Functional imaging of numerical processing in adults and 4-y-old children

Jessica F Cantlon, Elizabeth M Brannon, Elizabeth J Carter, Kevin A Pelphrey, Jessica F Cantlon, Elizabeth M Brannon, Elizabeth J Carter, Kevin A Pelphrey

Abstract

Adult humans, infants, pre-school children, and non-human animals appear to share a system of approximate numerical processing for non-symbolic stimuli such as arrays of dots or sequences of tones. Behavioral studies of adult humans implicate a link between these non-symbolic numerical abilities and symbolic numerical processing (e.g., similar distance effects in accuracy and reaction-time for arrays of dots and Arabic numerals). However, neuroimaging studies have remained inconclusive on the neural basis of this link. The intraparietal sulcus (IPS) is known to respond selectively to symbolic numerical stimuli such as Arabic numerals. Recent studies, however, have arrived at conflicting conclusions regarding the role of the IPS in processing non-symbolic, numerosity arrays in adulthood, and very little is known about the brain basis of numerical processing early in development. Addressing the question of whether there is an early-developing neural basis for abstract numerical processing is essential for understanding the cognitive origins of our uniquely human capacity for math and science. Using functional magnetic resonance imaging (fMRI) at 4-Tesla and an event-related fMRI adaptation paradigm, we found that adults showed a greater IPS response to visual arrays that deviated from standard stimuli in their number of elements, than to stimuli that deviated in local element shape. These results support previous claims that there is a neurophysiological link between non-symbolic and symbolic numerical processing in adulthood. In parallel, we tested 4-y-old children with the same fMRI adaptation paradigm as adults to determine whether the neural locus of non-symbolic numerical activity in adults shows continuity in function over development. We found that the IPS responded to numerical deviants similarly in 4-y-old children and adults. To our knowledge, this is the first evidence that the neural locus of adult numerical cognition takes form early in development, prior to sophisticated symbolic numerical experience. More broadly, this is also, to our knowledge, the first cognitive fMRI study to test healthy children as young as 4 y, providing new insights into the neurophysiology of human cognitive development.

Figures

Figure 1. Task Design
Figure 1. Task Design
Participants were given the experiment-irrelevant task of fixating on a central crosshair and pressing a joystick button when the crosshair turned red. They passively viewed a stream of visual arrays, the majority of which contained the same number of elements and element shape. Occasionally, a stimulus was presented that deviated from the standard stimuli ineither number of elements (number deviants)or local element shape (shape deviants). Cumulative surface area, density, element size, and spatial arrangement varied among standard stimuli so that participants were not habituated to these dimensions. Deviant and standard stimuli overlapped in cumulative surface area, density, element size, or spatial arrangement so that these dimensions were never novel for deviant stimuli. Number deviants differed by a 2:1 ratio from the standard number of elements such that half of the numerical deviants had a greater number of elements than the standard, and the other half had fewer elements. Elements in standard arrays were circles while shape deviants contained squares or triangles.
Figure 2. Adult Participant's fMRI Results
Figure 2. Adult Participant's fMRI Results
(A) Regions that were more active during the presentation of number compared to shape deviants (p < .05, cluster size > six functional voxels). (B) Regions that were more active during the presentation of shape compared to number deviants (p < .05, cluster size > six functional voxels). (C) Time course of activity (percent signal change) for number-selective (number > shape) regions in the IPS, averaged from individually-drawn functional regions of interest from the IPS, from 3 s pre-stimulus to 12 s post-stimulus.
Figure 3. Child Participant's fMRI Results
Figure 3. Child Participant's fMRI Results
(A) Regions that were more active during the presentation of number compared to shape deviants (p < .05, cluster size > six functional voxels). (B) Regions that were more active during the presentation of shape compared to number deviants (p < .05, cluster size > six functional voxels). (C) Time course of activity (percent signal change) for number-selective (number > shape) regions in the IPS, averaged from individually-drawn functional regions of interest from the IPS, from 3 s pre-stimulus to 12 s post-stimulus.
Figure 4. Data from Individual Children
Figure 4. Data from Individual Children
Each row presents an individual participant's activation map indicating regions that were more active during the presentation of number compared to shape deviants (p < .05, cluster size > eight functional voxels) overlaid on that child's own anatomical images. One child moved during the anatomical scan (which occurred after the functional scan) and is thus not included in this figure.
Figure 5. Child and Adult Number-Selective Brain…
Figure 5. Child and Adult Number-Selective Brain Regions
(Number > shape from Figures 2 and 3) plotted in same space. Adults showed more extensive areas of activation than children; however, the same brain regions were active for children as for adults in this study.

References

    1. Brannon EM, Terrace HS. Ordering of the numerosities 1 to 9 by monkeys. Science. 1998;282:746–749.
    1. Butterworth B. The mathematical brain. London: Macmillan; 1999. 480 pp.
    1. Cantlon JF, Brannon EM. Shared system for ordering small and large numerosities in monkeys and humans. Psychol Sci. 2006 In press.
    1. Feigenson L, Dehaene S, Spelke ES. Core systems of number. Trends Cogn Sci. 2004;8:307–314.
    1. Hauser MD, MacNeilage P, Ware M. Numerical representations in primates. Proc Natl Acad Sci U S A. 1996;93:1514–1517.
    1. Hauser MD, Tsao F, Garcia P, Spelke ES. Evolutionary foundations of number: Spontaneous representation of numerical magnitudes by cotton-top tamarins. Proc Biol Sci. 2003;270:1441–1446.
    1. Gelman R, Gallistel CR. Language and the origin of numerical concepts. Science. 2004;306:441–443.
    1. Meck WH, Church RM. A mode control model of counting and timing processes. J Exp Psychol Anim Behav Process. 1983;9:320–334.
    1. Pica P, Lemer C, Izard V, Dehaene S. Exact and approximate arithmetic in an Amazonian indigene group. Science. 2004;306:499–503.
    1. Whalen J, Gallistel CR, Gelman R. Non-verbal counting in humans: The psychophysics of number representation. Psychol Sci. 1999;10:130–137.
    1. Barth H, Kanwisher N, Spelke E. The construction of large number representations in adults. Cognition. 2003;86:201–221.
    1. Buckley PB, Gillman CB. Comparisons of digits and dot patterns. J Exp Psychol. 1974;103:1131–1136.
    1. Moyer RS, Landauer TK. Time required for judgements of numerical inequality. Nature. 1967;215:1519–1520.
    1. Temple E, Posner MI. Brain mechanisms of quantity are similar in 5-y-old children and adults. Proc Natl Acad Sci U S A. 1998;95:7836–7841.
    1. Dehaene S. The number sense. New York: Oxford University Press; 1997. 288 pp.
    1. Spelke ES, Dehaene S. Biological foundations of numerical thinking. Trends Cogn Sci. 1999;3:365–366.
    1. Spelke ES. Developmental neuroimaging: A developmental psychologist looks ahead. Dev Sci. 2002;5:392–396.
    1. Cipolotti L, Butterworth B, Denes G. A specific deficit for numbers in a case of dense acalculia. Brain. 1991;114:2619–2637.
    1. Dehaene S, Cohen L. Cerebral pathways for calculation: Double dissociation between rote verbal and quantitative knowledge of arithmetic. Cortex. 1997;33:219–250.
    1. Dehaene S, Spelke E, Pinel P, Stanescu R, Tsivkin S. Sources of mathematical thinking: Behavioral and brain-imaging evidence. Science. 1999;284:970–974.
    1. Dehaene S, Piazza M, Pinel P, Cohen L. Three parietal circuits for number processing. Cogn Neuropsychol. 2003;20:487–506.
    1. Dehaene S, Dehaene-Lambertz G, Cohen L. Abstract representations of numbers in the animal and human brain. Trends Neurosci. 1998;21:355–361.
    1. Dehaene S, Molko N, Cohen L, Wilson A. Arithmetic and the brain. Curr Opin Neurobiol. 2004;14:218–224.
    1. Pesenti M, Thioux M, Seron X, De Volder A. Neuroanatomical substrates of Arabic number processing, numerical comparison, and simple addition: A PET study. J Cogn Neuro. 2000;12:461–479.
    1. Stanescu-Cosson R, Pinel P, van de Moortele P, Le Bihan R, Cohen L, et al. Cerebral bases of calculation processes: Impact of number size on the cerebral circuits for exact and approximate calculation. Brain. 2000;123:2240–2255.
    1. Eger E, Sterzer P, Russ MO, Giraud AL, Kleinschmidt A. A supramodal number representation in human intraparietal cortex. Neuron. 2003;37:719–725.
    1. Naccache L, Dehaene S. The priming method: Imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. Cereb Cortex. 2001;11:966–974.
    1. Piazza M, Izard V, Pinel P, Le Bihan D, Dehaene S. Tuning curves for approximate numerosity in the human intraparietal sulcus. Neuron. 2004;44:547–555.
    1. Shuman M, Kanwisher N. Numerical magnitude in the human parietal lobe: Tests of representational generality and domain specificity. Neuron. 2004;44:557–569.
    1. Ansari D, Dhital B, Siong SC. Parametric effects of numerical distance on the intraparietal sulcus during passive viewing of rapid numerosity changes. Brain Res Cogn Brain Res. 2006 In press.
    1. Barth H, La Mont K, Lipton J, Spelke ES. Abstract number and arithmetic in preschool children. Proc Natl Acad Sci U S A. 2005;102:16–21.
    1. Huntley-Fenner G. Children's understanding of number is similar to adults' and rats': Numerical estimation by 5- to 7-y-olds. Cognition. 2001;78:27–40.
    1. Huntley-Fenner G, Cannon E. Preschoolers' magnitude comparisons are mediated by a preverbal analog mechanism. Psychol Sci. 2000;11:147–152.
    1. Brannon EM. The independence of language and mathematical reasoning. Proc Natl Acad Sci U S A. 2005;102:3177–3178.
    1. Gelman R, Butterworth B. Number and language: How are they related? Trends Cogn Sci. 2005;9:6–10.
    1. Gelman R, Gallistel CR. The child's understanding of number. Cambridge (Massachusetts): Harvard University Press; 1978. 280 pp.
    1. Lipton JS, Spelke ES. Origins of number sense: Large-number discrimination in human infants. Psychol Sci. 2003;14:396–401.
    1. Xu F, Spelke ES. Large number discrimination in six-month-old infants. Cognition. 2000;74:B1–B11.
    1. Xu F, Spelke ES, Goddard S. Number sense in human infants. Dev Sci. 2005;8:88–101.
    1. Wynn K. Children's acquisition of the number words and the counting system. Cogn Psychol. 1992;24:220–251.
    1. Wynn K. Children's understanding of counting. Cognition. 1992b;36:155–193.
    1. Le Corre M, Van de Walle G, Brannon EM, Carey S. Re-visiting the competence/performance debate in the acquisition of the counting principles. Cogn Psychol. 2006;52:130–169.
    1. Lipton JS, Spelke ES. Preschool children's mapping of number words to non-symbolic numerosities. Child Dev. 2005;76:978–988.
    1. Fuson K. Relationships between counting and cardinality from age 2 to age 8. In: Bideaud J, Meljac C, Fischer JP, editors. Pathways to number: Children's developing numerical abilities. Hillsdale (New Jersey): Lawrence Erlbaum Associates; 1992. pp. 349–361.
    1. Brannon EM, Van de Walle GA. The development of ordinal numerical competence in young children. Cogn Psychol. 2002;43:53–81.
    1. Grill-Spector K, Kushnir T, Edelman S, Avidan G, Itzchak Y, et al. Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron. 1999;24:187–203.
    1. Buckner RL, Goodman J, Burock M, Rotte M, Koutstaal W, et al. Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI. Neuron. 1998;20:285–296.
    1. Grill-Spector K, Malach F. fMR-adaptation: A tool for studying the functional properties of human cortical neurons. Acta Psychol. 2001;107:293–232.
    1. Huettel SA, Güzeldere G, McCarthy G. Dissociating the neural mechanisms of visual attention in change detection using functional MRI. J Cogn Neurosci. 2001;13:1006–1018.
    1. Kawashima R, O'Sullivan BT, Roland PE. Positron-emission tomography studies of cross-modality inhibition in selective attentional tasks: Closing the “mind's eye.”. Proc Natl Acad Sci U S A. 1995;92:5969–5972.
    1. Laurienti PJ, Burdette JH, Wallace MT, Yen Y, Field AS, et al. Deactivation of sensory-specific cortex by cross-modal stimuli. J Cogn Neurosci. 2002;14:420–429.
    1. Pelphrey KA, Mack PB, Song A, Güzeldere G, McCarthy G. Faces evoke spatially differentiated patterns of BOLD activation and deactivation. NeuroReport. 2003;14:955–959.
    1. Pelphrey KA, Mitchell TV, McKeown M, Goldstein J, Allison T, et al. Brain activity evoked by perception of human walking: Controlling for meaningful coherent motion. J Neurosci. 2003;23:6819–6825.
    1. Wenzel R, Wobst P, Heekeren HH, Kwong KK, Brandt SA, et al. Saccadic suppression induces focal hypooxygenation in the occipital cortex. J Cereb Blood Flow Metab. 2000;7:1103–1110.
    1. Rivera SM, Reiss AL, Eckert MA, Menon V. Developmental changes in mental arithmetic: Evidence for increased functional specialization of the left inferior parietal cortex. Cereb Cortex. 2005;15:1779–1790.
    1. Piazza M, Mechelli A, Butterworth B, Price C. Are subitizing and counting implemented as separate or functionally overlapping processes? Neuroimage. 2002;15:435–446.
    1. Burgund ED, Kang HC, Kelly JE, Buckner RL, Snyder AZ, et al. The feasibility of a common stereotactic space for children and adults in fMRI studies of development. Neuroimage. 2002;17:184–200.
    1. Kang HC, Burgund ED, Lugar HM, Petersen SE, Schlaggar BL. Comparison of functional activation foci in children and adults using a common stereotactic space. Neuroimage. 2002;19:16–28.
    1. Barth H, La Mont K, Lipton J, Dehaene S, Kanwisher N, et al. Non-symbolic arithmetic in adults and young children. Cognition. 2006;98:199–222.
    1. Nieder A. The number domain—can we count on parietal cortex? Neuron. 2004;44:407–409.
    1. Nieder A. Counting on neurons: The neurobiology of numerical competence. Nat Rev Neurosci. 2005;6:177–190.
    1. Carey S. Bootstrapping and the origins of concepts. Daedalus. 2004;4:59–68.
    1. Pinel P, Piazza M, Le Bihan D, Dehaene S. Distributed and overlapping cerebral representations of number, size, and luminance during comparative judgments. Neuron. 2004;41:983–993.
    1. Chochon F, Cohen L, van de Moortele PF, Dehaene S. Differential contributions of the left and right inferior parietal lobules to number processing. J Cogn Neurosci. 1999;11:617–630.
    1. Gobel S, Walsh V, Rushworth M. The mental number line and the human angular gyrus. Neuroimage. 2001;14:1278–1289.
    1. Rusconi E, Walsh V, Butterworth B. Dexterity with numbers: rTMS over left angular gyrus disrupts finger gnosis and number processing. Neuropsychologia. 2005;43:1609–1624.
    1. Cantlon JF, Brannon EM. Semantic congruity affects numerical judgments similarly in monkeys and humans. Proc Natl Acad Sci U S A. 2005;102:16507–16511.
    1. Nieder A, Miller EK. Coding of cognitive magnitude: Compressed scaling of numerical information in the primate prefrontal cortex. Neuron. 2003;34:149–157.
    1. Wynn K. An evolved capacity for number. In: Cummins-Dellarosa D, Allen C, editors. The evolution of mind. New York: Oxford University Press; 1998. pp. 107–126.
    1. Glover G, Law C. Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn Res Med. 2001;46:515–522.
    1. Guo H, Song A. Single-shot spiral image acquisition with embedded z-shimming for susceptibility signal recovery. J Magn Res Imaging. 2003;18:389–395.

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