Characterization of Multiple Synaptic Boutons in Cerebral Motor Cortex in Physiological and Pathological Condition: Acrobatic Motor Training Model and Traumatic Brain Injury Model

Hyun-Wook Kim; Ji eun Na; ImJoo Rhyu

doi:10.9729/AM.2018.48.4.102

https://doi.org/10.9729/AM.2018.48.4.102

Characterization of Multiple Synaptic Boutons in Cerebral Motor Cortex in Physiological and Pathological Condition: Acrobatic Motor Training Model and Traumatic Brain Injury Model

Applied Microscopy 2018;48:102-9

Published online December 28, 2018

Hyun-Wook Kim¹, Ji eun Na¹, and ImJoo Rhyu^1,2,*

¹Department of Anatomy, Korea University College of Medicine, Seoul 02841, Korea, ²Division of Brain Korea 21 Plus Program for Biomedical Science, Korea University College of Medicine, Seoul 02841, Korea

Correspondence to: Rhyu IJ, http://orcid.org/0000-0002-5558-6278, Tel: +82-2-2286-1149, Fax: +82-2-929-5696, E-mail: irhyu@korea.ac.kr

Received December 19, 2018; Revised December 23, 2018; Accepted December 23, 2018.

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract: Multiple synaptic boutons (MSBs) have been reported to be synapse with two or more postsynaptic terminals in one presynaptic terminal. These MSBs are known to be increased by various brain stimuli. In the motor cortex, increased number of MSB was observed in both acrobat training (AC) model and traumatic brain injury (TBI) model. Interestingly one is a physiological stimuli and the other is pathological insult. The purpose of this study is to compare the connectivity of MSBs between AC model and TBI model in the cerebral motor cortex, based on the hypothesis that the connectivity of MSBs might be different according to the models. The motor cortex was dissected from perfused brain of each experimental animal, the samples were prepared for routine transmission electron microscopy. The 60~70 serial sections were mounted on the one-hole grid and MSB was analyzed. The 3-dimensional analysis revealed that 94% of MSBs found in AC model synapse two postsynaptic spines from same dendrite. But, 28% MSBs from TBI models synapse two postsynaptic spines from different dendrite. This imply that the MSBs observed in motor cortex of AC model and TBI model might have different circuits for the processing the information.; Keywords : Multiple synaptic boutons (MSBs), Synaptic plasticity, Acrobat training (AC), Traumatic brain injury (TBI)

References

Dunnett, SB (1995). Functional repair of striatal systems by neural transplants: evidence for circuit reconstruction. Behav Brain Res. 66, 133-142.
Federmeier, KD, Kleim, JA, and Greenough, WT (2002). Learning-induced multiple synapse formation in rat cerebellar cortex. Neurosci Lett. 332, 180-184.
Fujii, R, Ichikawa, M, and Ozaki, M (2008). Imaging of molecular dynamics regulated by electrical activities in neural circuits and in synapses. Neurosignals. 16, 260-277.
Greenough, WT, Larson, JR, and Withers, GS (1985). Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. Behav Neural Biol. 44, 301-314.
Gundersen, HJ, Bagger, P, Bendtsen, TF, Evans, SM, Korbo, L, Marcussen, N, Moller, A, Nielsen, K, Nyengaard, JR, and Pakkenberg, B (1988). The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS. 96, 857-881.
Jones, TA (1999). Multiple synapse formation in the motor cortex opposite unilateral sensorimotor cortex lesions in adult rats. J Comp Neurol. 414, 57-66.
Jones, TA, Chu, CJ, Grande, LA, and Gregory, AD (1999). Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J Neurosci. 19, 10153-10163.
Jones, TA, Kleim, JA, and Greenough, WT (1996). Synaptogenesis and dendritic growth in the cortex opposite unilateral sensorimotor cortex damage in adult rats: a quantitative electron microscopic examination. Brain Res. 733, 142-148.
Kim, HW, Oh, S, Lee, SH, Lee, S, Na, JE, Lee, KJ, and Rhyu, IJ (2018). Different types of multiple-synapse boutons in the cerebellar cortex between physically enriched and ataxic mutant mice. Microscopy research and technique.
Kleim, JA, Barbay, S, Cooper, NR, Hogg, TM, Reidel, CN, Remple, MS, and Nudo, RJ (2002). Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol Learn Mem. 77, 63-77.
Kleim, JA, Barbay, S, and Nudo, RJ (1998). Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol. 80, 3321-3325.
Lee, KJ, Jung, JG, Arii, T, Imoto, K, and Rhyu, IJ (2007). Morphological changes in dendritic spines of Purkinje cells associated with motor learning. Neurobiol Learn Mem. 88, 445-450.
Lee, KJ, Park, IS, Kim, H, Greenough, WT, Pak, DT, and Rhyu, IJ (2013). Motor skill training induces coordinated strengthening and weakening between neighboring synapses. J Neurosci. 33, 9794-9799.
Medvedev, NI, Dallerac, G, Popov, VI, Rodriguez Arellano, JJ, Davies, HA, Kraev, IV, Doyere, V, and Stewart, MG (2012). Multiple spine boutons are formed after long-lasting LTP in the awake rat. Brain Struct Funct.
Neves, G, Cooke, SF, and Bliss, TV (2008). Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci. 9, 65-75.
Seung, HS (2011). Neuroscience: Towards functional connectomics. Nature. 471, 170-172.
Telgkamp, P, Padgett, DE, Ledoux, VA, Woolley, CS, and Raman, IM (2004). Maintenance of high-frequency transmission at purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron. 41, 113-126.
Toni, N, Buchs, PA, Nikonenko, I, Bron, CR, and Muller, D (1999). LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature. 402, 421-425.
Wanaverbecq, N, Bodor, AL, Bokor, H, Slezia, A, Luthi, A, and Acsady, L (2008). Contrasting the functional properties of GABAergic axon terminals with single and multiple synapses in the thalamus. J Neurosci. 28, 11848-11861.