK

    Google Scholar 

  • Dehaene S, Cohen L (1991) Two mental calculation systems: a case study of severe acalculia with preserved approximation. Neuropsychologia 29:1045–1074

    Article  PubMed  CAS  Google Scholar 

  • Dehaene S, Cohen L (1997) Cerebral pathways for calculation: double dissociation between rote verbal and quantitative knowledge of arithmetic. Cortex 33:219–250

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Dehaene S, Piazza M, Pinel P, Cohen L (2003) Three parietal circuits for number processing. Cogn Neuropsychol 20:487–506

    Article  Google Scholar 

  • Eger E, Sterzer P, Russ M, Giraud A, Kleinschmidt A (2001) A supramodal number representation in human intraparietal cortex. Neuron 37(4):719–725

    Article  Google Scholar 

  • Faillenot I, Decety J, Jeannerod M (1998) Human brain activity related to the perception of spatial features of objects. Neuroimage 10:114–124

    Article  Google Scholar 

  • Feigenson L, Carey S, Hauser M (2002) The representations underlying infants’ choice of more: object files versus analogue magnitude. Psychol Sci 13:150–156

    Article  PubMed  Google Scholar 

  • Fias W, Lammertyn J, Reynvoet B, Dupont P, Orban G (2003) Parietal representation of symbolic and non-symbolic magnitude. J Cogn Neurosci 15:1–11

    Article  Google Scholar 

  • Forster KI, Forster JC (2003) DMDX: a windows display program with millisecond accuracy. Behav Res Methods Instrum Comput 35:116–124

    PubMed  Google Scholar 

  • Fregni F, Boggio PS, Valle AC, Rocha RR, Duarte J, Ferreira et al (2006) A sham-controlled trial of 5-day course of rTMS of the unaffected hemisphere in stroke patients. Stroke 37(8):2115–2122

    Article  PubMed  Google Scholar 

  • Fullbright R, Manson C, Skudlarski P, Lacadie C, Gore J (2003) Quantity determination and the distance effect with letters numbers and shapes: a functional MR imaging study of number processing. AJNR Am J Neuroradiol 23:197–200

    Google Scholar 

  • Gelman R, Gallistel CR (2004) Language and the origin of numerical cognition. Science 306:441–443

    Article  PubMed  CAS  Google Scholar 

  • Göbel SM, Walsh V, Rushworth MFS (2001) The mental number line and the human angular gyrus. NeuroImage 14:1278–1289

    Article  PubMed  Google Scholar 

  • Göbel SM, Johansen-Berg H, Behrens TE, Rushworth MFS (2004) Response-selection related parietal activation during number comparison. J Cogn Neurosci 16:1536–1551

    Article  PubMed  Google Scholar 

  • Göbel SM, Calabria M, Farné A, Rossetti Y (2005) Parietal rTMS distorts the mental number line: simulating ‘spatial’ neglect in healthy subjects. Neuropsychologia 44:860–868

    Article  PubMed  Google Scholar 

  • Göbel SM, Calabria M, Farné A, Giraud A, Rossetti Y (2006) Parietal rTMS distorts the mental number line: simulating “spatial” neglect in healthy subjects. Neuropsychologia 44:860–868

    Article  PubMed  Google Scholar 

  • Hilgetag CC, Theoret H, Pascual-Leone A (2001) Enhanced visual spatial attention ipsilateral to rTMS-induced ‘virtual lesions’ of human parietal cortex. Nat Neurosci 4:953–957

    Article  PubMed  CAS  Google Scholar 

  • Johnson DM (1939) Confidence and speed in the two-category judgment. Arch Psychol 241:1–52

    Google Scholar 

  • Kadosh R, Henik A, Rubinsten O, Mohr H, Dori H, Van de Ven V, Zorzi M, Goebel R, Linden D (2005) Are numbers special? the comparison systems of the human brain investigated by fMRI. Neuropsychologia 43:1238–1248

    Article  Google Scholar 

  • Kobayashi M, Hutchinson S, Theoret H, Schlaug G, Pascual-Leone A (2004) A Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements. Neurology 62:91–98

    PubMed  CAS  Google Scholar 

  • Kolb B, Whishaw IQ (1998) Brain plasticity and behavior. Annu Rev Psychol 49:43–64

    Article  PubMed  CAS  Google Scholar 

  • Kosslyn SM, Pascual-Leone A, Felician O, Camposano S, Keenan JP, Thompson WL, Ganis G, Sukel KE, Alpert NM (1999) The role of area 17 in visual imagery: convergent evidence from PET and rTMS. Science 284:167–170

    Article  PubMed  CAS  Google Scholar 

  • Lemer C, Dehaene S, Spelke E, Cohen L (2003) Approximate quantities and exact number words: dissociable systems. Neuropsychologia 41:1942–1958

    Article  PubMed  Google Scholar 

  • Mansur CG, Fregni F, Boggio PS, Riberto M, Gallucci-Neto J, Santos CM, Wagner T, Rigonatti SP, Marcolin MA, Pascual-Leone A (2005) A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology 64:802–804

    Article  Google Scholar 

  • Martin P, Naeser MA, Theoret H, Tormos JM, Nicholas M, Kurland J, Fregni F, Seekins H, Doron K, Pascual-Leone A (2004) Transcranial magnetic stimulation as a complementary treatment for Aphasia. Semin Speech Lang 25:181–191

    Article  PubMed  Google Scholar 

  • Mennemeier M, Pierce CA, Chatterjee A, Anderson B, Jewell G, Dowler R, Woods AJ, Glenn T, Mark VM (2005) Biases in attentional orientation and magnitude estimation explain crossover: neglect is a disorder of both. J Cogn Neurosci 17:1194–1211

    Article  PubMed  Google Scholar 

  • Moyer RS, Landauer TK (1967) Time required for judgements of numerical inequality. Nature 215:1519–1520

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Naeser MA, Martin PI, Nicholas M, Baker EH, Seekins H, Helm-Estabrooks N, Cayer-Meade C, Kobayashi M, Theoret H, Fregni F, Tormos JM, Kurland J, Doron KW, Pascual-Leone A (2005) Improved picture naming in chronic aphasia after TMS to part of right Broca’s area: an open-protocol study. Brain Lang 93:95–105

    Article  PubMed  Google Scholar 

  • Nieder A, Miller EK (2004) A parieto-frontal network for visual numerical information in the monkey. Proc Natl Acad Sci USA 101:7457–7462

    Article  PubMed  CAS  Google Scholar 

  • Nieder A, Freedman DJ, Miller EK (2002) Representation of the quantity of visual items in the primate prefrontal cortex. Science 297:1708–1711

    Article  PubMed  CAS  Google Scholar 

  • Oliveri M, Rausei V, Koch G, Torriero S, Turriziani P, Caltagirone C (2004) Overestimation of numerical distances in the left side of space. Neurology 11:2139–2141

    Google Scholar 

  • Ono M, Kubik S, Abernathey CD (1990) Atlas of the Cerebral Sulci. Thieme

  • Pascual-Leone A, Walsh V, Rothwell J (2000) Transcranial magnetic stimulation in cognitive neuroscience–Virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol 10:232–237

    Article  PubMed  CAS  Google Scholar 

  • Pascual-Leone AP, Davey NJ, Rothwell J, Wassermann EM, Puri BK (2002) Handbook of transcranial magnetic stimulation. Arnold Publisher, Paris

    Google Scholar 

  • Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans A (1997) Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the cerebral cortex. J Neurosci 179:3178–3184

    Google Scholar 

  • Paus T (1999) Imaging the brain before, during, and after transcranial magnetic stimulation. Neuropsychologia 37:219–224

    Article  PubMed  CAS  Google Scholar 

  • Piazza M, Izard V, Pinel P, Le Bihan D, Dehaene S (2004) Tuning curves for approximate numerosity in the human intraparietal sulcus. Neuron 44:547–555

    Article  PubMed  CAS  Google Scholar 

  • Pinel P, Piazza M, Le Bihan D, Dehaene S (2004) Distributed and overlapping cerebral representations of number, size, and luminance during comparative judgments. Neuron 41:983–993

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Polk T, Reed C, Keenan J, Hogard P, Anderson CA (2001) A dissociation between symbolic number knowledge and analogue magnitude information. Brain Cogn 47:545–563

    Article  PubMed  CAS  Google Scholar 

  • Ratinckx E, Brysbaert M, Reynvoet B (2001) Bilateral field interactions and hemispheric asymmetry in number comparison. Neuropsychologia 39(4):335–345

    Article  PubMed  CAS  Google Scholar 

  • Robertson EM, Theoret H, Pascual-Leone A (2003) The problems solved and created by transcranial magnetic stimulation. J Cogn Neurosci 15:948–960

    Article  PubMed  CAS  Google Scholar 

  • Romero R, Anschel D, Sparing R, Gangitano M, Pascual-Leone A (2002) Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex. Clin Neurophysiol 113:101–107

    Article  PubMed  Google Scholar 

  • Rusconi E, Walsh V, Butterworth B (2005) Dexterity with numbers: rTMS over left angular gyrus disrupts finger gnosis and number processing. Neuropsychologia 43:1609–1624

    Article  PubMed  Google Scholar 

  • Sandrini M, Rossini PM, Miniussi C (2004) The differential involvement of inferior parietal lobule in number comparison: a rTMS study. Neuropsychologia 42:1902–1909

    Article  PubMed  Google Scholar 

  • Sathian K, Simon TJ, Peterson S, Patel GA, Hoffman JM, Grafton ST (1999) Neural evidence linking visual object enumeration and attention. J Cogn Neurosci 11:36–51

    Article  PubMed  CAS  Google Scholar 

  • Sawamura H, Shima K, Tanji J (2002) Numerical representation for action in the parietal cortex of the monkey. Nature 415:918–922

    Article  PubMed  CAS  Google Scholar 

  • Seymour SA, Reuter-Lorenz PA, Gazzaniga MS (1994) The disconnection syndrome: basic findings reaffirmed. Brain 117:105–115

    Article  PubMed  Google Scholar 

  • Shuman M, Kanwisher N (2004) Numerical magnitude in the nhuman parietal lobe; tests of representational generality and domain specificity. Neuron 44:557–569

    Article  PubMed  CAS  Google Scholar 

  • Stanescu-Cosson R, Pinel P, van de Moortele PF, LeBihan D, Cohen L, Dehaene S (2000) Cerebral bases of calculation processes: impact of number size on the cerebral circuits for exact and approximative calculation. Brain 123:2240–2255

    Article  PubMed  Google Scholar 

  • Stokes M, Chambers CD, Gould IC, Henderson TR, Janko NE, Allen NB, Mattingley JB (2005) Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. J Neurophysiol 94:4520–4527

    Article  PubMed  Google Scholar 

  • Takeuchi N, Chuma T, Matsuo Y, Watanabe I, Ikoma K (2005) Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 36:2681–2686

    Article  PubMed  Google Scholar 

  • Theoret H, Haque J, Pascual-Leone A (2001) Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans. Neurosci Lett 306:29–32

    Article  PubMed  CAS  Google Scholar 

  • Theoret H, Kobayashi M, Valero-Cabre A, Pascual Leone A (2003) Exploring paradoxical functional facilitation with TMS. Suppl Clin Neurophysiol 56:211–219

    Article  PubMed  Google Scholar 

  • Thioux M, Pillon A, Samson D, De Partz MP, Noël MP, Seron X (1998) The isolation of numerals at the semantic level. Neurocase 4:371–389

    Google Scholar 

  • Turconi E, Jemel B, Rossion B, Seron X (2004) Electrophysiological evidence for differential processing of numerical quantity and order in humans. Cogn Brain Res 21(1):22–38

    Article  Google Scholar 

  • Verguts T, Fias W (2004) Representation of number in animals and humans: a neural model. J Cogn Neurosci 16:1493–1504

    Article  PubMed  Google Scholar 

  • Walsh V, Rushworth MFS (1999) The use of transcranial magnetic stimulation in neuropsychological testing. Neuropsychologia 37:125–135

    PubMed  CAS  Google Scholar 

  • Walsh V, Pascual-Leone A (2003) Transcranial magnetic stimulation. A neurochronometrics of mind. The MIT Press, Cambridge, Massachusetts, London, England

    Google Scholar 

  • Warrington EK (1982) The fractionation of arithmetic skills: a single case study. Q J Exp Psychol 34A:31–51

    Google Scholar 

  • Wasserman EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International workshop on the safety of repetitive transcranial magnetic stimulation, June 5–7, 1996. Electroencelophagr Clin Neurophysiol 108:1–16

    Article  Google Scholar 

  • Woods AJ, Mennemeier M, Garcia-Rill E, Meythaler J, Mark VW, Jewel GR, Murphy H (2006) Bias in magnitude estimation following left hemisphere injury. Neuropsychologia. 44:1406–1412

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zorzi M, Stoianov I, Umiltà C (2005) Computational modeling of numerical cognition. In: Campbell J (ed) Handbook of mathematical cognition, vol 5. Psychology Press, London, pp 67–83

    Google Scholar 

  • Xu F (2000) Numerical competence in infancy: two systems of representation. Paper presented at the 12th Biennial International Conference on Infant Studies, Brighton, UK

    Google Scholar 

  • Xu F, Spelke ES (2000) Large number discrimination in 6-month old infants. Cognition 74:B1–B11

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by British Academy and Wellcome Trust Grants to MC, by a National Academy of Education/Spencer Foundation Postdoctoral Fellowship to HB, by grants from the National Institutes of Health (K24 RR018875, RO1-EY12091, RO1-DC05672, RO1-NS 47,754, RO1-NS 20,068, and R01-EB 00,5047) to APL and by the Harvard Medical School Scholars in Clinical Science Program (NIH K30 HL04095-03) to FF. We would like to thank M. Finkbeiner for technical support, A. Caramazza, E. Freeman, and V. Walsh for useful comments, and the Harvard-Thorndike General Clinical Research Center for help in implementing the study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marinella Cappelletti.

Additional information

H. Barth and F. Fregni contributed equally to this study.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cappelletti, M., Barth, H., Fregni, F. et al. rTMS over the intraparietal sulcus disrupts numerosity processing. Exp Brain Res 179, 631–642 (2007). https://doi.org/10.1007/s00221-006-0820-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-006-0820-0

Keywords

Navigation