Early sensory experience influences the development of multisensory thalamocortical and intracortical connections of primary sensory cortices

  • Julia U. Henschke
  • Anja M. Oelschlegel
  • Frank Angenstein
  • Frank W. Ohl
  • Jürgen Goldschmidt
  • Patrick O. Kanold
  • Eike Budinger
Original Article

Abstract

The nervous system integrates information from multiple senses. This multisensory integration already occurs in primary sensory cortices via direct thalamocortical and corticocortical connections across modalities. In humans, sensory loss from birth results in functional recruitment of the deprived cortical territory by the spared senses but the underlying circuit changes are not well known. Using tracer injections into primary auditory, somatosensory, and visual cortex within the first postnatal month of life in a rodent model (Mongolian gerbil) we show that multisensory thalamocortical connections emerge before corticocortical connections but mostly disappear during development. Early auditory, somatosensory, or visual deprivation increases multisensory connections via axonal reorganization processes mediated by non-lemniscal thalamic nuclei and the primary areas themselves. Functional single-photon emission computed tomography of regional cerebral blood flow reveals altered stimulus-induced activity and higher functional connectivity specifically between primary areas in deprived animals. Together, we show that intracortical multisensory connections are formed as a consequence of sensory-driven multisensory thalamocortical activity and that spared senses functionally recruit deprived cortical areas by an altered development of sensory thalamocortical and corticocortical connections. The functional–anatomical changes after early sensory deprivation have translational implications for the therapy of developmental hearing loss, blindness, and sensory paralysis and might also underlie developmental synesthesia.

Keywords

Cross-modal Deprivation Development Sensory integration Rodent Synesthesia 

Supplementary material

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Supplementary material 1 (PDF 2237 kb)

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Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department Systems Physiology of LearningLeibniz Institute for NeurobiologyMagdeburgGermany
  2. 2.German Center for Neurodegenerative Diseases Within the Helmholtz AssociationMagdeburgGermany
  3. 3.Institute of Cognitive Neurology and Dementia Research (IKND)Otto-von-Guericke-University MagdeburgMagdeburgGermany
  4. 4.Research Group NeuropharmacologyLeibniz Institute for NeurobiologyMagdeburgGermany
  5. 5.Institute of AnatomyOtto-von-Guericke-University MagdeburgMagdeburgGermany
  6. 6.Functional Neuroimaging GroupGerman Center for Neurodegenerative Diseases Within the Helmholtz AssociationMagdeburgGermany
  7. 7.Institute of BiologyOtto-von-Guericke-University MagdeburgMagdeburgGermany
  8. 8.Department of BiologyUniversity of MarylandCollege ParkUSA
  9. 9.Center for Behavioral Brain SciencesMagdeburgGermany

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