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The Journal of Neuroscience, March 19, 2008, 28(12):3090-3102; doi:10.1523/JNEUROSCI.5266-07.2008
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Cellular/Molecular
Structural Correlates of Efficient GABAergic Transmission in the Basal Ganglia–Thalamus Pathway
Ágnes L. Bodor,1 Kristóf Giber,1 Zita Rovó,1 István Ulbert,2,3 andLászló Acsády1 1Department of Cellular and Network Neurobiology, Institute of Experimental Medicine, Hungarian Academy of Sciences, H-1450 Budapest, Hungary, 2Institute of Psychology, Hungarian Academy of Sciences, 1068 Budapest, Hungary, and 3Department of Information Technology, Péter Pázmány Catholic University, H-1083 Budapest, Hungary
Correspondence should be addressed to Dr. László Acsády, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u. 43, H-1083, Budapest, Hungary. Email: acsady{at}koki.hu
Giant inhibitory terminals with multiple synapses, the counterparts of excitatory "detonator" or "driver" terminals, have not been described in the forebrain. Using three-dimensional reconstructions of electron microscopic images, we quantitatively characterize a GABAergic pathway that establishes synaptic contacts exclusively via multiple synapses. Axon terminals of the nigrothalamic pathway formed, on average, 8.5 synapses on large-diameter dendrites and somata of relay cells in the ventromedial nucleus of the rat thalamus. All synapses of a given terminal converged on a single postsynaptic element. The vast majority of the synapses established by a single terminal were not separated by astrocytic processes. Nigrothalamic terminals in the macaque monkey showed the same ultrastructural features both in qualitative and quantitative terms (the median number of synapse per target was also 8.5). The individual synapses were closely spaced in both species. The nearest-neighbor synaptic distances were 169 nm in the rat and 178 nm in the monkey. The average number of synapses within 0.75 µm from any given synapse was 3.8 in the rat and 3.5 in the monkey. The arrangement of synapses described in this study creates favorable conditions for intersynaptic spillover of GABA among the multiple synapses of a single bouton, which can result in larger charge transfer. This could explain faithful and efficient GABAergic signal transmission in the nigrothalamic pathway in the healthy condition and during Parkinson's disease. In addition, our structural data suggest that the rodent nigrothalamic pathway can be a valid model of the primate condition, when the mechanism of GABAergic transmission is studied.
Key words: spillover; driver; axon terminal; active zone; substantia nigra; Parkinson's disease
Received Aug. 29, 2007; revised Feb. 2, 2008; accepted Feb. 4, 2008.
Correspondence should be addressed to Dr. László Acsády, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u. 43, H-1083, Budapest, Hungary. Email: acsady{at}koki.hu
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