7
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Cortical Presynaptic Boutons Progressively Engulf Spinules as They Mature

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Despite decades of discussion in the neuroanatomical literature, the role of the synaptic “spinule” in synaptic development and function remains elusive. Canonically, spinules are finger-like projections that emerge from postsynaptic spines and can become enveloped by presynaptic boutons. When a presynaptic bouton encapsulates a spinule in this manner, the membrane apposition between the spinule and surrounding bouton can be significantly larger than the membrane interface at the synaptic active zone. Hence, spinules may represent a mechanism for extrasynaptic neuronal communication and/or may function as structural “anchors” that increase the stability of cortical synapses. Yet despite their potential to impact synaptic function, we have little information on the percentages of developing and adult cortical bouton populations that contain spinules, the percentages of these cortical spinule-bearing boutons (SBBs) that contain spinules from distinct neuronal/glial origins, or whether the onset of activity or cortical plasticity are correlated with increased prevalence of cortical SBBs. Here, we employed 2D and 3D electron microscopy to determine the prevalence of spinules in excitatory presynaptic boutons at key developmental time points in the primary visual cortex (V1) of female and male ferrets. We find that the prevalence of SBBs in V1 increases across postnatal development, such that ∼25% of excitatory boutons in late adolescent ferret V1 contain spinules. In addition, we find that a majority of spinules within SBBs at later developmental time points emerge from postsynaptic spines and adjacent boutons/axons, suggesting that synaptic spinules may enhance synaptic stability and allow for axo-axonal communication in mature sensory cortex.

          Related collections

          Most cited references65

          • Record: found
          • Abstract: found
          • Article: not found

          Fiji: an open-source platform for biological-image analysis.

          Fiji is a distribution of the popular open-source software ImageJ focused on biological-image analysis. Fiji uses modern software engineering practices to combine powerful software libraries with a broad range of scripting languages to enable rapid prototyping of image-processing algorithms. Fiji facilitates the transformation of new algorithms into ImageJ plugins that can be shared with end users through an integrated update system. We propose Fiji as a platform for productive collaboration between computer science and biology research communities.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Optogenetic stimulation of a hippocampal engram activates fear memory recall

            A specific memory is thought to be encoded by a sparse population of neurons 1,2 . These neurons can be tagged during learning for subsequent identification 3 and manipulation 4,5,6 . Moreover, their ablation or inactivation results in reduced memory expression, suggesting their necessity in mnemonic processes. However, a critical question of sufficiency remains: can one elicit the behavioral output of a specific memory by directly activating a population of neurons that was active during learning? Here we show that optogenetic reactivation of hippocampal neurons activated during fear conditioning is sufficient to induce freezing behavior. We labeled a population of hippocampal dentate gyrus neurons activated during fear learning with channelrhodopsin-2 (ChR2) 7,8 and later optically reactivated these neurons in a different context. The mice showed increased freezing only upon light stimulation, indicating light-induced fear memory recall. This freezing was not detected in non-fear conditioned mice expressing ChR2 in a similar proportion of cells, nor in fear conditioned mice with cells labeled by EYFP instead of ChR2. Finally, activation of cells labeled in a context not associated with fear did not evoke freezing in mice that were previously fear conditioned in a different context, suggesting that light-induced fear memory recall is context-specific. Together, our findings indicate that activating a sparse but specific ensemble of hippocampal neurons that contribute to a memory engram is sufficient for the recall of that memory. Moreover, our experimental approach offers a general method of mapping cellular populations bearing memory engrams.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Release probability of hippocampal glutamatergic terminals scales with the size of the active zone

              Cortical synapses display remarkable structural, molecular and functional heterogeneity. Our knowledge regarding the relationship between the ultrastructural and functional parameters is still fragmented. Here we asked how the release probability and presynaptic [Ca2+] transients relate to the ultrastructure of rat hippocampal glutamatergic axon terminals. Two-photon Ca2+ imaging-derived optical quantal analysis and correlated electron microscopic reconstructions revealed a tight correlation between the release probability and the active zone area. The peak amplitude of [Ca2+] transients in single boutons also positively correlated with the active zone area. Freeze-fracture immunogold labeling revealed that the voltage-gated Ca2+ channel subunit Cav2.1 and the presynaptic protein Rim1/2 are confined to the active zone and their numbers scale linearly with the active zone area. Gold particles for Cav2.1 showed a nonrandom distribution within the active zones. Our results demonstrate that the number of several active zone proteins, including presynaptic Ca2+ channels, docked vesicles and the release probability scales linearly with the active zone area.
                Bookmark

                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                18 September 2020
                14 October 2020
                Sep-Oct 2020
                : 7
                : 5
                : ENEURO.0426-19.2020
                Affiliations
                [1 ]Division of Sciences and Mathematics, University of Washington | Tacoma , Tacoma, WA 98402
                [2 ]Department of Psychology, University of Virginia , Charlottesville, VA 22904
                Author notes

                The authors declare no competing financial interests.

                Author contributions: M.N. designed research; C.C., S.L., A.K., and M.N. performed research; A.E. contributed unpublished reagents/analytic tools; C.C., S.L., A.K., and M.N. analyzed data; A.E. and M.N. wrote the paper.

                This work was supported by the University of Washington Bridge Fund, the University of Washington – Tacoma Internal Pilot Royalty Research Fund, and the University of Washington – Tacoma Scholarship and Teaching Fund.

                Correspondence should be addressed to Marc Nahmani at mnahmani@ 123456uw.edu .
                Article
                eN-NWR-0426-19
                10.1523/ENEURO.0426-19.2020
                7568603
                32958478
                208855fb-89a0-4e71-93ed-fb3a4cf1806d
                Copyright © 2020 Campbell et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 14 October 2019
                : 20 August 2020
                : 8 September 2020
                Page count
                Figures: 8, Tables: 3, Equations: 1, References: 66, Pages: 16, Words: 00
                Funding
                Funded by: University of Washingon Bridge Fund
                Funded by: University of Washington - Tacoma Scholarship and Teaching Fund
                Funded by: University of Washington - Tacoma Internal Pilot Royalty Research Fund
                Categories
                2
                Research Article: New Research
                Development
                Custom metadata
                September/October 2020

                critical period,developmental plasticity,electron microscopy,focused ion beam scanning electron microscopy,presynaptic terminal,synaptic plasticity

                Comments

                Comment on this article