Distinct Cerebral Pathways for Object Identity and Number in Human Infants

All humans, regardless of their culture and education, possess an intuitive understanding of number. Behavioural evidence suggests that numerical competence may be present early on in infancy. Here, we present brain-imaging evidence for distinct cerebral coding of number and object identity in 3-mo-old infants. We compared the visual event-related potentials evoked by unforeseen changes either in the identity of objects forming a set, or in the cardinal of this set. In adults and 4-y-old children, number sense relies on a dorsal system of bilateral intraparietal areas, different from the ventral occipitotemporal system sensitive to object identity. Scalp voltage topographies and cortical source modelling revealed a similar distinction in 3-mo-olds, with changes in object identity activating ventral temporal areas, whereas changes in number involved an additional right parietoprefrontal network. These results underscore the developmental continuity of number sense by pointing to early functional biases in brain organization that may channel subsequent learning to restricted brain areas.

[1]  T. Simon,et al.  The foundations of numerical thinking in a brain without numbers , 1999, Trends in Cognitive Sciences.

[2]  Mark H Johnson,et al.  Development of face-sensitive event-related potentials during infancy: a review. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[3]  Teodora Gliga,et al.  Structural Encoding of Body and Face in Human Infants and Adults , 2005, Journal of Cognitive Neuroscience.

[4]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[5]  S. Carey,et al.  On the limits of infants' quantification of small object arrays , 2005, Cognition.

[6]  永福 智志 The Organization of Learning , 2005, Journal of Cognitive Neuroscience.

[7]  Philippe Pinel,et al.  Tuning Curves for Approximate Numerosity in the Human Intraparietal Sulcus , 2004, Neuron.

[8]  T. Gliga,et al.  Development of a view-invariant representation of the human head , 2007, Cognition.

[9]  Rochel Gelman,et al.  Variability signatures distinguish verbal from nonverbal counting for both large and small numbers , 2001, Psychonomic bulletin & review.

[10]  Elizabeth S. Spelke,et al.  Chronometric studies of numerical cognition in five-month-old infants , 2005, Cognition.

[11]  E. Spelke,et al.  Infants' Discrimination of Number vs. Continuous Extent , 2002, Cognitive Psychology.

[12]  Andreas Nieder,et al.  Temporal and Spatial Enumeration Processes in the Primate Parietal Cortex , 2006, Science.

[13]  H S Terrace,et al.  Ordering of the numerosities 1 to 9 by monkeys. , 1998, Science.

[14]  P. Starkey,et al.  Perception of numbers by human infants. , 1980, Science.

[15]  V Menon,et al.  Cerebral Cortex doi:10.1093/cercor/bhi055 Developmental Changes in Mental Arithmetic: Evidence for Increased Functional Specialization in the Left Inferior Parietal Cortex , 2005 .

[16]  Renée Baillargeon,et al.  Why do young infants fail to search for hidden objects? , 1990, Cognition.

[17]  S. Carey,et al.  Infants’ Metaphysics: The Case of Numerical Identity , 1996, Cognitive Psychology.

[18]  Fei Xu,et al.  Sortal concepts, object individuation, and language , 2007, Trends in Cognitive Sciences.

[19]  M. Sigman,et al.  Functional organization of perisylvian activation during presentation of sentences in preverbal infants , 2006, Proceedings of the National Academy of Sciences.

[20]  E. Spelke Nativism, empiricism, and the origins of knowledge , 1998 .

[21]  J. Kagan,et al.  Effect of Auditory Numerical Information on Infants ' Looking Behavior : Contradictory Evidence , 2004 .

[22]  John E Richards,et al.  Familiarization, attention, and recognition memory in infancy: an event-related potential and cortical source localization study. , 2005, Developmental psychology.

[23]  Susan Carey,et al.  One, two, three, four, nothing more: An investigation of the conceptual sources of the verbal counting principles , 2007, Cognition.

[24]  S. Carey Bootstrapping & the origin of concepts , 2004, Daedalus.

[25]  S. Dehaene,et al.  Timing of the brain events underlying access to consciousness during the attentional blink , 2005, Nature Neuroscience.

[26]  Daniel P. Keating,et al.  Perception of numerical invariance in neonates. , 1983, Child development.

[27]  S. Carey,et al.  Knowledge of Number: Its Evolution and Ontogeny , 1998, Science.

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

[29]  Andreas Nieder,et al.  A parieto-frontal network for visual numerical information in the monkey. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Baillargeon Young infants’ expectations about hidden objects: a reply to three challenges , 1999 .

[31]  Mark H. Johnson,et al.  The “what” and “where” of object representations in infancy , 2003, Cognition.

[32]  Jacques Mehler,et al.  How do 4-day-old infants categorize multisyllabic utterances? , 1993 .

[33]  S E Antell,et al.  Perception of numerical invariance in neonates. , 1983, Child development.

[34]  Elizabeth S Spelke,et al.  Origins of Number Sense , 2003, Psychological science.

[35]  Rochel Gelman,et al.  Language and Conceptual Development series Number and language : how are they related ? , 2004 .

[36]  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.

[37]  A. Streri,et al.  Evidence of amodal representation of small numbers across visuo-tactile modalities in 5-month-old infants , 2006 .

[38]  Lisa Feigenson,et al.  Tracking individuals via object-files: evidence from infants' manual search , 2003 .

[39]  Kelly S. Mix,et al.  Numerical abstraction in infants: another look. , 1997, Developmental psychology.

[40]  A. Meltzoff,et al.  OBJECT REPRESENTATION, IDENTITY, AND THE PARADOX OF EARLY PERMANENCE: Steps Toward a New Framework. , 1998, Infant behavior & development.

[41]  E. Spelke,et al.  Large number discrimination in 6-month-old infants , 2000, Cognition.

[42]  C. Nelson,et al.  Neural correlates of attention and memory in the first year of life , 1992 .

[43]  Susan Carey,et al.  Spontaneous number representation in semi–free–ranging rhesus monkeys , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  Kelly S. Mix,et al.  Number Versus Contour Length in Infants' Discrimination of Small Visual Sets , 1999 .

[45]  S. Dehaene,et al.  Speed and cerebral correlates of syllable discrimination in infants , 1994, Nature.

[46]  Lisa Feigenson,et al.  A double-dissociation in infants' representations of object arrays , 2005, Cognition.

[47]  N. Kraus,et al.  The time course of auditory perceptual learning: neurophysiological changes during speech‐sound training , 1998, Neuroreport.

[48]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[49]  E. Spelke,et al.  Language and Conceptual Development series Core systems of number , 2004 .

[50]  Michael J Beran,et al.  Rhesus monkeys (Macaca mulatta) enumerate large and small sequentially presented sets of items using analog numerical representations. , 2007, Journal of experimental psychology. Animal behavior processes.

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

[52]  A. Norcia,et al.  Event-related brain potentials to human faces in infants. , 1981, Child Development.

[53]  Karen Wynn,et al.  Addition and subtraction by human infants , 1992, Nature.

[54]  E. J. Carter,et al.  Functional Imaging of Numerical Processing in Adults and 4-y-Old Children , 2006, PLoS biology.

[55]  E. Spelke,et al.  Numerical abstraction by human infants , 1990, Cognition.

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

[57]  Andrea Berger,et al.  Infant brains detect arithmetic errors , 2006, Proceedings of the National Academy of Sciences.

[58]  Elizabeth S. Spelke,et al.  Sources of Flexibility in Human Cognition: Dual-Task Studies of Space and Language , 1999, Cognitive Psychology.

[59]  Mark H. Johnson,et al.  Distinct Processing of Objects and Faces in the Infant Brain , 2008, Journal of Cognitive Neuroscience.

[60]  E. Spelke,et al.  Detection of intermodal numerical correspondences by human infants. , 1983, Science.

[61]  S. Carey,et al.  The Representations Underlying Infants' Choice of More: Object Files Versus Analog Magnitudes , 2002, Psychological science.

[62]  Andreas Nieder,et al.  A Labeled-Line Code for Small and Large Numerosities in the Monkey Prefrontal Cortex , 2007, The Journal of Neuroscience.

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

[64]  R H Bayford,et al.  Two-dimensional finite element modelling of the neonatal head. , 2000, Physiological measurement.

[65]  Daniel Ansari,et al.  Age-related Changes in the Activation of the Intraparietal Sulcus during Nonsymbolic Magnitude Processing: An Event-related Functional Magnetic Resonance Imaging Study , 2006, Journal of Cognitive Neuroscience.

[66]  S. Dehaene,et al.  Functional Neuroimaging of Speech Perception in Infants , 2002, Science.

[67]  H S Terrace,et al.  Representation of the numerosities 1-9 by rhesus macaques (Macaca mulatta). , 2000, Journal of experimental psychology. Animal behavior processes.

[68]  A. Diamond Developmental Time Course in Human Infants and Infant Monkeys, and the Neural Bases of, Inhibitory Control in Reaching a , 1990, Annals of the New York Academy of Sciences.

[69]  S. Sternberg,et al.  Separate modifiability, mental modules, and the use of pure and composite measures to reveal them. , 2001, Acta psychologica.