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01-09-2015 | Review Paper

Structure, Distribution, and Function of Neuronal/Synaptic Spinules and Related Invaginating Projections

Authors: Ronald S. Petralia, Ya-Xian Wang, Mark P. Mattson, Pamela J. Yao

Published in: NeuroMolecular Medicine | Issue 3/2015

Abstract

Neurons and especially their synapses often project long thin processes that can invaginate neighboring neuronal or glial cells. These “invaginating projections” can occur in almost any combination of postsynaptic, presynaptic, and glial processes. Invaginating projections provide a precise mechanism for one neuron to communicate or exchange material exclusively at a highly localized site on another neuron, e.g., to regulate synaptic plasticity. The best-known types are postsynaptic projections called “spinules” that invaginate into presynaptic terminals. Spinules seem to be most prevalent at large very active synapses. Here, we present a comprehensive review of all kinds of invaginating projections associated with both neurons in general and more specifically with synapses; we describe them in all animals including simple, basal metazoans. These structures may have evolved into more elaborate structures in some higher animal groups exhibiting greater synaptic plasticity. In addition to classic spinules and filopodial invaginations, we describe a variety of lesser-known structures such as amphid microvilli, spinules in giant mossy terminals and en marron/brush synapses, the highly specialized fish retinal spinules, the trophospongium, capitate projections, and fly gnarls, as well as examples in which the entire presynaptic or postsynaptic process is invaginated. These various invaginating projections have evolved to modify the function of a particular synapse, or to channel an effect to one specific synapse or neuron, without affecting those nearby. We discuss how they function in membrane recycling, nourishment, and cell signaling and explore how they might change in aging and disease.

Acsády, L., Katona, I., Martinez-Guijarro, F. J., Buzsaki, G., & Freund, T. F. (2000). Unusual target selectivity of perisomatic inhibitory cells in the hilar region of the rat hippocampus. Journal of Neuroscience, 20(18), 6907–6919.PubMed

Adamo, N. J., & Daigneault, E. A. (1973a). Ultrastructural features of neurons and nerve fibres in the spiral ganglia of cats. Journal of Neurocytology, 2(1), 91–103.PubMed

Adamo, N. J., & Daigneault, E. A. (1973b). Ultrastructural morphology of Schwann cell-neuronal relationships in the spiral ganglia of cats. American Journal of Anatomy, 138(1), 73–77. doi:10.1002/aja.1001380105.PubMed

Altman, J. (1971). Coated vesicles and synaptogenesis. A developmental study in the cerebellar cortex of the rat. Brain Research, 30(2), 311–322.PubMed

Altman, J. (1993). Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. Journal of Comparative Neurology, 145, 399–464.

Altman, J., & Bayer, S. A. (1997). Development of the cerebellar system in relation to its evolution, structure, and functions. New York: CRC Press.

Anglade, P., Mouatt-Prigent, A., Agid, Y., & Hirsch, E. (1996). Synaptic plasticity in the caudate nucleus of patients with Parkinson’s disease. Neurodegeneration, 5(2), 121–128.PubMed

Ashton, F. T., Li, J., & Schad, G. A. (1999). Chemo- and thermosensory neurons: Structure and function in animal parasitic nematodes. Veterinary Parasitology, 84(3–4), 297–316.PubMed

Atwood, H. L., Govind, C. K., & Wu, C. F. (1993). Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. Journal of Neurobiology, 24(8), 1008–1024. doi:10.1002/neu.480240803.PubMed

Bailey, C. H., Chen, M., Keller, F., & Kandel, E. R. (1992). Serotonin-mediated endocytosis of apCAM: An early step of learning-related synaptic growth in Aplysia. Science, 256(5057), 645–649.PubMed

Bailey, C. H., Thompson, E. B., Castellucci, V. F., & Kandel, E. R. (1979). Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex in Aplysia. Journal of Neurocytology, 8(4), 415–444.PubMed

Biserova, N. M. (2008). Do glial cells exist in the nervous system of parasitic and free-living flatworms? An ultrastructural and immunocytochemical investigation. Acta Biologica Hungarica, 59(Suppl), 209–219. doi:10.1556/ABiol.59.2008.Suppl.30.PubMed

Biserova, N. M., Gordeev, I. I., Korneva, J. V., & Salnikova, M. M. (2010). Structure of the glial cells in the nervous system of parasitic and free-living flatworms. Biology Bulletin, 37(3), 277–287.

Blanco, R. E. (1988). Glial cells in peripheral nerves of the cockroach, Periplaneta americana. Tissue and Cell, 20(5), 771–782.PubMed

Blanque, A., Repetto, D., Rohlmann, A., Brockhaus, J., Duning, K., Pavenstädt, H., et al. (2015). Deletion of KIBRA, protein expressed in kidney and brain, increases filopodial-like long dendritic spines in neocortical and hippocampal neurons in vivo and in vitro. Frontiers in Neuroanatomy, 9, 13. doi:10.3389/fnana.2015.00013.PubMedCentralPubMed

Bonga, S. E. W. (1970). Ultrastructure and histochemistry of neurosecretory cells and neurohaemal areas in the pond snail Lymnaea stagnalis. Zeitschrift für Zellforschung und Mikroskopische Anatomie, 108, 190–224.

Boschek, C. B. (1971). On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. Zeitschrift für Zellforschung und Mikroskopische Anatomie, 118(3), 369–409.PubMed

Boyne, A. F., & McLeod, S. (1979). Ultrastructural plasticity in stimulated nerve terminals: Pseudopodial invasions of abutted terminals in Torpedine ray electric organ. Neuroscience, 4(5), 615–624.PubMed

Boyne, A. F., & Tarrant, S. B. (1982). Pseudopodial interdigitations between abutted nerve terminals: diffusion traps which occur in several nuclei of the rat limbic system. Journal of Neuroscience, 2(4), 463–469.PubMed

Bozhilova-Pastirova, A., & Ovtscharoff, W. (1999). Intramembranous structure of synaptic membranes with special reference to spinules in the rat sensorimotor cortex. European Journal of Neuroscience, 11(5), 1843–1846.PubMed

Buchheit, T. E., & Tytell, M. (1992). Transfer of molecules from glia to axon in the squid may be mediated by glial vesicles. Journal of Neurobiology, 23(3), 217–230. doi:10.1002/neu.480230303.PubMed

Budziakowski, M. E., & Mettrick, D. F. (1985). Ultrastructural morphology of the neuropile of the cerebral ganglion of Moniliformis moniliformis (Acanthocephala). Journal of Parasitology, 71(1), 75–85.PubMed

Bumbarger, D. J., Wijeratne, S., Carter, C., Crum, J., Ellisman, M. H., & Baldwin, J. G. (2009). Three-dimensional reconstruction of the amphid sensilla in the microbial feeding nematode, Acrobeles complexus (Nematoda: Rhabditida). Journal of Comparative Neurology, 512(2), 271–281. doi:10.1002/cne.21882.PubMedCentralPubMed

Cadete-Leite, A., Tavares, M. A., Paula-Barbosa, M. M., & Gray, E. G. (1986). ‘Perforated’ synapses in frontal cortex of chronic alcohol-fed rats. Journal of Submicroscopic Cytology, 18(3), 495–499.PubMed

Cagan, R. L., Kramer, H., Hart, A. C., & Zipursky, S. L. (1992). The bride of sevenless and sevenless interaction: Internalization of a transmembrane ligand. Cell, 69(3), 393–399.PubMed

Calverley, R. K., & Jones, D. G. (1987). A serial-section study of perforated synapses in rat neocortex. Cell and Tissue Research, 247(3), 565–572.PubMed

Campos-Ortega, J. A., & Strausfeld, N. J. (1973). Synaptic connections of intrinsic cells and basket arborizations in the external plexiform layer of the fly’s eye. Brain Research, 59, 119–136.PubMed

Carlin, R. K., & Siekevitz, P. (1983). Plasticity in the central nervous system: Do synapses divide? Proceedings of the National Academy of Sciences of the USA, 80(11), 3517–3521.PubMedCentralPubMed

Carlson, S. D. (1987). Ultrastructure of the arthropod neuroglia and neuropil. In A. P. Gupta (Ed.), Arthropod brain: Its evolution, development, structure, and functions (pp. 323–346). New York: Wiley.

Case, N. M., Gray, E. G., & Young, J. Z. (1972). Ultrastructure and synaptic relations in the optic lobe of the brain of Eledone and Octopus. Journal of Ultrastructure Research, 39(1), 115–123.PubMed

Chi, C., & Carlson, S. D. (1976). Close apposition of photoreceptor cell axons in the house fly. Journal of Insect Physiology, 22(8), 1153–1157.PubMed

Chicurel, M. E., & Harris, K. M. (1992). Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. Journal of Comparative Neurology, 325(2), 169–182. doi:10.1002/cne.903250204.PubMed

Chivet, M., Hemming, F., Pernet-Gallay, K., Fraboulet, S., & Sadoul, R. (2012). Emerging role of neuronal exosomes in the central nervous system. Frontiers in Physiology, 3, 145. doi:10.3389/fphys.2012.00145.PubMedCentralPubMed

Cocucci, E., & Meldolesi, J. (2015). Ectosomes and exosomes: Shedding the confusion between extracellular vesicles. Trends in Cell Biology, 25(6), 364–372.PubMed

Cocucci, E., Racchetti, G., & Meldolesi, J. (2009). Shedding microvesicles: Artefacts no more. Trends in Cell Biology, 19(2), 43–51. doi:10.1016/j.tcb.2008.11.003.PubMed

Coggeshall, R. E., & Fawcett, D. W. (1964). The fine structure of the central nervous system of the leech, Hirudo medicinalis. Journal of Neurophysiology, 27, 229–289.PubMed

Cohen, A. I. (1973). An ultrastructural analysis of the photoreceptors of the squid and their synaptic connections. 3. Photoreceptor terminations in the optic lobes. Journal of Comparative Neurology, 147(3), 399–426. doi:10.1002/cne.901470306.PubMed

Curcio, C. A., McNelly, N. A., & Hinds, J. W. (1985). Aging in the rat olfactory system: Relative stability of piriform cortex contrasts with changes in olfactory bulb and olfactory epithelium. Journal of Comparative Neurology, 235(4), 519–528. doi:10.1002/cne.902350409.PubMed

Dayel, M. J., Alegado, R. A., Fairclough, S. R., Levin, T. C., Nichols, S. A., McDonald, K., et al. (2011). Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Development Biology, 357(1), 73–82. doi:10.1016/j.ydbio.2011.06.003.

Desmond, N. L., & Levy, W. B. (1983). Synaptic correlates of associative potentiation/depression: An ultrastructural study in the hippocampus. Brain Research, 265(1), 21–30.PubMed

Dilly, P. N., Gray, E. G., & Young, J. Z. (1963). Electron microscopy of optic nerves and optic lobes of Octopus and Eledone. Proceedings of the Royal Society of London. Series B: Biological Sciences, 158, 446–456.

Dino, M. R., Nunzi, M. G., Anelli, R., & Mugnaini, E. (2000). Unipolar brush cells of the vestibulocerebellum: Afferents and targets. Progress in Brain Research, 124, 123–137. doi:10.1016/S0079-6123(00)24013-2.PubMed

Dirks, P., Tieding, S., Schneider, I., Mey, J., & Weiler, R. (2004). Characterization of retinoic acid neuromodulation in the carp retina. Journal of Neuroscience Research, 78(2), 177–185. doi:10.1002/jnr.20253.PubMed

Dyson, S. E., & Jones, D. G. (1984). Synaptic remodelling during development and maturation: Junction differentiation and splitting as a mechanism for modifying connectivity. Brain Research, 315(1), 125–137.PubMed

Eckenhoff, M. F., & Pysh, J. J. (1979). Double-walled coated vesicle formation: Evidence for massive and transient conjugate internalization of plasma membranes during cerebellar development. Journal of Neurocytology, 8(5), 623–638.PubMed

Erisir, A., & Dreusicke, M. (2005). Quantitative morphology and postsynaptic targets of thalamocortical axons in critical period and adult ferret visual cortex. Journal of Comparative Neurology, 485(1), 11–31. doi:10.1002/cne.20507.PubMed

Fabian-Fine, R., Verstreken, P., Hiesinger, P. R., Horne, J. A., Kostyleva, R., Zhou, Y., et al. (2003). Endophilin promotes a late step in endocytosis at glial invaginations in Drosophila photoreceptor terminals. Journal of Neuroscience, 23(33), 10732–10744.PubMed

Fader, C. M., & Colombo, M. I. (2009). Autophagy and multivesicular bodies: Two closely related partners. Cell Death and Differentiation, 16(1), 70–78. doi:10.1038/cdd.2008.168.PubMed

Fairchild, C. L., & Barna, M. (2014). Specialized filopodia: At the “tip” of morphogen transport and vertebrate tissue patterning. Current Opinion in Genetics & Development, 27, 67–73.

Familtsev, D. (2013). Synapses, spines, zinc and pathology of Alzheimer’s disease. Louisville, Kentucky: University of Louisville.

Farley, R. D., & Chan, D. J. (1985). The ultrastructure of the cardiac ganglion of the desert scorpion, Paruroctonus mesaensis (Scorpionida: Vaejovidae). J Morph, 184, 231–252.

Fedorenko, G. M., & Uzdensky, A. B. (2009). Ultrastructure of neuroglial contacts in crayfish stretch receptor. Cell and Tissue Research, 337(3), 477–490. doi:10.1007/s00441-009-0825-7.PubMed

Fiala, J. C., Allwardt, B., & Harris, K. M. (2002). Dendritic spines do not split during hippocampal LTP or maturation. Nature Neuroscience, 5(4), 297–298. doi:10.1038/nn830.PubMed

Fiala, J. C., Feinberg, M., Popov, V., & Harris, K. M. (1998). Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. Journal of Neuroscience, 18(21), 8900–8911.PubMed

Floris, A., Dino, M., Jacobowitz, D. M., & Mugnaini, E. (1994). The unipolar brush cells of the rat cerebellar cortex and cochlear nucleus are calretinin-positive: A study by light and electron microscopic immunocytochemistry. Anatomy and Embryology (Berl), 189(6), 495–520.

Fox, C. A., Andrade, A. N., Lu Qui, I. J., & Rafols, J. A. (1974). The primate globus pallidus: A Golgi and electron microscopic study. Journal fur Hirnforschung, 15(1), 75–93.PubMed

Friedlander, M. J., Martin, K. A. C., & Wassenhove-McCarthy, D. (1991). Effects of monocular visual deprivation on geniculocortical innervation of area 18 in cat. Journal of Neuroscience, 11(10), 3268–3288.PubMed

Fritzsch, B., & Straka, H. (2014). Evolution of vertebrate mechanosensory hair cells and inner ears: Toward identifying stimuli that select mutation driven altered morphologies. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 200(1), 5–18. doi:10.1007/s00359-013-0865-z.PubMedCentralPubMed

Fröhlich, A., & Meinertzhagen, I. A. (1982). Synaptogenesis in the first optic neuropile of the fly’s visual system. Journal of Neurocytology, 11(1), 159–180.PubMed

Gad, H., Low, P., Zotova, E., Brodin, L., & Shupliakov, O. (1998). Dissociation between Ca²⁺-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron, 21(3), 607–616.PubMed

Ganeshina, O., Berry, R. W., Petralia, R. S., Nicholson, D. A., & Geinisman, Y. (2004a). Synapses with a segmented, completely partitioned postsynaptic density express more AMPA receptors than other axospinous synaptic junctions. Neuroscience, 125(3), 615–623.PubMed

Ganeshina, O., Berry, R. W., Petralia, R. S., Nicholson, D. A., & Geinisman, Y. (2004b). Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. Journal of Comparative Neurology, 468(1), 86–95.PubMed

Gao, C., Cao, W., Bao, L., Zuo, W., Xie, G., Cai, T., et al. (2010). Autophagy negatively regulates Wnt signalling by promoting Dishevelled degradation. Nature Cell Biology, 12(8), 781–790. doi:10.1038/ncb2082.PubMed

Geinisman, Y. (2000). Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cerebral Cortex, 10(10), 952–962.PubMed

Geinisman, Y., deToledo-Morrell, L., & Morrell, F. (1994). Comparison of structural synaptic modifications induced by long-term potentiation in the hippocampal dentate gyrus of young adult and aged rats. Annals of the New York Academy of Sciences, 747, 452–466.PubMed

Gennaro, J. F, Jr, Nastuk, W. L., & Rutherford, D. T. (1978). Reversible depletion of synaptic vesicles induced by application of high external potassium to the frog neuromuscular junction. Journal of Physiology, 280, 237–247.PubMedCentralPubMed

Gonobobleva, E., & Maldonado, M. (2009). Choanocyte ultrastructure in Halisarca dujardini (Demospongiae, Halisarcida). Journal of Morphology, 270(5), 615–627. doi:10.1002/jmor.10709.PubMed

Gordon, W. C. (1985). Nonconventional interactions between photoreceptor axons in the butterfly lamina ganglionaris. Zeitschrift für Naturforschung, 40c, 460–463.

Gray, E. G. (1961). The granule cells, mossy synapses and Purkinje spine synapses of the cerebellum: Light and electron microscope observations. Journal of Anatomy, 95, 345–356.PubMedCentralPubMed

Greco, V., Hannus, M., & Eaton, S. (2001). Argosomes: A potential vehicle for the spread of morphogens through epithelia. Cell, 106(5), 633–645.PubMed

Gregory, W. A., Hall, D. H., & Bennett, M. V. (1988). Satellite glial cells penetrate neurosecretory cells to perinuclear position in the goldfish preoptic area. Developmental Brain Research, 44(1), 1–8.PubMed

Gurke, S., Barroso, J. F., & Gerdes, H. H. (2008). The art of cellular communication: Tunneling nanotubes bridge the divide. Histochemistry and Cell Biology, 129(5), 539–550. doi:10.1007/s00418-008-0412-0.PubMedCentralPubMed

Haamedi, S. N., Karten, H. J., & Djamgoz, M. B. (2001). Nerve growth factor induces light adaptive cellular and synaptic plasticity in the outer retina of fish. Journal of Comparative Neurology, 431(4), 397–404.PubMed

Halanych, K. M. (2015). The ctenophore lineage is older than sponges? That cannot be right! Or can it? Journal of Experimental Biology, 218(Pt 4), 592–597. doi:10.1242/jeb.111872.PubMed

Harreveld, A. V., & Trubatch, J. (1975). Synaptic changes in frog brain after stimulation with potassium chloride. Journal of Neurocytology, 4(1), 33–46.PubMed

Hartfelder, K., Hanton, W. K., & Bollenbacher, W. E. (1994). Diapause-dependent changes in prothoracicotropic hormone-producing neurons of the tobacco hornworm, Manduca sexta. Cell and Tissue Research, 277(1), 69–78.PubMed

Heuser, J. E., & Reese, T. S. (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. Journal of Cell Biology, 57(2), 315–344.PubMedCentralPubMed

Holtmann, M., & Thurm, U. (2001). Mono- and oligo-vesicular synapses and their connectivity in a Cnidarian sensory epithelium (Coryne tubulosa). J Comp Neurol, 432(4), 537–549.PubMed

Hoyle, G., Williams, M., & Philips, C. (1986). Functional morphology of insect neuronal cell-surface/glial contacts: The trophospongium. Journal of Comparative Neurology, 246, 113–128.PubMed

Huganir, R. L., & Nicoll, R. A. (2013). AMPARs and synaptic plasticity: The last 25 years. Neuron, 80(3), 704–717. doi:10.1016/j.neuron.2013.10.025.PubMedCentralPubMed

Jia, X. X., Gorczyca, M., & Budnik, V. (1993). Ultrastructure of neuromuscular junctions in Drosophila: Comparison of wild type and mutants with increased excitability. Journal of Neurobiology, 24(8), 1025–1044. doi:10.1002/neu.480240804.PubMed

Jones, D. G., & Calverley, R. K. (1991). Perforated and non-perforated synapses in rat neocortex: Three-dimensional reconstructions. Brain Research, 556(2), 247–258.PubMed

Jorgensen, E. M. (2014). Animal evolution: Looking for the first nervous system. Current Biology, 24(14), R655–R658. doi:10.1016/j.cub.2014.06.036.PubMed

Joshi, P., Benussi, L., Furlan, R., Ghidoni, R., & Verderio, C. (2015). Extracellular Vesicles in Alzheimer’s Disease: Friends or Foes? Focus on Abeta-Vesicle Interaction. International Journal of Molecular Sciences, 16(3), 4800–4813. doi:10.3390/ijms16034800.PubMedCentralPubMed

Klooster, J., Yazulla, S., & Kamermans, M. (2009). Ultrastructural analysis of the glutamatergic system in the outer plexiform layer of zebrafish retina. Journal of Chemical Neuroanatomy, 37(4), 254–265. doi:10.1016/j.jchemneu.2009.02.004.PubMed

Klueg, K. M., & Muskavitch, M. A. (1999). Ligand-receptor interactions and trans-endocytosis of Delta, Serrate and Notch: Members of the Notch signalling pathway in Drosophila. Journal of Cell Science, 112(Pt 19), 3289–3297.PubMed

Korkut, C., Ataman, B., Ramachandran, P., Ashley, J., Barria, R., Gherbesi, N., et al. (2009). Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell, 139(2), 393–404. doi:10.1016/j.cell.2009.07.051.PubMedCentralPubMed

Korkut, C., Li, Y., Koles, K., Brewer, C., Ashley, J., Yoshihara, M., et al. (2013). Regulation of postsynaptic retrograde signaling by presynaptic exosome release. Neuron, 77(6), 1039–1046. doi:10.1016/j.neuron.2013.01.013.PubMedCentralPubMed

Kornberg, T. B., & Roy, S. (2014). Cytonemes as specialized signaling filopodia. Development, 141(4), 729–736. doi:10.1242/dev.086223.PubMedCentralPubMed

Krämer, H., Cagan, R. L., & Zipursky, S. L. (1991). Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor. Nature, 352(6332), 207–212. doi:10.1038/352207a0.PubMed

Kröger, R. H., & Wagner, H. J. (1996). Horizontal cell spinule dynamics in fish are affected by rearing in monochromatic light. Vision Research, 36(24), 3879–3889.PubMed

Larsen, W. J. (1983). Biological implications of gap junction structure, distribution and composition: A review. Tissue and Cell, 15(5), 645–671.PubMed

Leise, E. M., & Cloney, R. A. (1982). Chiton integument: Ultrastructure of the sensory hairs of Mopalia muscosa (Mollusca: Polyplacophora). Cell and Tissue Research, 223(1), 43–59.PubMed

Leranth, C., & Frotscher, M. (1986). Synaptic connections of cholecystokinin-immunoreactive neurons and terminals in the rat fascia dentata: A combined light and electron microscopic study. Journal of Comparative Neurology, 254(1), 51–64. doi:10.1002/cne.902540105.PubMed

Leys, S. P. (2015). Elements of a ‘nervous system’ in sponges. Journal of Experimental Biology, 218(Pt 4), 581–591. doi:10.1242/jeb.110817.PubMed

Li, Y. C., Li, Y. N., Cheng, C. X., Sakamoto, H., Kawate, T., Shimada, O., et al. (2005). Subsurface cisterna-lined axonal invaginations and double-walled vesicles at the axonal-myelin sheath interface. Neuroscience Research, 53(3), 298–303. doi:10.1016/j.neures.2005.07.006.PubMed

Mäntylä, K., Reuter, M., Halton, D. W., Maule, A. G., Brennan, G. P., Shaw, C., et al. (1998). The nervous system of Procerodes littoralis (Maricola, Tricladida). An ultrastructural and immunoelectron microscopical study. Acta Zoologica, 79(1), 1–8.

Marston, D. J., Dickinson, S., & Nobes, C. D. (2003). Rac-dependent trans-endocytosis of ephrinBs regulates Eph–ephrin contact repulsion. Nature Cell Biology, 5(10), 879–888. doi:10.1038/ncb1044.PubMed

Mashanov, V. S., Zueva, O. R., Heinzeller, T., & Dolmatov, I. Y. (2006). Ultrastructure of the circumoral nerve ring and the radial nerve cords in holothurians (Echinodermata). Zoomorphology, 125, 27–38.

Matsuo, I., Kimura-Yoshida, C., & Shimokawa, K. (2014). Divergent roles of heparan sulfate in regulation of FGF signaling during mammalian embryogenesis. In H. Kondoh & A. Kuroiwa (Eds.), New principles in developmental processes (pp. 239–251). Japan: Springer.

Matthews, G., & Fuchs, P. (2010). The diverse roles of ribbon synapses in sensory neurotransmission. Nature Reviews Neuroscience, 11(12), 812–822. doi:10.1038/nrn2924.PubMedCentralPubMed

Medvedev, N. I., Dallérac, G., Popov, V. I., Rodriguez Arellano, J. J., Davies, H. A., Kraev, I. V., et al. (2014). Multiple spine boutons are formed after long-lasting LTP in the awake rat. Brain Structure and Function, 219(1), 407–414. doi:10.1007/s00429-012-0488-0.PubMed

Meyer, D., Bonhoeffer, T., & Scheuss, V. (2014). Balance and stability of synaptic structures during synaptic plasticity. Neuron, 82(2), 430–443. doi:10.1016/j.neuron.2014.02.031.PubMed

Mitchell, N., Petralia, R. S., Currier, D. G., Wang, Y. X., Kim, A., Mattson, M. P., et al. (2012). Sonic hedgehog regulates presynaptic terminal size, ultrastructure and function in hippocampal neurons. Journal of Cell Science, 125(Pt 18), 4207–4213. doi:10.1242/jcs.105080.PubMedCentralPubMed

Mueller, W. A., Hassel, M., & Grealy, M. (2015). Development and reproduction in humans and animal model species. Berlin: Springer.

Mugnaini, E., Floris, A., & Wright-Goss, M. (1994). Extraordinary synapses of the unipolar brush cell: An electron microscopic study in the rat cerebellum. Synapse, 16(4), 284–311. doi:10.1002/syn.890160406.PubMed

Mugnaini, E., Osen, K. K., Dahl, A. L., Friedrich, V. L, Jr, & Korte, G. (1980). Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat and mouse. Journal of Neurocytology, 9(4), 537–570.PubMed

Mugnaini, E., Sekerkova, G., & Martina, M. (2011). The unipolar brush cell: A remarkable neuron finally receiving deserved attention. Brain Research Reviews, 66(1–2), 220–245. doi:10.1016/j.brainresrev.2010.10.001.PubMedCentralPubMed

Muralidharan-Chari, V., Clancy, J., Plou, C., Romao, M., Chavrier, P., Raposo, G., et al. (2009). ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Current Biology, 19(22), 1875–1885. doi:10.1016/j.cub.2009.09.059.PubMedCentralPubMed

Muriel, M. P., Agid, Y., & Hirsch, E. (2001). Plasticity of afferent fibers to striatal neurons bearing D1 dopamine receptors in Parkinson’s disease. Movement Disorders, 16(3), 435–441.PubMed

Murphy, D. D., & Andrews, S. B. (2000). Culture models for the study of estradiol-induced synaptic plasticity. Journal of Neurocytology, 29(5–6), 411–417.PubMed

Nickel, M. (2010). Evolutionary emergence of synaptic nervous systems: What can we learn from the non-synaptic, nerveless Porifera? Invertebrate Biology, 129(1), 1–16.

Nitsch, C., & Rinne, U. (1981). Large dense-core vesicle exocytosis and membrane recycling in the mossy fibre synapses of the rabbit hippocampus during epileptiform seizures. Journal of Neurocytology, 10(2), 201–209.PubMed

Nordlander, R. H., Masnyi, J. A., & Singer, M. (1975). Distribution of ultrastructural tracers in crustacean axons. Journal of Comparative Neurology, 161, 499–514.PubMed

Omiya, Y., Uchigashima, M., Konno, K., Yamasaki, M., Miyazaki, T., Yoshida, T., et al. (2015). VGluT3-Expressing CCK-positive basket cells construct invaginating synapses enriched with endocannabinoid signaling proteins in particular cortical and cortex-like amygdaloid regions of mouse brains. Journal of Neuroscience, 35(10), 4215–4228. doi:10.1523/JNEUROSCI.4681-14.2015.PubMed

Osborne, M. P. (1967). The fine structure of neuromuscular junctions in the segmental muscles of the blowfly larva. Journal of Insect Physiology, 13, 827–833.

Palacios-Prü, E. L., Palacios, L., & Mendoza, R. V. (1981). Synaptogenetic mechanisms during chick cerebellar cortex development. Journal of Submicroscopic Cytology, 13(2), 145–167.PubMed

Palay, S. L., & Chan-Palay, V. (1974). Cerebellar cortex. Cytology and organization. New York: Springer.

Papassotiropoulos, A., Stephan, D. A., Huentelman, M. J., Hoerndli, F. J., Craig, D. W., Pearson, J. V., et al. (2006). Common Kibra alleles are associated with human memory performance. Science, 314(5798), 475–478. doi:10.1126/science.1129837.PubMed

Pappas, G. D., & Purpura, D. P. (1961). Fine structure of dendrites in the superficial neocortical neuropil. Experimental Neurology, 4, 507–530.PubMed

Paspalas, C. D., Rakic, P., & Goldman-Rakic, P. S. (2006). Internalization of D2 dopamine receptors is clathrin-dependent and select to dendro-axonic appositions in primate prefrontal cortex. European Journal of Neuroscience, 24(5), 1395–1403. doi:10.1111/j.1460-9568.2006.05023.x.PubMed

Passey, S., Pellegrin, S., & Mellor, H. (2004). What is in a filopodium? Starfish versus hedgehogs. Biochemical Society Transactions, 32(Pt 6), 1115–1117. doi:10.1042/BST0321115.PubMed

Pavans de Ceccatty, M. (1966). Ultrastructures et rapports des cellules mesenchymateuses de type nerveux de l’eponge Tethya lyncurium Link. Annales des Sciences Naturelles—Zoologie et Biologie Animale, 8, 577–614.

Pentreath, V. W., Berry, M. S., & Cobb, J. L. (1975). Nerve-ending specializations in the central ganglia of Planorbis corneus. Cell and Tissue Research, 163(1), 99–110.PubMed

Pérez-Cruz, C., Delgado, L., Lopez-Iglesias, C., & Mercade, E. (2015). Outer-inner membrane vesicles naturally secreted by gram-negative pathogenic bacteria. PLoS One, 10(1), e0116896. doi:10.1371/journal.pone.0116896.PubMedCentralPubMed

Petralia, R. S., Mattson, M. P., & Yao, P. J. (2014a). Communication breakdown: The impact of ageing on synapse structure. Ageing Res Rev, 14, 31–42.PubMedCentralPubMed

Petralia, R. S., Mattson, M. P., & Yao, P. J. (2014b). Aging and longevity in the simplest animals and the quest for immortality. Ageing Research Reviews, 16, 66–82. doi:10.1016/j.arr.2014.05.003.PubMed

Petralia, R. S., Schwartz, C. M., Wang, Y. X., Mattson, M. P., & Yao, P. J. (2011). Subcellular localization of patched and smoothened, the receptors for sonic hedgehog signaling, in the hippocampal neuron. Journal of Comparative Neurology, 519(18), 3684–3699. doi:10.1002/cne.22681.PubMedCentralPubMed

Petralia, R. S., Wang, Y. X., Mattson, M. P., & Yao, P. J. (2012). Subcellular distribution of patched and smoothened in the cerebellar neurons. Cerebellum, 11(4), 972–981. doi:10.1007/s12311-012-0374-6.PubMedCentralPubMed

Petralia, R. S., & Wenthold, R. J. (1992). Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. Journal of Comparative Neurology, 318(3), 329–354. doi:10.1002/cne.903180309.PubMed

Popov, V. I., Kleschevnikov, A. M., Klimenko, O. A., Stewart, M. G., & Belichenko, P. V. (2011). Three-dimensional synaptic ultrastructure in the dentate gyrus and hippocampal area CA3 in the Ts65Dn mouse model of down syndrome. Journal of Comparative Neurology, 519(7), 1338–1354. doi:10.1002/cne.22573.PubMed

Popova, E. (2014). Role of dopamine in distal retina. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 200(5), 333–358. doi:10.1007/s00359-014-0906-2.PubMed

Prokop, A., & Meinertzhagen, I. A. (2006). Development and structure of synaptic contacts in Drosophila. Seminars in Cell and Developmental Biology, 17(1), 20–30. doi:10.1016/j.semcdb.2005.11.010.PubMed

Raikova, O. I., Reuter, M., Jondelius, U., & Gustafsson, M. K. S. (2000). An immunocytochemical and ultrastructural study of the nervous and muscular systems of Xenoturbella westbladi (Bilateria inc. sed.). Zoomorphology, 120, 107–118.

Rajendran, L., Bali, J., Barr, M. M., Court, F. A., Kramer-Albers, E. M., Picou, F., et al. (2014). Emerging roles of extracellular vesicles in the nervous system. Journal of Neuroscience, 34(46), 15482–15489. doi:10.1523/JNEUROSCI.3258-14.2014.PubMedCentralPubMed

Ramirez-Weber, F. A., & Kornberg, T. B. (1999). Cytonemes: Cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell, 97(5), 599–607.PubMed

Remis, J. P., Wei, D., Gorur, A., Zemla, M., Haraga, J., Allen, S., et al. (2014). Bacterial social networks: Structure and composition of Myxococcus xanthus outer membrane vesicle chains. Environmental Microbiology, 16(2), 598–610. doi:10.1111/1462-2920.12187.PubMedCentralPubMed

Renard, E., Vacelet, J., Gazave, E., Lapebie, P., Borchiellini, C., & Ereskovsky, A. V. (2009). Origin of the neuro-sensory system: New and expected insights from sponges. Integrative Zoology, 4(3), 294–308. doi:10.1111/j.1749-4877.2009.00167.x.PubMed

Richards, D. A., Mateos, J. M., Hugel, S., de Paola, V., Caroni, P., Gahwiler, B. H., et al. (2005). Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures. Proceedings of the National Academy of Sciences of the USA, 102(17), 6166–6171. doi:10.1073/pnas.0501881102.PubMedCentralPubMed

Ringstad, N., Gad, H., Low, P., Di Paolo, G., Brodin, L., Shupliakov, O., et al. (1999). Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron, 24(1), 143–154.PubMed

Risinger, M. A., & Larsen, W. J. (1981). Endocytosis of cell-cell junctions and spontaneous cell disaggregation in a cultured human ovarian adenocarcinoma. (COLO 316). Tissue and Cell, 13(2), 413–430.PubMed

Robbins, J. R., Barth, A. I., Marquis, H., de Hostos, E. L., Nelson, W. J., & Theriot, J. A. (1999). Listeria monocytogenes exploits normal host cell processes to spread from cell to cell. Journal of Cell Biology, 146(6), 1333–1350.PubMedCentralPubMed

Saint Marie, R. L., & Carlson, S. D. (1982). Synaptic vesicle activity in stimulated and unstimulated photoreceptor axons in the housefly. A freeze-fracture study. Journal of Neurocytology, 11(5), 747–761.PubMed

Sasaki, S., & Iwata, M. (1995). Synaptic loss in the proximal axon of anterior horn neurons in motor neuron disease. Acta Neuropathologica, 90(2), 170–175.PubMed

Sasaki, S., & Iwata, M. (1996). Synaptic loss in anterior horn neurons in lower motor neuron disease. Acta Neuropathologica, 91(4), 416–421.PubMed

Sasaki, S., & Iwata, M. (1999). Ultrastructural change of synapses of Betz cells in patients with amyotrophic lateral sclerosis. Neuroscience Letters, 268(1), 29–32.PubMed

Satterlie, R. A., & Case, J. F. (1978). Gap junctions suggest epithelial conduction within the comb plates of the ctenophore Pleurobrachia bachei. Cell and Tissue Research, 193(1), 87–91.PubMed

Schmidt, A., Hannah, M. J., & Huttner, W. B. (1997). Synaptic-like microvesicles of neuroendocrine cells originate from a novel compartment that is continuous with the plasma membrane and devoid of transferrin receptor. Journal of Cell Biology, 137(2), 445–458.PubMedCentralPubMed

Schultz, K., Janssen-Bienhold, U., Gundelfinger, E. D., Kreutz, M. R., & Weiler, R. (2004). Calcium-binding protein Caldendrin and CaMKII are localized in spinules of the carp retina. Journal of Comparative Neurology, 479(1), 84–93. doi:10.1002/cne.20314.PubMed

Schuster, T., Krug, M., & Wenzel, J. (1990). Spinules in axospinous synapses of the rat dentate gyrus: Changes in density following long-term potentiation. Brain Research, 523(1), 171–174.PubMed

Sebé-Pedrós, A., Burkhardt, P., Sanchez-Pons, N., Fairclough, S. R., Lang, B. F., King, N., et al. (2013). Insights into the origin of metazoan filopodia and microvilli. Molecular Biology and Evolution, 30(9), 2013–2023. doi:10.1093/molbev/mst110.PubMedCentralPubMed

Shaw, S. R., & Meinertzhagen, I. A. (1986). Evolutionary progression at synaptic connections made by identified homologous neurones. Proceedings of the National Academy of Sciences of the USA, 83(20), 7961–7965.PubMedCentralPubMed

Sherer, N. M., Lehmann, M. J., Jimenez-Soto, L. F., Horensavitz, C., Pypaert, M., & Mothes, W. (2007). Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nature Cell Biology, 9(3), 310–315. doi:10.1038/ncb1544.PubMedCentralPubMed

Sherer, N. M., & Mothes, W. (2008). Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis. Trends in Cell Biology, 18(9), 414–420. doi:10.1016/j.tcb.2008.07.003.PubMedCentralPubMed

Shupliakov, O., Low, P., Grabs, D., Gad, H., Chen, H., David, C., et al. (1997). Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science, 276(5310), 259–263.PubMed

Smith, J. E., Clark, A. W., & Kuster, T. A. (1977). Suppression by elevated calcium of black widow spider venom activity at frog neuromuscular junctions. Journal of Neurocytology, 6(5), 519–539.PubMed

Smith, C. L., Varoqueaux, F., Kittelmann, M., Azzam, R. N., Cooper, B., Winters, C. A., et al. (2014). Novel cell types, neurosecretory cells, and body plan of the early-diverging metazoan Trichoplax adhaerens. Current Biology, 24(14), 1565–1572. doi:10.1016/j.cub.2014.05.046.PubMedCentralPubMed

Sobkowicz, H. M., August, B. K., Slapnick, S. M., & Luthy, D. F. (1998). Terminal dendritic sprouting and reactive synaptogenesis in the postnatal organ of Corti in culture. Journal of Comparative Neurology, 397(2), 213–230.PubMed

Sobkowicz, H. M., Rose, J. E., Scott, G. L., & Levenick, C. V. (1986). Distribution of synaptic ribbons in the developing organ of Corti. Journal of Neurocytology, 15(6), 693–714.PubMed

Sobkowicz, H. M., Slapnick, S. M., & August, B. K. (1999). Apoptosis of inner hair cells caused by laser ablation of their spiral ganglion neurons in cultures of the mouse organ of Corti. Journal of Neurocytology, 28(10–11), 939–954.PubMed

Sobkowicz, H. M., Slapnick, S. M., & August, B. K. (2002). Differentiation of spinous synapses in the mouse organ of corti. Synapse, 45(1), 10–24. doi:10.1002/syn.10080.PubMed

Sobkowicz, H. M., Slapnick, S. M., & August, B. K. (2003). Reciprocal synapses between inner hair cell spines and afferent dendrites in the organ of corti of the mouse. Synapse, 50(1), 53–66. doi:10.1002/syn.10241.PubMed

Sorra, K. E., Fiala, J. C., & Harris, K. M. (1998). Critical assessment of the involvement of perforations, spinules, and spine branching in hippocampal synapse formation. Journal of Comparative Neurology, 398(2), 225–240.PubMed

Spacek, J., & Harris, K. M. (2004). Trans-endocytosis via spinules in adult rat hippocampus. Journal of Neuroscience, 24(17), 4233–4241. doi:10.1523/JNEUROSCI.0287-04.2004.PubMed

Stark, W. S., & Carlson, S. D. (1986). Ultrastructure of capitate projections in the optic neuropil of Diptera. Cell and Tissue Research, 246(3), 481–486.PubMed

Stark, W. S., Sapp, R., & Carlson, S. D. (1989). Ultrastructure of the ocellar visual system in normal and mutant Drosophila melanogaster. Journal of Neurogenetics, 5, 127–153.PubMed

Stewart, M. G., Davies, H. A., Sandi, C., Kraev, I. V., Rogachevsky, V. V., Peddie, C. J., et al. (2005a). Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: A three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities. Neuroscience, 131(1), 43–54. doi:10.1016/j.neuroscience.2004.10.031.PubMed

Stewart, M. G., Medvedev, N. I., Popov, V. I., Schoepfer, R., Davies, H. A., Murphy, K., et al. (2005b). Chemically induced long-term potentiation increases the number of perforated and complex postsynaptic densities but does not alter dendritic spine volume in CA1 of adult mouse hippocampal slices. European Journal of Neuroscience, 21(12), 3368–3378. doi:10.1111/j.1460-9568.2005.04174.x.PubMed

Sukhdeo, S. C., & Sukhdeo, M. V. K. (1994). Mesenchyme cells in Fasciola hepatica (Platyhelminthes): Primitive glia? Tissue and Cell, 26(1), 123–131.PubMed

Tao-Cheng, J. H., Dosemeci, A., Gallant, P. E., Miller, S., Galbraith, J. A., Winters, C. A., et al. (2009). Rapid turnover of spinules at synaptic terminals. Neuroscience, 160(1), 42–50. doi:10.1016/j.neuroscience.2009.02.031.PubMedCentralPubMed

Tarrant, S. B., & Routtenberg, A. (1977). The synaptic spinule in the dendritic spine: Electron microscopic study of the hippocampal dentate gyrus. Tissue and Cell, 9(3), 461–473.PubMed

Tarrant, S. B., & Routtenberg, A. (1979). Postsynaptic membrane and spine apparatus: Proximity in dendritic spines. Neuroscience Letters, 11(3), 289–294.PubMed

Toh, Y., & Kuwabara, M. (1974). Fine structure of the dorsal ocellus of the worker honeybee. Journal of Morphology, 143, 285–306.

Toh, Y., & Kuwabara, M. (1975). Synaptic organization of the fleshfly ocellus. Journal of Neurocytology, 4(3), 271–287.PubMed

Toni, N., Buchs, P. A., Nikonenko, I., Bron, C. R., & Muller, D. (1999). LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature, 402(6760), 421–425. doi:10.1038/46574.PubMed

Trujillo-Cenóz, O. (1965). Some aspects of the structural organization of the intermediate retina of dipterans. Journal of Ultrastructure Research, 13(1), 1–33.PubMed

Ueda, Y. (2014). The role of phosphoinositides in synapse function. Molecular Neurobiology, 50(3), 821–838. doi:10.1007/s12035-014-8768-8.PubMed

Ueda, Y., & Hayashi, Y. (2013). PIP(3) regulates spinule formation in dendritic spines during structural long-term potentiation. Journal of Neuroscience, 33(27), 11040–11047. doi:10.1523/JNEUROSCI.3122-12.2013.PubMedCentralPubMed

Vaughn, J. E. (1989). Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse, 3(3), 255–285. doi:10.1002/syn.890030312.PubMed

Wagner, H. J. (1980). Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas. Journal of Neurocytology, 9(5), 573–590.PubMed

Wagner, H. J., & Djamgoz, M. B. (1993). Spinules: a case for retinal synaptic plasticity. Trends in Neurosciences, 16(6), 201–206.PubMed

Wanner, G., Vogl, K., & Overmann, J. (2008). Ultrastructural characterization of the prokaryotic symbiosis in “Chlorochromatium aggregatum”. Journal of Bacteriology, 190(10), 3721–3730. doi:10.1128/JB.00027-08.PubMedCentralPubMed

Waxman, S. G., Waxman, M., & Pappas, G. D. (1980). Coordinated micropinocytotic activity of adjacent neuronal membranes in mammalian central nervous system. Neuroscience Letters, 20(2), 141–146.PubMed

Weedman, D. L., Pongstaporn, T., & Ryugo, D. K. (1996). Ultrastructural study of the granule cell domain of the cochlear nucleus in rats: Mossy fiber endings and their targets. The Journal of Comparative Neurology, 369(3), 345–360. doi:10.1002/(SICI)1096-9861(19960603)369:3<345:AID-CNE2>3.0.CO;2-5.PubMed

Weiler, R., & Schultz, K. (1993). Ionotropic non-N-methyl-D-aspartate agonists induce retraction of dendritic spinules from retinal horizontal cells. Proceedings of the National Academy of Sciences of the USA, 90(14), 6533–6537.PubMedCentralPubMed

Weiler, R., Schultz, K., & Janssen-Bienhold, U. (1996). Ca(2+)-dependency of spinule plasticity at dendrites of retinal horizontal cells and its possible implication for the functional role of spinules. Vision Research, 36(24), 3891–3900.PubMed

Westfall, J. A. (1970). Ultrastructure of synapses in a primitive coelenterate. Journal of Ultrastructure Research, 32(3), 237–246.PubMed

Westrum, L. E., & Blackstad, T. W. (1962). An electron microscopic study of the stratum radiatum of the rat hippocampus (regio superior, CA 1) with particular emphasis on synaptology. Journal of Comparative Neurology, 119, 281–309.PubMed

Wierenga, C. J., Becker, N., & Bonhoeffer, T. (2008). GABAergic synapses are formed without the involvement of dendritic protrusions. Nature Neuroscience, 11(9), 1044–1052. doi:10.1038/nn.2180.PubMed

Williams, J. B. (1994). Unicellular adhesive secretion glands and other cells in the parenchyma of Temnocephala novaezealandiae (Platyhelminthes, Temnocephaloidea): Intercell relationships and nuclear pockets. New Zealand Journal of Zoology, 21(2), 167–178.

Wood, C. R., & Rosenbaum, J. L. (2015). Ciliary ectosomes: Transmissions from the cell’s antenna. Trends in Cell Biology, 25(5), 276–285.PubMed

Wright, K. A. (1992). Peripheral sensilla of some lower invertebrates: The Platyhelminthes and Nematoda. Microscopy Research and Technique, 22(3), 285–297. doi:10.1002/jemt.1070220306.PubMed

Wright, K. A., & Hui, N. (1976). Post-labial sensory structures on the cecal worm, Heterakis gallinarum. Journal of Parasitology, 62(4), 579–584.PubMed

Yao, P. J., Petralia, R. S., Bushlin, I., Wang, Y., & Furukawa, K. (2005). Synaptic distribution of the endocytic accessory proteins AP180 and CALM. Journal of Comparative Neurology, 481(1), 58–69. doi:10.1002/cne.20362.PubMed

Yoshida, T., Uchigashima, M., Yamasaki, M., Katona, I., Yamazaki, M., Sakimura, K., et al. (2011). Unique inhibitory synapse with particularly rich endocannabinoid signaling machinery on pyramidal neurons in basal amygdaloid nucleus. Proceedings of the National Academy of Sciences of the USA, 108(7), 3059–3064. doi:10.1073/pnas.1012875108.PubMedCentralPubMed

Zhao, H. M., Wenthold, R. J., & Petralia, R. S. (1998). Glutamate receptor targeting to synaptic populations on Purkinje cells is developmentally regulated. Journal of Neuroscience, 18(14), 5517–5528.PubMed

Zimmer, J., Lawrence, J., & Raisman, G. (1982). A quantitative electron microscopic study of synaptic reorganization in the rat medial habenular nucleus after transection of the stria medullaris. Neuroscience, 7(8), 1905–1928.PubMed

Title: Structure, Distribution, and Function of Neuronal/Synaptic Spinules and Related Invaginating Projections
Authors: Ronald S. Petralia
Ya-Xian Wang
Mark P. Mattson
Pamela J. Yao
Publication date: 01-09-2015
Publisher: Springer US
Published in: NeuroMolecular Medicine / Issue 3/2015
Print ISSN: 1535-1084
Electronic ISSN: 1559-1174
DOI: https://doi.org/10.1007/s12017-015-8358-6

At a glance: The STEP trials

Springer Medicine

Structure, Distribution, and Function of Neuronal/Synaptic Spinules and Related Invaginating Projections

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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