Opinion
Origins of the specialization for letters and numbers in ventral occipitotemporal cortex

https://doi.org/10.1016/j.tics.2015.05.006Get rights and content

Highlights

  • The VWFA and NFA are areas specializing in letter and number recognition, respectively.

  • The locations of these symbol form areas are conserved in blind participants.

  • Their existence cannot be explained by evolutionary changes or visual constraints.

  • Symbol form areas may emerge from connectivity biases and/or shape feature preferences.

Deep in the occipitotemporal cortex lie two functional regions, the visual word form area (VWFA) and the number form area (NFA), which are thought to play a special role in letter and number recognition, respectively. We review recent progress made in characterizing the origins of these symbol form areas in children or adults, sighted or blind subjects, and humans or monkeys. We propose two non-mutually-exclusive hypotheses on the origins of the VWFA and NFA: the presence of a connectivity bias, and a sensitivity to shape features. We assess the explanatory power of these hypotheses, describe their consequences, and offer several experimental tests.

Section snippets

The puzzle of symbol form areas in the brain

Written symbols such as letters or numbers are a late but far-reaching addition to the mental toolkit of humanity. It should therefore be no surprise that the brain dedicates significant resources to recognizing them. More surprising is that these resources, the VWFA and the NFA, are always localized and highly reproducible in the occipitotemporal cortex across subjects, fonts, and even sensory modalities. This is especially puzzling because letters and numbers are such recent cultural

Two hypotheses for symbol form areas in vOTC

We spell out two hypotheses on the initial conditions that lead to the maturation of the letter and number form areas depicted in Figure 1. These hypotheses are not mutually exclusive but have distinct consequences.

Concluding remarks

Symbol form areas are highly reproducible in vOTC across subjects of different cultures, and localized proto-symbol form areas also consistently emerge in IT cortex after training juvenile macaques. Nonetheless, these areas could not have specifically evolved for processing symbols, and their locations, which are conserved in congenitally blind humans, cannot proceed from purely visual constraints. Our analysis of the available data suggests that two hypotheses, the biased connectivity and the

Acknowledgments

The research leading to these results has received funding from the European Commission Seventh Framework Programme (FP7/2007-2013) under grant agreement 604102 (Human Brain Project), from the program ‘Investissements d’Avenir’ ANR-10-IAIHU-06, and was supported by INSERM, the CEA, the Collège de France, and the Bettencourt-Schueller foundation. A.A. is a European Research Council (ERC) fellow and is supported by ERC-ITG grant (310809) as well as the Gatsby Charitable Foundation and a James S.

Glossary

Deep convolutional networks
neural network systems inspired from the primate brain, which classify patterns using a hierarchy of layers with restricted receptive fields, and interleaved pooling and sampling units.
Diffusion tensor imaging (DTI)/tractography
DTI is a brain-imaging technique whereby the properties of neural tissues are inferred from the pattern of diffusion of water molecules as measured by MRI. Tractography is the application of computerized algorithms to DTI images of white matter

References (107)

  • S. Dehaene

    Why do children make mirror errors in reading? Neural correlates of mirror invariance in the visual word form area

    Neuroimage

    (2010)
  • F. Pegado

    Breaking the symmetry: mirror discrimination for single letters but not for pictures in the visual word form area

    Neuroimage

    (2011)
  • N. Logothetis

    Shape representation in the inferior temporal cortex of monkeys

    Curr. Biol.

    (1995)
  • J. Maier

    Reading with the ears

    Neurosci. Lett.

    (2004)
  • T. Schmidt-Wilcke

    Distinct patterns of functional and structural neuroplasticity associated with learning Morse code

    Neuroimage

    (2010)
  • A. Pascual-Leone et al.

    The metamodal organization of the brain

    Prog. Brain. Res.

    (2001)
  • I. Matteau

    Beyond visual, aural and haptic movement perception: hMTþ is activated by electrotactile motion stimulation of the tongue in sighted and in congenitally blind individuals

    Brain Res. Bull.

    (2010)
  • C. Poirier

    Specific activation of the V5 brain area by auditory motion processing: an fMRI study

    Cogn. Brain Res.

    (2005)
  • E. Striem-Amit et al.

    Visual cortex extrastriate body-selective area activation in congenitally blind people ‘seeing’ by using sounds

    Curr. Biol.

    (2014)
  • O. Collignon

    Sensory rehabilitation in the plastic brain

    Prog. Brain Res.

    (2011)
  • T. Kohonen

    Essentials of the self-organizing map

    Neural Netw.

    (2013)
  • U. Hasson

    Large-scale mirror-symmetry organization of human occipito-temporal object areas

    Neuron

    (2003)
  • J.R. Binder

    Tuning of the human left fusiform gyrus to sublexical orthographic structure

    Neuroimage

    (2006)
  • S. Dehaene

    Reading in the Brain

    (2009)
  • S. Dehaene et al.

    Towards an anatomical and functional model of number processing

    Math. Cogn.

    (1995)
  • J. Shum

    A brain area for visual numerals

    J. Neurosci.

    (2013)
  • J.J. Dejerine

    Contribution à l’étude anatomo-pathologique et clinique des différentes variétés de cécité verbale

    Mem. Soc. Biol.

    (1892)
  • L. Cohen et al.

    Number processing in pure alexia: the effect of hemispheric asymmetries and task demands

    Neurocase

    (1995)
  • L. Cohen et al.

    Cerebral networks for number processing: evidence from a case of posterior callosal lesion

    Neurocase

    (1996)
  • R. Starrfelt et al.

    Number reading in pure alexia – a review

    Neuropsychologia

    (2011)
  • S. Abboud

    A number-form area in the blind

    Nat. Commun.

    (2015)
  • S. Abboud

    EyeMusic: introducing a ‘visual’ colorful experience for the blind using auditory sensory substitution

    Restor. Neurol. Neurosci.

    (2013)
  • A. Nieder et al.

    Representation of number in the brain

    Annu. Rev. Neurosci.

    (2009)
  • L. Cohen

    The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients

    Brain

    (2000)
  • S. Dehaene

    Letter binding and invariant recognition of masked words: behavioral and neuroimaging evidence

    Psychol. Sci.

    (2004)
  • L.S. Glezer

    Adding words to the brain's visual dictionary: novel word learning selectively sharpens orthographic representations in the VWFA

    J. Neurosci.

    (2015)
  • S. Dehaene

    The visual word form area. A prelexical representation of visual words in the fusiform gyrus

    Neuroreport

    (2002)
  • Y.N. Yoncheva

    Auditory selective attention to speech modulates activity in the visual word form area

    Cereb. Cortex

    (2010)
  • S. Dehaene

    How learning to read changes the cortical networks for vision and language

    Science

    (2010)
  • M. Ben-Shachar

    The development of cortical sensitivity to visual word forms

    J. Cogn. Neurosci.

    (2011)
  • P. Pinel et al.

    Beyond hemispheric dominance: brain regions underlying the joint lateralization of language and arithmetic to the left hemisphere

    J. Cogn. Neurosci.

    (2010)
  • Q. Cai

    The left ventral occipito-temporal response to words depends on language lateralization but not on visual familiarity

    Cereb. Cortex

    (2010)
  • C. Büchel

    Different activation patterns in the visual cortex of late and congenitally blind subjects

    Brain

    (1998)
  • L. Reich

    A ventral visual stream reading center independent of visual experience

    Curr. Biol.

    (2011)
  • N. Kanwisher

    The fusiform face area: a module in human extrastriate cortex specialized for the perception of faces

    J. Neurosci.

    (1997)
  • R.F. Schwarzlose

    Separate face and body selectivity on the fusiform gyrus

    J. Neurosci.

    (2005)
  • K. Grill-Spector et al.

    The functional architecture of the ventral temporal cortex and its role in categorization

    Nat. Rev. Neurosci.

    (2014)
  • J.F. Cantlon

    Cortical representations of symbols, objects, and faces are pruned back during early childhood

    Cereb. Cortex

    (2011)
  • S. Brem

    Brain sensitivity to print emerges when children learn letter–speech sound correspondences

    Proc. Natl. Acad. Sci. U.S.A.

    (2010)
  • J.D. Yeatman

    The development of white matter and reading skills

    Proc. Natl. Acad. Sci. U.S.A.

    (2012)
  • Cited by (155)

    View all citing articles on Scopus
    View full text