The mossy fiber bouton: the "common" or the "unique" synapse? - PubMed (original) (raw)
The mossy fiber bouton: the "common" or the "unique" synapse?
Astrid Rollenhagen et al. Front Synaptic Neurosci. 2010.
Abstract
Synapses are the key elements for signal processing and plasticity in the brain. They are composed of nearly the same structural subelements, an apposition zone including a pre- and postsynaptic density, a cleft and a pool of vesicles. It is, however, their actual composition that determines their different behavior in synaptic transmission and plasticity. Here, we describe and discuss the structural factors underlying the unique functional properties of the hippocampal mossy fiber (MF) synapse. Two membrane specializations, active zones (AZs; transmitter release sites), and puncta adherentia (PA), putative adhesion complexes were found. On average, individual boutons had ∼20 AZs with a mean surface area of 0.1 μm(2) and a short distance of 0.45 μm between individual AZs. Mossy fiber boutons (MFBs) and their target structures were isolated from each other by astrocytes, but fine glial processes never reached the AZs. Therefore, two structural factors are likely to promote synaptic cross-talk: the short distance and the absence of fine glial processes between individual AZs. Thus, synaptic crosstalk may contribute to the high efficacy of hippocampal MF synapses. On average, an adult bouton contained ∼16,000 synaptic vesicles; ∼600 vesicles were located within 60 nm from the AZ, ∼4000 between 60 nm and 200 nm, and the remaining beyond 200 nm, suggesting large readily releasable, recycling, and reserve pools. Thus, the size of the three pools together with the number and distribution of AZs underlie the unique extent of synaptic efficacy and plasticity of the hippocampal MF synapse.
Keywords: 3D-reconstructions; actives zones; different pools of synaptic vesicles; electron microscopy; mossy fiber-CA3 pyramidal cell synapse; quantitative analysis; synaptic crosstalk; synaptic transmission and plasticity.
Figures
Figure 1
The hippocampal mossy fiber bouton. (A) Low power electron microscopic image of two adjacent MFBs (MFB1, MFB2) taken from an adult rat. Both MFBs outlined in yellow terminate on different dendritic segments, but preferentially on spiny excrescences (blue contours). AZs are given in red and astrocytic profiles (dark diaminobenzidine reaction product) in green. Scale bar: 2.5 μm. (B) Glial coverage of an individual MFB showing the distribution of astrocytic processes (highlighted in green) as revealed by glutamine synthetase pre-embedding immunohistochemistry. The surface of an individual MFB (in light yellow), its postsynaptic spiny excrescences (ex; in light blue) was surrounded by several astrocytic processes (in green). Note, that the fine glial processes do not reach the AZs (in red) and the synaptic cleft. The mitochondria (mi) within the MFB are highlighted in white. Scale bar: 1 μm.
Figure 2
Three-dimensional reconstructions of an adult MFB and its postsynaptic target dendrite. (A) Volume reconstructions of an en passant MFB (depicted in yellow) and its postsynaptic target dendrite (blue). Note, that the spiny excrescences were almost entirely covered by the nerve terminal. (B) Distribution of the two membrane specializations, AZs (in red) and PAs (in orange) on the postsynaptic target dendrite (blue). Note, that AZs were mainly located on the spiny excrescences, whereas PAs were exclusively found at the dendritic shaft. (C) Organization of the pool of synaptic vesicles (green dots) at an individual MFB. Here, the pool was distributed throughout the entire nerve terminal. Mitochondria (in white) formed either cluster-like arrangements or bands associated with the pool of synaptic vesicles (green dots).
Figure 3
Number, shape and location of AZs. Two representative examples of AZs (red areas) found on simple (A1) and complex (A2) spiny excrescences (blue) taken from an adult rat. Simple spines had only a single or at most two AZs whereas complex spines had up to eight AZs. Note, also the different shape and size of individual AZs that formed ring- or patch-like arrangements. Scale bar: 1 μm. (B) Histogram showing the distribution of surface areas of AZs for adult MFBs. (C) Histogram of the distribution of nearest-neighbor distances between centers of gravity of all AZs for adult MFBs (modified from Rollenhagen et al., 2007a).
Figure 4
Organization of the pool of synaptic vesicles. (A, B) Two representative examples with a large ((A) 17,138 vesicles) and smaller ((B) 7559 vesicles) total pool of synaptic vesicles (green dots) are given. (C) The graph shows the correlation for the mean number of synaptic vesicles as a function of distance from an AZ (averaged over all AZs) for P28 MFBs (light blue line), adult MFBs (dark blue line), the calyx of Held (green line) and layer 5 input synapses (red line). The light yellow boxes indicate the borders between the RRP, the RP and the reserve pool of synaptic vesicles. Note, that the slope of the curves is markedly higher in the MFBs and layer 5 input synapses when compared with the calyx of Held synapse, even though the spacing between individual AZs is comparable at these synapses.
Similar articles
- Structural determinants of transmission at large hippocampal mossy fiber synapses.
Rollenhagen A, Sätzler K, Rodríguez EP, Jonas P, Frotscher M, Lübke JH. Rollenhagen A, et al. J Neurosci. 2007 Sep 26;27(39):10434-44. doi: 10.1523/JNEUROSCI.1946-07.2007. J Neurosci. 2007. PMID: 17898215 Free PMC article. - Structural determinants underlying the high efficacy of synaptic transmission and plasticity at synaptic boutons in layer 4 of the adult rat 'barrel cortex'.
Rollenhagen A, Klook K, Sätzler K, Qi G, Anstötz M, Feldmeyer D, Lübke JH. Rollenhagen A, et al. Brain Struct Funct. 2015 Nov;220(6):3185-209. doi: 10.1007/s00429-014-0850-5. Epub 2014 Aug 2. Brain Struct Funct. 2015. PMID: 25084745 - Ultrastructural analysis of wild-type and RIM1α knockout active zones in a large cortical synapse.
Lichter K, Paul MM, Pauli M, Schoch S, Kollmannsberger P, Stigloher C, Heckmann M, Sirén AL. Lichter K, et al. Cell Rep. 2022 Sep 20;40(12):111382. doi: 10.1016/j.celrep.2022.111382. Cell Rep. 2022. PMID: 36130490 - Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network.
Bischofberger J, Engel D, Frotscher M, Jonas P. Bischofberger J, et al. Pflugers Arch. 2006 Dec;453(3):361-72. doi: 10.1007/s00424-006-0093-2. Epub 2006 Jun 27. Pflugers Arch. 2006. PMID: 16802161 Review. - The morphology of excitatory central synapses: from structure to function.
Rollenhagen A, Lübke JH. Rollenhagen A, et al. Cell Tissue Res. 2006 Nov;326(2):221-37. doi: 10.1007/s00441-006-0288-z. Epub 2006 Aug 24. Cell Tissue Res. 2006. PMID: 16932936 Review.
Cited by
- Non-canonical function of ADAM10 in presynaptic plasticity.
Bär J, Fanutza T, Reimann CC, Seipold L, Grohe M, Bolter JR, Delfs F, Bucher M, Gee CE, Schweizer M, Saftig P, Mikhaylova M. Bär J, et al. Cell Mol Life Sci. 2024 Aug 9;81(1):342. doi: 10.1007/s00018-024-05327-8. Cell Mol Life Sci. 2024. PMID: 39123091 Free PMC article. - Inhibitory neurons marked by a connectivity molecule regulate memory precision.
Tuñon-Ortiz A, Tränkner D, Brockway SN, Raines O, Mahnke A, Grega M, Zelikowsky M, Williams ME. Tuñon-Ortiz A, et al. bioRxiv [Preprint]. 2024 Aug 14:2024.07.05.602304. doi: 10.1101/2024.07.05.602304. bioRxiv. 2024. PMID: 39005261 Free PMC article. Preprint. - Regulation of hippocampal mossy fiber-CA3 synapse function by a Bcl11b/C1ql2/Nrxn3(25b+) pathway.
Koumoundourou A, Rannap M, De Bruyckere E, Nestel S, Reissner C, Egorov AV, Liu P, Missler M, Heimrich B, Draguhn A, Britsch S. Koumoundourou A, et al. Elife. 2024 Feb 15;12:RP89854. doi: 10.7554/eLife.89854. Elife. 2024. PMID: 38358390 Free PMC article. - Senktide blocks aberrant RTN3 interactome to retard memory decline and tau pathology in social isolated Alzheimer's disease mice.
Huang HZ, Ai WQ, Wei N, Zhu LS, Liu ZQ, Zhou CW, Deng MF, Zhang WT, Zhang JC, Yang CQ, Hu YZ, Han ZT, Zhang HH, Jia JJ, Wang J, Liu FF, Li K, Xu Q, Yuan M, Man H, Guo Z, Lu Y, Shu K, Zhu LQ, Liu D. Huang HZ, et al. Protein Cell. 2024 Apr 1;15(4):261-284. doi: 10.1093/procel/pwad056. Protein Cell. 2024. PMID: 38011644 Free PMC article. - An inhibitory circuit-based enhancer of DYRK1A function reverses Dyrk1a-associated impairment in social recognition.
Shih YT, Alipio JB, Sahay A. Shih YT, et al. Neuron. 2023 Oct 4;111(19):3084-3101.e5. doi: 10.1016/j.neuron.2023.09.009. Neuron. 2023. PMID: 37797581 Free PMC article.
References
LinkOut - more resources
Full Text Sources
Miscellaneous