Distribution of excitatory and inhibitory axon terminals on the rat hypoglossal motoneurons
- 125 Downloads
Detailed information about the excitatory and inhibitory synapses on the hypoglossal motoneurons may help understand the neural mechanism for control of the hypoglossal motoneuron excitability and hence the precise and coordinated movements of the tongue during chewing, swallowing and licking. For this, we investigated the distribution of GABA-, glycine (Gly)- and glutamate (Glut)-immunopositive (+) axon terminals on the genioglossal (GG) motoneurons by retrograde tracing, electron microscopic immunohistochemistry, and quantitative analysis. Small GG motoneurons (< 400 μm2 in cross-sectional area) had fewer primary dendrites, significantly higher nuclear/cytoplasmic ratio, and smaller membrane area covered by synaptic boutons than large GG motoneurons (> 400 μm2). The fraction of inhibitory boutons (GABA + only, Gly + only, and mixed GABA +/Gly + boutons) of all boutons was significantly higher for small GG motoneurons than for large ones, whereas the fraction of Glut + boutons was significantly higher for large GG motoneurons than for small ones. Almost all boutons (> 95%) on both small and large GG motoneurons were GABA + , Gly + or Glut + . The frequency of mixed GABA +/Gly + boutons was the highest among inhibitory boutons types for both small and large GG motoneurons. These findings may elucidate the anatomical substrate for precise regulation of the motoneuron firing required for the fine movements of the tongue, and also suggest that the excitability of small and large GG motoneurons may be regulated differently.
KeywordsHypoglossal motoneuron Excitatory Inhibitory Presynaptic axon terminal Immunohistochemistry Electron microscopy
The authors sincerely thank Dr. Juli Valtschanoff for helpful discussion and careful reading of the manuscript. We also sincerely thank Dr. O.P. Ottersen for the gift of the glutamate, GABA and glycine antibodies and the sandwich block for the test sections.
This work was supported by the National Research Foundation of Korea (NRF) Grant funded by the Korea government (MSIT, NRF-2017R1A5A2015391, NRF-2017R1A2B2003561).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
- Bach-y-Rita P, Lennerstrand G, Alvarado J, Nichols K, McHolm G (1977) Extraocular muscle fibers: ultrastructural identification of iontophoretically labeled fibers contracting in response to succinylcholine. Invest Ophthalmol Vis Sci 16:561–565Google Scholar
- Bae YC, Choi BJ, Lee MG, Lee HJ, Park KP, Zhang LF, Honma S, Fukami H, Yoshida A, Ottersen OP, Shigenaga Y (2002) Quantitative ultrastructural analysis of glycine- and gamma-aminobutyric acid-immunoreactive terminals on trigeminal alpha- and gamma-motoneuron somata in the rat. J Comp Neurol 442:308–319CrossRefGoogle Scholar
- Barret KE, Barman SM, Boitano S, Brooks H (2009) Excitable tissue: nerve. In: Barret KE, Barman SM, Boitano S, Brooks H (eds) Ganong’s review of medical physiology, 23rd edn. McGraw-Hill Medical, New York, pp 79–92Google Scholar
- Berkowitz A (2012) Motor Output from the Brain and Spinal Cord. In: eLS. https://doi.org/10.1002/9780470015902.a0000189.pub3
- Brull SJ (2014) Physiology of neuromuscular transmission. In: Murray MJ, Harrison BA, Mueller JT, Rose SH, Wass CT, Wedel DJ (eds) Faust’s anesthesiology review, 4th edn. Elsevier Saunders, Philadelphia, pp 98–99Google Scholar
- Conradi S (1969) Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult cat. Acta Physiol Scand Suppl 332:5–48Google Scholar
- Hall WC (2004) Lower motor neuron circuits and motor control. In: Purves D, Augustine GJ, Fitzpatrick D, Hall WC, LaMantia A-S, McNamara JO, Williams SM (eds) Neuroscience, 3rd edn. Sinauer Associates, Sunderland, pp 371–392Google Scholar
- Krol RC, Knuth SL, Bartlett D Jr (1984) Selective reduction of genioglossal muscle activity by alcohol in normal human subjects. Am Rev Respir Dis 129:247–250Google Scholar
- O’Reilly PM, FitzGerald MJ (1990) Fibre composition of the hypoglossal nerve in the rat. J Anat 172:227–243Google Scholar
- Ornung G, Shupliakov O, Linda H, Ottersen OP, Storm-Mathisen J, Ulfhake B, Cullheim S (1996) Qualitative and quantitative analysis of glycine- and GABA-immunoreactive nerve terminals on motoneuron cell bodies in the cat spinal cord: a postembedding electron microscopic study. J Comp Neurol 365:413–426CrossRefGoogle Scholar
- Ottersen OP, Storm-Mathisen J, Madsen S, Skumlien S, Stromhaug J (1986) Evaluation of the immunocytochemical method for amino acids. Med Biol 64:147–158Google Scholar
- Paik SK, Bae JY, Park SE, Moritani M, Yoshida A, Yeo EJ, Choi KS, Ahn DK, Moon C, Shigenaga Y, Bae YC (2007) Developmental changes in distribution of gamma-aminobutyric acid- and glycine-immunoreactive boutons on rat trigeminal motoneurons. I. Jaw-closing motoneurons. J Comp Neurol 503:779–789CrossRefGoogle Scholar
- Paik SK, Kwak MK, Bae JY, Yi HW, Yoshida A, Ahn DK, Bae YC (2012b) gamma-Aminobutyric acid-, glycine-, and glutamate-immunopositive boutons on mesencephalic trigeminal neurons that innervate jaw-closing muscle spindles in the rat: ultrastructure and development. J Comp Neurol 520:3414–3427CrossRefGoogle Scholar
- Peters A, Palay SL, Webster Hd (1991) The fine structure of the nervous system: neurons and their supporting cells, 3rd edn. Oxford University Press, New YorkGoogle Scholar
- Remmers JE, deGroot WJ, Sauerland EK, Anch AM (1978) Pathogenesis of upper airway occlusion during sleep. J Appl Physiol Respir Environ Exerc Physiol 44:931–938Google Scholar
- Shepherd GM, Koch C (1990) Appendix: Dendritic electrotonus and synaptic integration. In: Shepherd GM (ed) The synaptic organization of the brain, 3rd edn. Oxford University Press, New York, pp 439–473Google Scholar