Sublamina-Specific Dynamics and Ultrastructural Heterogeneity of Layer 6 Excitatory Synaptic Boutons in the Adult Human Temporal Lobe Neocortex

Overview

Journal Cereb Cortex

Publisher Oxford University Press

Specialty Neurology

Date 2021 Sep 16

PMID 34530440

Citations 8

Authors

Sandra Schmuhl-Giesen

Astrid Rollenhagen

Bernd Walkenfort

Rachida Yakoubi

Kurt Satzler

Dorothea Miller

Marec von Lehe

Mike Hasenberg

Joachim H R Lubke

Affiliations

Soon will be listed here.

Abstract

Synapses "govern" the computational properties of any given network in the brain. However, their detailed quantitative morphology is still rather unknown, particularly in humans. Quantitative 3D-models of synaptic boutons (SBs) in layer (L)6a and L6b of the temporal lobe neocortex (TLN) were generated from biopsy samples after epilepsy surgery using fine-scale transmission electron microscopy, 3D-volume reconstructions and electron microscopic tomography. Beside the overall geometry of SBs, the size of active zones (AZs) and that of the three pools of synaptic vesicles (SVs) were quantified. SBs in L6 of the TLN were middle-sized (~5 μm2), the majority contained only a single but comparatively large AZ (~0.20 μm2). SBs had a total pool of ~1100 SVs with comparatively large readily releasable (RRP, ~10 SVs L6a), (RRP, ~15 SVs L6b), recycling (RP, ~150 SVs), and resting (~900 SVs) pools. All pools showed a remarkably large variability suggesting a strong modulation of short-term synaptic plasticity. In conclusion, L6 SBs are highly reliable in synaptic transmission within the L6 network in the TLN and may act as "amplifiers," "integrators" but also as "discriminators" for columnar specific, long-range extracortical and cortico-thalamic signals from the sensory periphery.

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References

Ghijsen W, Leenders A . Differential signaling in presynaptic neurotransmitter release. Cell Mol Life Sci. 2005; 62(9):937-54. DOI: 10.1007/s00018-004-4525-0. View

Umeda T, Ebihara T, Okabe S . Simultaneous observation of stably associated presynaptic varicosities and postsynaptic spines: morphological alterations of CA3-CA1 synapses in hippocampal slice cultures. Mol Cell Neurosci. 2005; 28(2):264-74. DOI: 10.1016/j.mcn.2004.09.010. View

Testa-Silva G, Verhoog M, Linaro D, de Kock C, Baayen J, Meredith R . High bandwidth synaptic communication and frequency tracking in human neocortex. PLoS Biol. 2014; 12(11):e1002007. PMC: 4244038. DOI: 10.1371/journal.pbio.1002007. View

Andjelic S, Gallopin T, Cauli B, Hill E, Roux L, Badr S . Glutamatergic nonpyramidal neurons from neocortical layer VI and their comparison with pyramidal and spiny stellate neurons. J Neurophysiol. 2008; 101(2):641-54. PMC: 2657076. DOI: 10.1152/jn.91094.2008. View

Schneggenburger R, Sakaba T, Neher E . Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci. 2002; 25(4):206-12. DOI: 10.1016/s0166-2236(02)02139-2. View

Thomson A . Neocortical layer 6, a review. Front Neuroanat. 2010; 4:13. PMC: 2885865. DOI: 10.3389/fnana.2010.00013. View

Courchesne E, Hillyard S, GALAMBOS R . Stimulus novelty, task relevance and the visual evoked potential in man. Electroencephalogr Clin Neurophysiol. 1975; 39(2):131-43. DOI: 10.1016/0013-4694(75)90003-6. View

Sherman S . Thalamocortical interactions. Curr Opin Neurobiol. 2012; 22(4):575-9. PMC: 3398163. DOI: 10.1016/j.conb.2012.03.005. View

Zhao S, Studer D, Chai X, Graber W, Brose N, Nestel S . Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing. J Comp Neurol. 2012; 520(11):2340-51. DOI: 10.1002/cne.23040. View

10.

Denker A, Rizzoli S . Synaptic vesicle pools: an update. Front Synaptic Neurosci. 2011; 2:135. PMC: 3059705. DOI: 10.3389/fnsyn.2010.00135. View

11.

Holderith N, Lorincz A, Katona G, Rozsa B, Kulik A, Watanabe M . Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat Neurosci. 2012; 15(7):988-97. PMC: 3386897. DOI: 10.1038/nn.3137. View

12.

Boyer C, Schikorski T, Stevens C . Comparison of hippocampal dendritic spines in culture and in brain. J Neurosci. 1998; 18(14):5294-300. PMC: 6793498. View

13.

Nava N, Chen F, Wegener G, Popoli M, Nyengaard J . A new efficient method for synaptic vesicle quantification reveals differences between medial prefrontal cortex perforated and nonperforated synapses. J Comp Neurol. 2013; 522(2):284-97. DOI: 10.1002/cne.23482. View

14.

Tamada H, Blanc J, Korogod N, Petersen C, Knott G . Ultrastructural comparison of dendritic spine morphology preserved with cryo and chemical fixation. Elife. 2020; 9. PMC: 7748412. DOI: 10.7554/eLife.56384. View

15.

DeFelipe J, Marco P, Busturia I, Merchan-Perez A . Estimation of the number of synapses in the cerebral cortex: methodological considerations. Cereb Cortex. 1999; 9(7):722-32. DOI: 10.1093/cercor/9.7.722. View

16.

Constantinople C, Bruno R . Deep cortical layers are activated directly by thalamus. Science. 2013; 340(6140):1591-4. PMC: 4203320. DOI: 10.1126/science.1236425. View

17.

Spirou G, Rowland K, Berrebi A . Ultrastructure of neurons and large synaptic terminals in the lateral nucleus of the trapezoid body of the cat. J Comp Neurol. 1998; 398(2):257-72. DOI: 10.1002/(sici)1096-9861(19980824)398:2<257::aid-cne7>3.0.co;2-#. View

18.

Matz J, Gilyan A, Kolar A, McCarvill T, Krueger S . Rapid structural alterations of the active zone lead to sustained changes in neurotransmitter release. Proc Natl Acad Sci U S A. 2010; 107(19):8836-41. PMC: 2889309. DOI: 10.1073/pnas.0906087107. View

19.

Fiala J, Harris K . Extending unbiased stereology of brain ultrastructure to three-dimensional volumes. J Am Med Inform Assoc. 2001; 8(1):1-16. PMC: 134588. DOI: 10.1136/jamia.2001.0080001. View

20.

Zhang Z, Deschenes M . Projections to layer VI of the posteromedial barrel field in the rat: a reappraisal of the role of corticothalamic pathways. Cereb Cortex. 1998; 8(5):428-36. DOI: 10.1093/cercor/8.5.428. View