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Research Article

Syllabic discrimination in premature human infants prior to complete formation of cortical layers

Mahdi Mahmoudzadeh, Ghislaine Dehaene-Lambertz, Marc Fournier, Guy Kongolo, Sabrina Goudjil, Jessica Dubois, Reinhard Grebe, and Fabrice Wallois
  1. aInstitut National de la Santé et de la Recherche Médicale (INSERM) U1105, GRAMFC, Université de Picardie Jules Verne, CHU Amiens, F80000 Amiens, France;
  2. bINSERM U992, Cognitive Neuroimaging Unit, F91191 Gif-sur-Yvette, France;
  3. cCommissariat à l’Energie Atomique, NeuroSpin, F91191 Gif-sur-Yvette, France; and
  4. dUniversité Paris XI, F91405 Orsay, France

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PNAS first published February 25, 2013; https://doi.org/10.1073/pnas.1212220110
Mahdi Mahmoudzadeh
aInstitut National de la Santé et de la Recherche Médicale (INSERM) U1105, GRAMFC, Université de Picardie Jules Verne, CHU Amiens, F80000 Amiens, France;
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Ghislaine Dehaene-Lambertz
bINSERM U992, Cognitive Neuroimaging Unit, F91191 Gif-sur-Yvette, France;
cCommissariat à l’Energie Atomique, NeuroSpin, F91191 Gif-sur-Yvette, France; and
dUniversité Paris XI, F91405 Orsay, France
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Marc Fournier
aInstitut National de la Santé et de la Recherche Médicale (INSERM) U1105, GRAMFC, Université de Picardie Jules Verne, CHU Amiens, F80000 Amiens, France;
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Guy Kongolo
aInstitut National de la Santé et de la Recherche Médicale (INSERM) U1105, GRAMFC, Université de Picardie Jules Verne, CHU Amiens, F80000 Amiens, France;
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Sabrina Goudjil
aInstitut National de la Santé et de la Recherche Médicale (INSERM) U1105, GRAMFC, Université de Picardie Jules Verne, CHU Amiens, F80000 Amiens, France;
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Jessica Dubois
bINSERM U992, Cognitive Neuroimaging Unit, F91191 Gif-sur-Yvette, France;
cCommissariat à l’Energie Atomique, NeuroSpin, F91191 Gif-sur-Yvette, France; and
dUniversité Paris XI, F91405 Orsay, France
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Reinhard Grebe
aInstitut National de la Santé et de la Recherche Médicale (INSERM) U1105, GRAMFC, Université de Picardie Jules Verne, CHU Amiens, F80000 Amiens, France;
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Fabrice Wallois
aInstitut National de la Santé et de la Recherche Médicale (INSERM) U1105, GRAMFC, Université de Picardie Jules Verne, CHU Amiens, F80000 Amiens, France;
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  • For correspondence: fabrice.wallois@u-picardie.fr
  1. Edited by Patricia Kuhl, University of Washington, Seattle, WA, and approved January 22, 2013 (received for review July 19, 2012)

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Abstract

The ontogeny of linguistic functions in the human brain remains elusive. Although some auditory capacities are described before term, whether and how such immature cortical circuits might process speech are unknown. Here we used functional optical imaging to evaluate the cerebral responses to syllables at the earliest age at which cortical responses to external stimuli can be recorded in humans (28- to 32-wk gestational age). At this age, the cortical organization in layers is not completed. Many neurons are still located in the subplate and in the process of migrating to their final location. Nevertheless, we observed several points of similarity with the adult linguistic network. First, whereas syllables elicited larger right than left responses, the posterior temporal region escaped this general pattern, showing faster and more sustained responses over the left than over the right hemisphere. Second, discrimination responses to a change of phoneme (ba vs. ga) and a change of human voice (male vs. female) were already present and involved inferior frontal areas, even in the youngest infants (29-wk gestational age). Third, whereas both types of changes elicited responses in the right frontal region, the left frontal region only reacted to a change of phoneme. These results demonstrate a sophisticated organization of perisylvian areas at the very onset of cortical circuitry, 3 mo before term. They emphasize the influence of innate factors on regions involved in linguistic processing and social communication in humans.

  • hemodynamic response
  • premature human brain
  • language
  • hemispheric lateralization
  • near infrared spectroscopy

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: fabrice.wallois{at}u-picardie.fr.
  • Author contributions: G.D.-L., G.K., S.G., and F.W. designed research; M.M. and F.W. performed research; M.M. and J.D. contributed new reagents/analytic tools; M.M., G.D.-L., M.F., and R.G. analyzed data; and M.M., G.D.-L., and F.W. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1212220110/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Syllabic discrimination in premature human infants
Mahdi Mahmoudzadeh, Ghislaine Dehaene-Lambertz, Marc Fournier, Guy Kongolo, Sabrina Goudjil, Jessica Dubois, Reinhard Grebe, Fabrice Wallois
Proceedings of the National Academy of Sciences Feb 2013, 201212220; DOI: 10.1073/pnas.1212220110

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Syllabic discrimination in premature human infants
Mahdi Mahmoudzadeh, Ghislaine Dehaene-Lambertz, Marc Fournier, Guy Kongolo, Sabrina Goudjil, Jessica Dubois, Reinhard Grebe, Fabrice Wallois
Proceedings of the National Academy of Sciences Feb 2013, 201212220; DOI: 10.1073/pnas.1212220110
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