Early sensory experience influences the development of multisensory thalamocortical and intracortical connections of primary sensory cortices
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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.
KeywordsCross-modal Deprivation Development Sensory integration Rodent Synesthesia
We like to thank K. Böttger, A. Gürke, D. Montag, J. Stallmann, and D. Vincenz-Zörner for excellent technical assistance. We also thank the three anonymous reviewers for their most helpful comments on the manuscript. This work was supported by the DFG (http://www.dfg.de) SFB TRR31 (J.U.H., F.W.O., E.B.) and NIH (http://www.nih.gov) RO1 DC009607 (P.O.K.).
Compliance with ethical standards
Informed consent was obtained from all individual participants included in the study.
Conflict of interest
All authors declare that they have no financial, personal, or professional conflict of interest.
Authors declare that all animal studies have been approved by the appropriate ethics committee (see “Materials and methods”) and have, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.
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