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Growth and refinement of excitatory synapses in the human auditory cortex

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Abstract

We had earlier demonstrated a neurofilament-rich plexus of axons in the presumptive human auditory cortex during fetal development which became adult-like during infancy. To elucidate the origin of these axons, we studied the expression of the vesicular glutamate transporters (VGLUT) 1 and 2 in the human auditory cortex at different stages of development. While VGLUT-1 expression predominates in intrinsic and cortico-cortical synapses, VGLUT-2 expression predominates in thalamocortical synapses. Levels of VGLUT-2 mRNA were higher in the auditory cortex before birth compared to postnatal development. In contrast, levels of VGLUT-1 mRNA were low before birth and increased during postnatal development to peak during childhood and then began to decrease in adolescence. Both VGLUT-1 and VGLUT-2 proteins were present in the human auditory cortex as early as 15GW. Further, immunohistochemistry revealed that the supra- and infragranular layers were more immunoreactive for VGLUT-1 compared to that in Layer IV at 34GW and this pattern was maintained until adulthood. As for VGLUT-1 mRNA, VGLUT-1 synapses increased in density between prenatal development and childhood in the human auditory cortex after which they appeared to undergo attrition or pruning. The adult pattern of VGLUT-2 immunoreactivity (a dense band of VGLUT-2-positive terminals in Layer IV) also began to appear in the presumptive Heschl’s gyrus at 34GW. The density of VGLUT-2-positive puncta in Layer IV increased between prenatal development and adolescence, followed by a decrease in adulthood, suggesting that thalamic axons which innervate the human auditory cortex undergo pruning comparatively late in development.

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Acknowledgments

This work was supported by intramural funds from the National Brain Research Centre, Manesar. The authors gratefully acknowledge the support provided by NBRC and Dr. OP Sharma for setting up the collection of post-mortem tissue and Ram Mehar (NBRC, Manesar) for technical support. We are also grateful to Dr. Supriya Bhavnani (NBRC, Manesar), Himanshu Malhotra and Prof. Manoj Raje (IMTECH, Chandigarh) for help with confocal microscopy and Dr. V.Rema (NBRC, Manesar) and the reviewers for their insightful comments which helped improve this manuscript. This study was supported initially by a grant from the Department of Biotechnology, India (BT/PR5373/MED/14/630/2004) to SI and funds from NBRC, Manesar, India.

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    1. Division of Systems Neuroscience, National Brain Research Centre (Deemed University), NH-8, Manesar, Gurgaon, Haryana, 122051, India

      Arvind Singh Pundir, Utkarsha A. Singh, Nikhil Ahuja, Sonal Makhija & Soumya Iyengar

    2. Department of Forensic Medicine, Maulana Azad Medical College, Bahadur Shah Zafar Marg, New Delhi, 110002, India

      P. C. Dikshit

    3. Department of Histopathology, Post Graduate Institute of Medical Education and Research, Sector-12, Chandigarh, 160012, India

      Bishan Radotra

    4. Department of Obstetrics and Gynecology, Base Hospital, Delhi Cantonment, Delhi, 110010, India

      Praveen Kumar

    5. Department of Neuropathology, National Institute of Mental Health and Allied Sciences, Hosur Road, Bangalore, 560029, India

      S. K. Shankar & Anita Mahadevan

    6. Department of Anatomy, All India Institute of Medical Sciences, New Delhi, 110002, India

      T. S. Roy

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    A. S. Pundir and U. A. Singh have contributed equally to this manuscript.

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    Pundir, A.S., Singh, U.A., Ahuja, N. et al. Growth and refinement of excitatory synapses in the human auditory cortex. Brain Struct Funct 221, 3641–3674 (2016). https://doi.org/10.1007/s00429-015-1124-6

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