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Maturation of glutamatergic transmission in the vestibulo-olivary pathway impacts on the registration of head rotational signals in the brainstem of rats

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Abstract

The recognition of head orientation in the adult involves multi-level integration of inputs within the central vestibular circuitry. How the different inputs are recruited during postnatal development remains unclear. We hypothesize that glutamatergic transmission at the vestibular nucleus contributes to developmental registration of head orientations along the vestibulo-olivary pathway. To investigate the maturation profile by which head rotational signals are registered in the brainstem, we used sinusoidal rotations on the orthogonal planes of the three pairs of semicircular canals. Fos expression was used as readout of neurons responsive to the rotational stimulus. Neurons in the vestibular nucleus and prepositus hypoglossal nucleus responded to all rotations as early as P4 and reached adult numbers by P21. In the reticular formation and inferior olive, neurons also responded to horizontal rotations as early as P4 but to vertical rotations not until P21 and P25, respectively. Neuronal subpopulations that distinguish between rotations activating the orthogonally oriented vertical canals were identifiable in the medial and spinal vestibular nuclei by P14 and in the inferior olivary subnuclei IOβ and IOK by P25. Neonatal perturbation of glutamate transmission in the vestibular nucleus was sufficient to derange formation of this distribution in the inferior olive. This is the first demonstration that developmental refinement of glutamatergic synapses in the central vestibular circuitry is essential for developmental registration of head rotational signals in the brainstem.

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Acknowledgments

We are grateful to Simon S. M. Chan for calibration of the mechanical set-up and Kimmy F. L. Tsang for assistance with histology and radioisotope work. This study was supported by GRF grants of the Hong Kong Research Grants Council (HKU 761409, 761710, 761711).

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  1. Suk-King Lai

    Present address: Department of Neurophysiology, Tokyo University, Tokyo, 113-0033, Japan

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  1. Department of Physiology, LKS Faculty of Medicine, The University of Hong Kong, 21 Sassoon Road, Hong Kong, People’s Republic of China

    Chun-Hong Lai, Chun-Wai Ma, Suk-King Lai, Lei Han & Ying-Shing Chan

  2. Department of Biochemistry, LKS Faculty of Medicine, The University of Hong Kong, 21 Sassoon Road, Hong Kong, People’s Republic of China

    Chun-Wai Ma & Daisy Kwok-Yan Shum

  3. Department of Orthopaedics and Traumatology, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong, People’s Republic of China

    Hoi-Man Wong & Kelvin Wai-Kwok Yeung

  4. Research Centre of Heart, Brain, Hormone and Healthy Aging, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, People’s Republic of China

    Suk-King Lai, Lei Han, Daisy Kwok-Yan Shum & Ying-Shing Chan

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C. H. Lai and C. W. Ma contributed equally to the work.

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Lai, CH., Ma, CW., Lai, SK. et al. Maturation of glutamatergic transmission in the vestibulo-olivary pathway impacts on the registration of head rotational signals in the brainstem of rats. Brain Struct Funct 221, 217–238 (2016). https://doi.org/10.1007/s00429-014-0903-9

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