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Congenital foot deformation alters the topographic organization in the primate somatosensory system

Abstract

Limbs may fail to grow properly during fetal development, but the extent to which such growth alters the nervous system has not been extensively explored. Here we describe the organization of the somatosensory system in a 6-year-old monkey (Macaca radiata) born with a deformed left foot in comparison to the results from a normal monkey (Macaca fascicularis). Toes 1, 3, and 5 were missing, but the proximal parts of toes 2 and 4 were present. We used anatomical tracers to characterize the patterns of peripheral input to the spinal cord and brainstem, as well as between thalamus and cortex. We also determined the somatotopic organization of primary somatosensory area 3b of both hemispheres using multiunit electrophysiological recording. Tracers were subcutaneously injected into matching locations of each foot to reveal their representations within the lumbar spinal cord, and the gracile nucleus (GrN) of the brainstem. Tracers injected into the representations of the toes and plantar pads of cortical area 3b labeled neurons in the ventroposterior lateral nucleus (VPL) of the thalamus. Contrary to the orderly arrangement of the foot representation throughout the lemniscal pathway in the normal monkey, the plantar representation of the deformed foot was significantly expanded and intruded into the expected representations of toes in the spinal cord, GrN, VPL, and area 3b. We also observed abnormal representation of the intact foot in the ipsilateral spinal cord and contralateral area 3b. Thus, congenital malformation influences the somatotopic representation of the deformed as well as the intact foot.

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Acknowledgments

This study is supported by National Institutes of Health Grant NS16446 to Jon H. Kaas and National Institutes of Health Grant NS067017 to Hui-Xin Qi. We are grateful to Laura Trice for help with histological procedures and Mary Feurtado for surgical assistance.

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Correspondence to Chia-Chi Liao.

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Liao, CC., Qi, HX., Reed, J.L. et al. Congenital foot deformation alters the topographic organization in the primate somatosensory system. Brain Struct Funct 221, 383–406 (2016). https://doi.org/10.1007/s00429-014-0913-7

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Keywords

  • Congenital limb deficiency
  • Macaque
  • Somatotopy
  • Plasticity
  • Reorganization