Local translation in presynaptic terminals

Proteins carry out most of the functions in cells, including neurons, which are one of the most morphologically complex cell types in the body. This poses challenges for how proteins can be supplied to remote regions where connections (synapses) are made with other neurons. One solution to the neuron protein-supply problem involves the local synthesis of proteins from messenger RNA (mRNA) molecules located at or near synapses. Hafner et al. used RNA sequencing methods and superresolution microscopy to show that axon terminals contain hundreds of mRNA molecules as well as the machinery needed for protein synthesis. Furthermore, the axon terminals were able to use these components to make proteins that participate in synaptic transmission.
Science, this issue p. eaau3644

Structured Abstract


The regulation of synaptic proteins by posttranslational modifications and by ongoing protein synthesis and degradation drives homeostasis and plasticity at synapses. A key question is where synaptic proteins are made. Most of the neuron’s volume comprises axons and dendrites that can be micrometers or millimeters long. Thus, a substantial fraction of proteomic remodeling could potentially occur locally within both axons and dendrites. Whereas there is wealth of data indicating that protein synthesis occurs in mature dendrites, there has been much less evidence in support of local translation in mature axons.


Efforts to localize molecules or cell biological events to neuronal pre- or postsynaptic compartments by using fluorescence microscopy are limited by the tight association of the axonal bouton and the dendritic spine; the synaptic cleft, the only clear region of separation, is only ~20 nm wide. In this study, to increase the resolving power to visualize RNA molecules in pre- and postsynaptic compartments, we optimized fluorescence in situ hybridization (FISH) and nascent protein detection methods for use with expansion microscopy. To characterize transcripts and translational machinery in excitatory presynaptic terminals, we used a recently developed platform that couples fluorescence sorting with biochemical fractionation to sort and purify fluorescently labeled synaptosomes. To obtain direct evidence for protein synthesis in synaptic compartments, particularly presynaptic boutons, we adapted the puromycin-based metabolic labeling strategy for detection with electron or expansion microscopy. We also examined the translational signature of these three different forms of local protein synthesis–dependent plasticity in three different synaptic compartments: dendritic spines, excitatory terminals, and inhibitory terminals.


In adult rodent brain slices and cultured neurons, we found that >75% of both excitatory and inhibitory presynaptic terminals contain the machinery for protein synthesis: rRNA, ribosomes, and polyadenylated [poly (A)+] mRNA. Using mature mouse forebrain synaptosomes that are enriched for vGLUT1+ presynaptic terminals, we identified ~450 transcripts that were enriched (relative to the generic synaptosome transcriptome). These included many mRNAs that code for proteins that regulate neurotransmitter release. Both light microscopy (confocal and super-resolution) and electron microscopy revealed that in the absence of overt stimulation, there was a notably high level of ongoing protein synthesis in both pre- and postsynaptic compartments. After just 5 min of metabolic labeling, ~40% of both excitatory and inhibitory presynaptic terminals and ~60% of dendritic spines exhibited active translation. Three different forms of synaptic plasticity resulted in distinct patterns of protein synthesis stimulation in dendritic spines and in excitatory and inhibitory presynaptic axon terminals.


In this study, we investigated the localization and stimulation of protein synthesis in mature synapses. We unambiguously identified protein synthesis machinery and mRNA translation in individual synaptic compartments. Both excitatory and inhibitory presynaptic boutons (as well as postsynaptic spines) carry out protein synthesis regularly, in the absence of any exogenous stimulation. Synthesis within these three compartments is differentially recruited to modify local proteomes during synaptic plasticity. Local protein synthesis adds spatial and temporal precision for proteome remodeling that can be exploited to rapidly modify synapses in specific subcellular compartments.
Plasticity differentially recruits local protein synthesis.
Summary scheme indicating how protein synthesis occurs in both post- and presynaptic compartments and how each different form of plasticity examined has a specific translational signature. The three compartments represented, excitatory and inhibitory presynaptic boutons and postsynaptic spines, exhibit different patterns of enhanced protein synthesis (arrows) after the treatments with (S)-3,5-dihydroxyphenylglycine hydrate [metabotropic glutamate receptor long-term depression (mGluR LTD)], brain-derived neurotrophic factor (BDNF) (BDNF potentiation), or arachidonyl-2-chloroethylamide (endocannabinoid receptor activation).


There is ample evidence for localization of messenger RNAs (mRNAs) and protein synthesis in neuronal dendrites; however, demonstrations of these processes in presynaptic terminals are limited. We used expansion microscopy to resolve pre- and postsynaptic compartments in rodent neurons. Most presynaptic terminals in the hippocampus and forebrain contained mRNA and ribosomes. We sorted fluorescently labeled mouse brain synaptosomes and then sequenced hundreds of mRNA species present within excitatory boutons. After brief metabolic labeling, >30% of all presynaptic terminals exhibited a signal, providing evidence for ongoing protein synthesis. We tested different classic plasticity paradigms and observed distinct patterns of rapid pre- and/or postsynaptic translation. Thus, presynaptic terminals are translationally competent, and local protein synthesis is differentially recruited to drive compartment-specific phenotypes that underlie different forms of plasticity.

Get full access to this article

View all available purchase options and get full access to this article.

Supplementary Material


Figs. S1 to 13
Tables S1 and S2
Movie S1


File (aau3644-hafner-sm.pdf)
File (aau3644_tables1.xls)
File (aau3644_tables2.xlsx)
File (
Correction (13 February 2020): The NCBI accession number for the raw data has been added to the Acknowledgments.

References and Notes

N. J. Bannister, A. U. Larkman, Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: II. Spine distributions. J. Comp. Neurol. 360, 161–171 (1995).
A. R. Dörrbaum, L. Kochen, J. D. Langer, E. M. Schuman, Local and global influences on protein turnover in neurons and glia. eLife 7, e34202 (2018).
C. T. Schanzenbächer, S. Sambandan, J. D. Langer, E. M. Schuman, Nascent proteome remodeling following homeostatic scaling at hippocampal synapses. Neuron 92, 358–371 (2016).
C. Hanus, E. M. Schuman, Proteostasis in complex dendrites. Nat. Rev. Neurosci. 14, 638–648 (2013).
K. C. Martin, A. Ephrussi, mRNA localization: Gene expression in the spatial dimension. Cell 136, 719–730 (2009).
S. J. Van Driesche, K. C. Martin, New frontiers in RNA transport and local translation in neurons. Dev. Neurobiol. 78, 331–339 (2018).
C. Glock, M. Heumüller, E. M. Schuman, mRNA transport & local translation in neurons. Curr. Opin. Neurobiol. 45, 169–177 (2017).
M. Crispino, J. T. Chun, C. Cefaliello, C. Perrone Capano, A. Giuditta, Local gene expression in nerve endings. Dev. Neurobiol. 74, 279–291 (2014).
C. E. Holt, E. M. Schuman, The central dogma decentralized: New perspectives on RNA function and local translation in neurons. Neuron 80, 648–657 (2013).
D. S. Campbell, C. E. Holt, Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013–1026 (2001).
C. J. Donnelly, M. Fainzilber, J. L. Twiss, Subcellular communication through RNA transport and localized protein synthesis. Traffic 11, 1498–1505 (2010).
K. M. Leung, F. P. van Horck, A. C. Lin, R. Allison, N. Standart, C. E. Holt, Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9, 1247–1256 (2006).
D. E. Willis, E. A. van Niekerk, Y. Sasaki, M. Mesngon, T. T. Merianda, G. G. Williams, M. Kendall, D. S. Smith, G. J. Bassell, J. L. Twiss, Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J. Cell Biol. 178, 965–980 (2007).
A. Poulopoulos, A. J. Murphy, A. Ozkan, P. Davis, J. Hatch, R. Kirchner, J. D. Macklis, Subcellular transcriptomes and proteomes of developing axon projections in the cerebral cortex. Nature 565, 356–360 (2019).
T. Shigeoka, H. Jung, J. Jung, B. Turner-Bridger, J. Ohk, J. Q. Lin, P. S. Amieux, C. E. Holt, Dynamic axonal translation in developing and mature visual circuits. Cell 166, 181–192 (2016).
T. J. Younts, H. R. Monday, B. Dudok, M. E. Klein, B. A. Jordan, I. Katona, P. E. Castillo, Presynaptic protein synthesis is required for long-term plasticity of GABA release. Neuron 92, 479–492 (2016).
M. S. Scarnati, R. Kataria, M. Biswas, K. G. Paradiso, Active presynaptic ribosomes in the mammalian brain, and altered transmitter release after protein synthesis inhibition. eLife 7, e36697 (2018).
A. Giuditta, W. D. Dettbarn, M. Brzin, Protein synthesis in the isolated giant axon of the squid. Proc. Natl. Acad. Sci. U.S.A. 59, 1284–1287 (1968).
R. J. Lasek, C. Dabrowski, R. Nordlander, Analysis of axoplasmic RNA from invertebrate giant axons. Nat. New Biol. 244, 162–165 (1973).
M. R. Akins, H. E. Berk-Rauch, J. R. Fallon, Presynaptic translation: Stepping out of the postsynaptic shadow. Front. Neural Circuits 3, 17 (2009).
R. D. Vale, T. S. Reese, M. P. Sheetz, Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39–50 (1985).
P. W. Tillberg, F. Chen, K. D. Piatkevich, Y. Zhao, C. C. Yu, B. P. English, L. Gao, A. Martorell, H. J. Suk, F. Yoshida, E. M. DeGennaro, D. H. Roossien, G. Gong, U. Seneviratne, S. R. Tannenbaum, R. Desimone, D. Cai, E. S. Boyden, Protein-retention expansion microscopy of cells and tissues labeled using standard fluorescent proteins and antibodies. Nat. Biotechnol. 34, 987–992 (2016).
E. Herzog, G. C. Bellenchi, C. Gras, V. Bernard, P. Ravassard, C. Bedet, B. Gasnier, B. Giros, S. El Mestikawy, The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J. Neurosci. 21, RC181 (2001).
R. T. Fremeau Jr.., M. D. Troyer, I. Pahner, G. O. Nygaard, C. H. Tran, R. J. Reimer, E. E. Bellocchio, D. Fortin, J. Storm-Mathisen, R. H. Edwards, The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31, 247–260 (2001).
S. L. McIntire, R. J. Reimer, K. Schuske, R. H. Edwards, E. M. Jorgensen, Identification and characterization of the vesicular GABA transporter. Nature 389, 870–876 (1997).
C. Sagné, S. El Mestikawy, M. F. Isambert, M. Hamon, J. P. Henry, B. Giros, B. Gasnier, Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett. 417, 177–183 (1997).
E. Luquet, C. Biesemann, A. Munier, E. Herzog, Purification of Synaptosome Populations Using Fluorescence-Activated Synaptosome Sorting. Methods Mol. Biol. 1538, 121–134 (2017).
C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, E. Herzog, Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting. EMBO J. 33, 157–170 (2014).
V. P. Whittaker, I. A. Michaelson, R. J. Kirkland, The separation of synaptic vesicles from nerve-ending particles (‘synaptosomes’). Biochem. J. 90, 293–303 (1964).
E. Herzog, F. Nadrigny, K. Silm, C. Biesemann, I. Helling, T. Bersot, H. Steffens, R. Schwartzmann, U. V. Nägerl, S. El Mestikawy, J. Rhee, F. Kirchhoff, N. Brose, In vivo imaging of intersynaptic vesicle exchange using VGLUT1 Venus knock-in mice. J. Neurosci. 31, 15544–15559 (2011).
A. Vukoja, U. Rey, A. G. Petzoldt, C. Ott, D. Vollweiter, C. Quentin, D. Puchkov, E. Reynolds, M. Lehmann, S. Hohensee, S. Rosa, R. Lipowsky, S. J. Sigrist, V. Haucke, Presynaptic Biogenesis Requires Axonal Transport of Lysosome-Related Vesicles. Neuron 99, 1216–1232.e7 (2018).
J. C. Darnell, S. J. Van Driesche, C. Zhang, K. Y. Hung, A. Mele, C. E. Fraser, E. F. Stone, C. Chen, J. J. Fak, S. W. Chi, D. D. Licatalosi, J. D. Richter, R. B. Darnell, FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146, 247–261 (2011).
E. K. Schmidt, G. Clavarino, M. Ceppi, P. Pierre, SUnSET, a nonradioactive method to monitor protein synthesis. Nat. Methods 6, 275–277 (2009).
G. M. Shepherd, K. M. Harris, Three-dimensional structure and composition of CA3—>CA1 axons in rat hippocampal slices: Implications for presynaptic connectivity and compartmentalization. J. Neurosci. 18, 8300–8310 (1998).
S. tom Dieck, L. Kochen, C. Hanus, M. Heumüller, I. Bartnik, B. Nassim-Assir, K. Merk, T. Mosler, S. Garg, S. Bunse, D. A. Tirrell, E. M. Schuman, Direct visualization of newly synthesized target proteins in situ. Nat. Methods 12, 411–414 (2015).
H. Kang, E. M. Schuman, A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402–1406 (1996).
K. M. Huber, J. C. Roder, M. F. Bear, Chemical induction of mGluR5- and protein synthesis—Dependent long-term depression in hippocampal area CA1. J. Neurophysiol. 86, 321–325 (2001).
J. Zhong, T. Zhang, L. M. Bloch, Dendritic mRNAs encode diversified functionalities in hippocampal pyramidal neurons. BMC Neurosci. 7, 17 (2006).
E. S. Lein, M. J. Hawrylycz, N. Ao, M. Ayres, A. Bensinger, A. Bernard, A. F. Boe, M. S. Boguski, K. S. Brockway, E. J. Byrnes, L. Chen, L. Chen, T. M. Chen, M. C. Chin, J. Chong, B. E. Crook, A. Czaplinska, C. N. Dang, S. Datta, N. R. Dee, A. L. Desaki, T. Desta, E. Diep, T. A. Dolbeare, M. J. Donelan, H. W. Dong, J. G. Dougherty, B. J. Duncan, A. J. Ebbert, G. Eichele, L. K. Estin, C. Faber, B. A. Facer, R. Fields, S. R. Fischer, T. P. Fliss, C. Frensley, S. N. Gates, K. J. Glattfelder, K. R. Halverson, M. R. Hart, J. G. Hohmann, M. P. Howell, D. P. Jeung, R. A. Johnson, P. T. Karr, R. Kawal, J. M. Kidney, R. H. Knapik, C. L. Kuan, J. H. Lake, A. R. Laramee, K. D. Larsen, C. Lau, T. A. Lemon, A. J. Liang, Y. Liu, L. T. Luong, J. Michaels, J. J. Morgan, R. J. Morgan, M. T. Mortrud, N. F. Mosqueda, L. L. Ng, R. Ng, G. J. Orta, C. C. Overly, T. H. Pak, S. E. Parry, S. D. Pathak, O. C. Pearson, R. B. Puchalski, Z. L. Riley, H. R. Rockett, S. A. Rowland, J. J. Royall, M. J. Ruiz, N. R. Sarno, K. Schaffnit, N. V. Shapovalova, T. Sivisay, C. R. Slaughterbeck, S. C. Smith, K. A. Smith, B. I. Smith, A. J. Sodt, N. N. Stewart, K. R. Stumpf, S. M. Sunkin, M. Sutram, A. Tam, C. D. Teemer, C. Thaller, C. L. Thompson, L. R. Varnam, A. Visel, R. M. Whitlock, P. E. Wohnoutka, C. K. Wolkey, V. Y. Wong, M. Wood, M. B. Yaylaoglu, R. C. Young, B. L. Youngstrom, X. F. Yuan, B. Zhang, T. A. Zwingman, A. R. Jones, Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168–176 (2007).
M. M. Poon, S. H. Choi, C. A. Jamieson, D. H. Geschwind, K. C. Martin, Identification of process-localized mRNAs from cultured rodent hippocampal neurons. J. Neurosci. 26, 13390–13399 (2006).
I. J. Cajigas, G. Tushev, T. J. Will, S. tom Dieck, N. Fuerst, E. M. Schuman, The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74, 453–466 (2012).
L. F. Gumy, G. S. Yeo, Y. C. Tung, K. H. Zivraj, D. Willis, G. Coppola, B. Y. Lam, J. L. Twiss, C. E. Holt, J. W. Fawcett, Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17, 85–98 (2011).
K. H. Zivraj, Y. C. Tung, M. Piper, L. Gumy, J. W. Fawcett, G. S. Yeo, C. E. Holt, Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J. Neurosci. 30, 15464–15478 (2010).
L. A. Autilio, S. H. Appel, P. Pettis, P. L. Gambetti, Biochemical studies of synapses in vitro. I. Protein synthesis. Biochemistry 7, 2615–2622 (1968).
I. G. Morgan, L. Austin, Synaptosomal protein synthesis in a cell-free system. J. Neurochem. 15, 41–51 (1968).
S. Maday, A. E. Twelvetrees, A. J. Moughamian, E. L. Holzbaur, Axonal transport: Cargo-specific mechanisms of motility and regulation. Neuron 84, 292–309 (2014).
S. J. Tang, G. Reis, H. Kang, A. C. Gingras, N. Sonenberg, E. M. Schuman, A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 99, 467–472 (2002).
M. A. Sutton, H. T. Ito, P. Cressy, C. Kempf, J. C. Woo, E. M. Schuman, Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125, 785–799 (2006).
J. D. Richter, G. J. Bassell, E. Klann, Dysregulation and restoration of translational homeostasis in fragile X syndrome. Nat. Rev. Neurosci. 16, 595–605 (2015).
M. R. Akins, H. E. Berk-Rauch, K. Y. Kwan, M. E. Mitchell, K. A. Shepard, L. I. Korsak, E. E. Stackpole, J. L. Warner-Schmidt, N. Sestan, H. A. Cameron, J. R. Fallon, Axonal ribosomes and mRNAs associate with fragile X granules in adult rodent and human brains. Hum. Mol. Genet. 26, 192–209 (2017).
K. M. Huber, M. S. Kayser, M. F. Bear, Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288, 1254–1256 (2000).
W. B. Smith, S. R. Starck, R. W. Roberts, E. M. Schuman, Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron 45, 765–779 (2005).
G. Tushev, C. Glock, M. Heumüller, A. Biever, M. Jovanovic, E. M. Schuman, Alternative 3′ UTRs modify the localization, regulatory potential, stability, and plasticity of mRNAs in neuronal compartments. Neuron 98, 495–511.e6 (2018).
G. Aakalu, W. B. Smith, N. Nguyen, C. Jiang, E. M. Schuman, Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30, 489–502 (2001).
A. S. Hafner, A. C. Penn, D. Grillo-Bosch, N. Retailleau, C. Poujol, A. Philippat, F. Coussen, M. Sainlos, P. Opazo, D. Choquet, Lengthening of the stargazin cytoplasmic tail increases synaptic transmission by promoting interaction to deeper domains of PSD-95. Neuron 86, 475–489 (2015).
C. Fallini, P. G. Donlin-Asp, J. P. Rouanet, G. J. Bassell, W. Rossoll, Deficiency of the survival of motor neuron protein impairs mRNA localization and local translation in the growth cone of motor neurons. J. Neurosci. 36, 3811–3820 (2016).
C. C. Chou, Y. Zhang, M. E. Umoh, S. W. Vaughan, I. Lorenzini, F. Liu, M. Sayegh, P. G. Donlin-Asp, Y. H. Chen, D. M. Duong, N. T. Seyfried, M. A. Powers, T. Kukar, C. M. Hales, M. Gearing, N. J. Cairns, K. B. Boylan, D. W. Dickson, R. Rademakers, Y. J. Zhang, L. Petrucelli, R. Sattler, D. C. Zarnescu, J. D. Glass, W. Rossoll, TDP-43 pathology disrupts nuclear pore complexes and nucleocytoplasmic transport in ALS/FTD. Nat. Neurosci. 21, 228–239 (2018).
Genome Reference Consortium Mouse Build 38, mm10 (2011);
A. Dobin, C. A. Davis, F. Schlesinger, J. Drenkow, C. Zaleski, S. Jha, P. Batut, M. Chaisson, T. R. Gingeras, STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
Walter and Eliza Hall Institute, featureCounts: a ultrafast and accurate read summarization program;
D. J. McCarthy, Y. Chen, G. K. Smyth, Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 40, 4288–4297 (2012).
Y. Benjamini, Y. Hochberg, Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).
W. J. Kent, BLAT—The BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).
J. C. Oliveros, (2015). Venny. An interactive tool for comparing lists with Venn’s diagrams;


eLetters is an online forum for ongoing peer review. Submission of eLetters are open to all. eLetters are not edited, proofread, or indexed. Please read our Terms of Service before submitting your own eLetter.

Log In to Submit a Response

No eLetters have been published for this article yet.

Information & Authors


Published In

Volume 364 | Issue 6441
17 May 2019

Submission history

Received: 3 June 2018
Accepted: 2 April 2019
Published in print: 17 May 2019


Request permissions for this article.


We thank I. Bartnik, N. Fuerst, A. Staab, D. Vogel, and C. Thum for the preparation of cultured neurons; S. tom Dieck and T.W. Lee for important work in preliminary studies; H. Nguyen for experiments shown in Fig. 4H and fig. S7B; M. F. Angelo, A. Stum, and V. Pitard (flow cytometry facility, CNRS UMS 3427, INSERM US 005, University of Bordeaux, F-33000 Bordeaux, France) for technical assistance with FASS experiments; F. Cordelières (Bordeaux Imaging Center, University of Bordeaux, F-33000 Bordeaux, France) for image analysis routines; and G. Tushev for help with RNA sequencing analyses. Funding: A.-S.H. is supported by an EMBO long-term postdoctoral fellowship (ALTF 1095-2015) and the Alexander von Humboldt Foundation (FRA-1184902-HFST-P), as well as the National Infrastructure France–BioImaging, supported by the French National Research Agency (ANR-10-INBS-04). P.G.D.-A. is supported by the Peter and Traudl Engelhorn Foundation and the Alexander von Humboldt Foundation (USA-1198990-HFST-P). E.M.S. is funded by the Max Planck Society, an Advanced Investigator award from the European Research Council, DFG CRC 1080: Molecular and Cellular Mechanisms of Neural Homeostasis, and DFG CRC 902: Molecular Principles of RNA-based Regulation. This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement 743216). B.L. is funded by the Royal Society NZ–Germany Science and Technology Programme (FRG-UOO1403). E.H. is funded by the French National Research Agency (ANR-10-LABX-43 BRAIN Dolipran) and the Fondation pour la Recherche Médicale (ING20150532192). Author contributions: A.-S.H. and P.G.D.-A. designed, conducted, and analyzed experiments. E.H. and B.L. designed and supervised experiments. E.M.S. designed experiments, supervised the project, and wrote the paper. All authors edited the paper. Competing interests: The authors declare no competing financial interests. Data and materials availability: All data are available in the main text or the supplementary materials. The accession number for the raw sequencing data reported in this paper is NCBI BioProject: PRJNA544779.



Max Planck Institute for Brain Research, Frankfurt, Germany.
Max Planck Institute for Brain Research, Frankfurt, Germany.
Department of Anatomy, School of Biomedical Sciences and the Brain Health Research Centre, University of Otago, Dunedin, New Zealand.
Interdisciplinary Institute for Neuroscience, University of Bordeaux, UMR 5297, F-33000, Bordeaux, France.
Interdisciplinary Institute for Neuroscience, CNRS, UMR 5297, F-33000, Bordeaux, France.
Max Planck Institute for Brain Research, Frankfurt, Germany.

Funding Information

Agence Nationale de la Recherche: ANR-10-LABX-43 BRAIN Dolipran
France-BioImaging: Access-1576


These authors contributed equally to this work.
Corresponding author. Email: [email protected]

Metrics & Citations


Article Usage


Export citation

Select the format you want to export the citation of this publication.

Cited by

  1. Axonal protein synthesis in central nervous system regeneration: is building an axon a local matter?, Neural Regeneration Research, 17, 5, (987), (2022).
  2. Cortical wiring by synapse type–specific control of local protein synthesis, Science, 378, 6622, (2022)./doi/10.1126/science.abm7466
  3. Expansion sequencing: Spatially precise in situ transcriptomics in intact biological systems, Science, 371, 6528, (2021)./doi/10.1126/science.aax2656
  4. Activity-regulated synaptic targeting of lncRNA ADEPTR mediates structural plasticity by localizing Sptn1 and AnkB in dendrites, Science Advances, 7, 16, (2021)./doi/10.1126/sciadv.abf0605
  5. Coordination between Transport and Local Translation in Neurons, Trends in Cell Biology, 31, 5, (372-386), (2021).
  6. Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex, Nature Neuroscience, 24, 3, (425-436), (2021).
  7. Neuromuscular junction‐on‐a‐chip: ALS disease modeling and read‐out development in microfluidic devices, Journal of Neurochemistry, 157, 3, (393-412), (2021).
  8. Neuroproteomics of the Synapse: Subcellular Quantification of Protein Networks and Signaling Dynamics, Molecular & Cellular Proteomics, 20, (100087), (2021).
  9. Five trendy technologies: where are they now?, Nature, 594, 7864, (602-604), (2021).
  10. Presynaptic activity and protein turnover are correlated at the single-synapse level, Cell Reports, 34, 11, (108841), (2021).
  11. See more

View Options

Check Access

Log in to view the full text


AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.

Log in via OpenAthens.
Log in via Shibboleth.
More options

Register for free to read this article

As a service to the community, this article is available for free. Login or register for free to read this article.

Purchase this issue in print

Buy a single issue of Science for just $15 USD.

View options

PDF format

Download this article as a PDF file

Download PDF

Full Text








Share article link

Share on social media