Synaptogenesis in the CNS: An Odyssey from Wiring Together to Firing Together

Munno, David W.; Syed, Naweed I.

doi:10.1113/jphysiol.2003.045062

Cited by 86Neuroscience and Neuropharmacology ResearchAxon Guidance and Neuronal SignalingNeurogenesis and neuroplasticity mechanisms

Synaptogenesis in the CNS: An Odyssey from Wiring Together to Firing Together

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Munno, David W., Syed, Naweed I.·2003·The Journal of Physiology

DOI 10.1113/jphysiol.2003.045062PMC PMC2343306

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Abstract

To acquire a better comprehension of nervous system function, it is imperative to understand how synapses are assembled during development and subsequently altered throughout life. Despite recent advances in the fields of neurodevelopment and synaptic plasticity, relatively little is known about the mechanisms that guide synapse formation in the central nervous system (CNS). Although many structural components of the synaptic machinery are pre-assembled prior to the arrival of growth cones at the site of their potential targets, innumerable changes, central to the proper wiring of the brain, must subsequently take place through contact-mediated cell-cell communications. Identification of such signalling molecules and a characterization of various events underlying synaptogenesis are pivotal to our understanding of how a brain cell completes its odyssey from "wiring together to firing together". Here we attempt to provide a comprehensive overview that pertains directly to the cellular and molecular mechanisms of selection, formation and refinement of synapses during the development of the CNS in both vertebrates and invertebrates.

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The homophilic adhesion molecules cadherins are involved in target recognition and synaptic specificity.
“The homophilic adhesion molecules cadherins are involved in target recognition and synaptic specificity [79].”
From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [79]

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In VitroSynaptogenesis between the Somata of IdentifiedLymnaeaNeurons Requires Protein Synthesis But Not Extrinsic Growth Factors or Substrate Adhesion Molecules
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Semaphorin Signaling
Yu, H., & Kolodkin, A. L. (1999) · Neuron · doi:10.1016/s0896-6273(00)80672-8 · Cited by 89 · see citing works
Neuron‐specific growth cone properties as seen in identified neurons of Helisoma
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Casein kinase II phosphorylates the synaptic vesicle protein p65
Bennett, M. K., Miller, K., & Scheller, R. H. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-04-01701.1993 · Cited by 85 · see citing works
Neurotransmitters and neurodevelopment. Role of dopamine in neurite outgrowth, target selection and specific synapse formation.
Spencer, G. E., Klumperman, J., & Syed, N. I. (1998) · PubMed · Cited by 81 · see citing works
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The formation of chemical synapses between cell-cultured neuronal somata
Haydon, P. G. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-03-01032.1988 · Cited by 80 · see citing works
Excitatory Synaptogenesis between IdentifiedLymnaeaNeurons Requires Extrinsic Trophic Factors and Is Mediated by Receptor Tyrosine Kinases
Hamakawa, T., Woodin, M. A., Bjorgum, M. C., Painter, S. D., Takasaki, M., Lukowiak, K., Nagle, G. T., & Syed, N. I. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09306.1999 · Cited by 78 · see citing works
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Spontaneous Acetylcholine Secretion from Developing Growth Cones ofDrosophilaCentral Neurons in Culture: Effects of cAMP-Pathway Mutations
Yao, W.-D., Rusch, J., Poo, M., & Wu, C. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-07-02626.2000 · Cited by 77 · see citing works
Knowing a Nascent Synapse When You See It
Ahmari, S. E., & Smith, S. J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00685-2 · Cited by 72 · see citing works
GABA release from mouse axonal growth cones
Gao, X., & van den Pol, A. N. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-1-00629.x · Cited by 72 · see citing works
Synapse Formation in the Absence of Cell Bodies Requires Protein Synthesis
Schacher, S., & Wu, F. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-05-01831.2002 · Cited by 64 · see citing works
Anterograde Transport and Trophic Actions of BDNF and NT-4/5 in the Developing Rat Visual System
Spalding, K. L., Tan, M. M. L., Hendry, I. A., & Harvey, A. R. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2001.1097 · Cited by 59 · see citing works
Neuroligation: building synapses around the neurexin–neuroligin link
Rao, A., Harms, K. J., & Craig, A. M. (2000) · Nature Neuroscience · doi:10.1038/77636 · Cited by 53 · see citing works
Transmitter–Receptor Interactions between Growth Cones of IdentifiedLymnaeaNeurons Determine Target Cell SelectionIn Vitro
Spencer, G. E., Lukowiak, K., & Syed, N. I. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08077.2000 · Cited by 51 · see citing works
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Formation and modulation of chemical connections: Evoked acetylcholine release from growth cones and neurites of specific identified neurons
Haydon, P. G., & Zoran, M. J. (1989) · Neuron · doi:10.1016/0896-6273(89)90194-3 · Cited by 50 · see citing works
Trophic Factor-Induced Plasticity of Synaptic Connections Between Identified Lymnaea NeuronsPreprint
Woodin, M. A., Hamakawa, T., Takasaki, M., Lukowiak, K., & Syed, N. I. (1999) · Learning & Memory · doi:10.1101/lm.6.3.307 · Cited by 49 · see citing works
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Trophic Factor-Induced Excitatory Synaptogenesis Involves Postsynaptic Modulation of Nicotinic Acetylcholine Receptors
Woodin, M. A., Munno, D. W., & Syed, N. I. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-00505.2002 · Cited by 48 · see citing works
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Reconstruction of neuronal networks in culture
Bulloch, A. G., & Syed, N. I. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90004-r · Cited by 48 · see citing works
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Silencing the Siren
Giger, R. J., & Kolodkin, A. L. (2001) · Cell · doi:10.1016/s0092-8674(01)00290-2 · Cited by 45 · see citing works
Synapse formation and function: Insights from identified leech neurons in culture
Fernández‐de‐Miguel, F., & Drapeau, P. (1995) · Journal of Neurobiology · doi:10.1002/neu.480270309 · Cited by 43 · see citing works
The Middle and the End
Vactor, D. V., & Flanagan, J. G. (1999) · Neuron · doi:10.1016/s0896-6273(00)80723-0 · Cited by 40 · see citing works
Genetic dissection of synaptic transmission in Drosophila
Wu, M. N., & Bellen, H. J. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80081-5 · Cited by 39 · see citing works
Development of Ca2+ hotspots between Lymnaea neurons during synaptogenesis
Feng, Z., Grigoriev, N. G., Munno, D. W., Lukowiak, K., MacVicar, B. A., Goldberg, J. I., & Syed, N. I. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013125 · Cited by 37 · see citing works
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Synapse formation: If it looks like a duck and quacks like a duck…
Cantallops, I., & Cline, H. T. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00663-1 · Cited by 31 · see citing works
Synapse Number and Synaptic Efficacy Are Regulated by Presynaptic cAMP and Protein Kinase A
Munno, D. W., Prince, D. J., & Syed, N. I. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-10-04146.2003 · Cited by 29 · see citing works
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Differential effects of cortical neurotrophic factors on development of lateral geniculate nucleus and superior colliculus neurons: anterograde and retrograde actions
Wahle, P., Cristo, G. D., Schwerdtfeger, G., Engelhardt, M., Berardi, N., & Maffei, L. (2003) · Development · doi:10.1242/dev.00224 · Cited by 29 · see citing works
Conserved Cues for Axon and Dendrite Growth in the Developing Cortex
McAllister, A. K. (2002) · Neuron · doi:10.1016/s0896-6273(01)00577-3 · Cited by 27 · see citing works
Synapse Formation Between Isolated Axons Requires Presynaptic Soma and Redistribution of Postsynaptic AChRs
Wiersma-Meems, R., Munno, D. W., van Minnen, J., & Syed, N. I. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00898.2002 · Cited by 23 · see citing works
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Synaptic Precedence During Synapse Formation Between Reciprocally Connected Neurons Involves Transmitter-Receptor Interactions and AA Metabolites
Lovell, P. V., McMahon, B. R., & Syed, N. I. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.3.1328 · Cited by 15 · see citing works
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The neocortical microcircuit as a tabula rasa
Kalisman, N., Silberberg, G., & Markram, H. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407088102 · Cited by 200 · see citing works
Leptin promotes rapid dynamic changes in hippocampal dendritic morphology
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General Anesthesia Causes Long-Lasting Disturbances in the Ultrastructural Properties of Developing Synapses in Young Rats
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Synapse formation: from cellular and molecular mechanisms to neurodevelopmental and neurodegenerative disorders
Batool, S., Raza, H., Zaidi, J., Riaz, S., Hasan, S., & Syed, N. I. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00833.2018 · Cited by 163 · see citing works
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A new hypothesis of drug refractory epilepsy: Neural network hypothesis
Fang, M., Xi, Z., Wu, Y. F., & Wang, X. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.02.039 · Cited by 118 · see citing works
Synaptic input to brain tumors: clinical implications
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In VitroStudies of Neuronal Networks and Synaptic Plasticity in Invertebrates and in Mammals Using Multielectrode Arrays
Massobrio, P., Tessadori, J., Chiappalone, M., & Ghirardi, M. (2015) · Neural Plasticity · doi:10.1155/2015/196195 · Cited by 87 · see citing works
The transition to experiencing: I. Limited learning and limited experiencing.
Ginsburg, S., & Jablonka, E. (2007) · Biological Theory · doi:10.1162/biot.2007.2.3.218 · Cited by 83 · see citing works
Comparative biology of pain: What invertebrates can tell us about how nociception works
Burrell, B. D. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00600.2016 · Cited by 79 · see citing works
Compound selection for in vitro modeling of developmental neurotoxicity
Kadereit, S. (2012) · Frontiers in bioscience · doi:10.2741/4064 · Cited by 74 · see citing works
Acoustofluidic assembly of 3D neurospheroids to model Alzheimer's disease
Cai, H., Ao, Z., Hu, L., Moon, Y., Wu, Z., Lu, H.-C., Kim, J., & Guo, F. (2020) · The Analyst · doi:10.1039/d0an01373k · Cited by 70 · see citing works
Protocadherin α (PCDHA) as a novel susceptibility gene for autism
Anitha, A., Thanseem, I., Nakamura, K., Yamada, K., Iwayama, Y., Toyota, T., Iwata, Y., Suzuki, K., Sugiyama, T., Tsujii, M., et al. (2013) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.120058 · Cited by 63 · see citing works
Dynamic Characterization of Structural, Molecular, and Electrophysiological Phenotypes of Human-Induced Pluripotent Stem Cell-Derived Cerebral Organoids, and Comparison with Fetal and Adult Gene Profiles
Logan, S., Arzua, T., Yan, Y., Jiang, C., Liu, X., Yu, L., Liu, Q.-S., & Bai, X. (2020) · Cells · doi:10.3390/cells9051301 · Cited by 62 · see citing works
Developing a Psychologically Inspired Cognitive Architecture for Robotic Control: The Symbolic and Subsymbolic Robotic Intelligence Control System (SS-RICS)
Kelley, T. D. (2006) · International Journal of Advanced Robotic Systems · doi:10.5772/5736 · Cited by 60 · see citing works
Axon and dendrite geography predict the specificity of synaptic connections in a functioning spinal cord network
Li, W., Cooke, T., Sautois, B., Soffe, S. R., Borisyuk, R. M., & Roberts, A. (2007) · Neural Development · doi:10.1186/1749-8104-2-17 · Cited by 60 · see citing works
Leptin regulation of neuronal morphology and hippocampal synaptic function
Harvey, J. (2013) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2013.00003 · Cited by 56 · see citing works
Bisphenol-A rapidly promotes dynamic changes in hippocampal dendritic morphology through estrogen receptor-mediated pathway by concomitant phosphorylation of NMDA receptor subunit NR2B
Xu, X., Ye, Y., Li, T., Chen, L., Dong, T., Luo, Q., & Lü, M. (2010) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2010.09.007 · Cited by 52 · see citing works
Taurine Promotes Neurite Outgrowth and Synapse Development of Both Vertebrate and Invertebrate Central Neurons
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An industry perspective: A streamlined screening strategy using alternative models for chemical assessment of developmental neurotoxicity
Li, J., Settivari, R. S., LeBaron, M. J., & Marty, M. S. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.02.010 · Cited by 43 · see citing works
Biohybrid neural interfaces: improving the biological integration of neural implants
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Memristor-Based Circuit Design for Neuron With Homeostatic Plasticity
Shi, X., Zeng, Z., Yang, L., & Huang, Y. (2018) · IEEE Transactions on Emerging Topics in Computational Intelligence · doi:10.1109/tetci.2018.2829914 · Cited by 38 · see citing works
Glutamate receptor-mediated regulation of c-fos expression in cultured microglia
Eun, S.-Y., Hong, Y. H., Kim, E., Jeon, H., Suh, Y. H., Lee, J. E., Jo, C., Jo, S. A., & Kim, J. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.10.035 · Cited by 37 · see citing works
Influence of serotonin receptor 2A His452Tyr polymorphism on brain temporal structures: a volumetric MR study
Filippini, N., Scassellati, C., Boccardi, M., Pievani, M., Testa, C., Bocchio‐Chiavetto, L., Frisoni, G. B., & Gennarelli, M. (2006) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201573 · Cited by 37 · see citing works
Spontaneous neuronal burst discharges as dependent and independent variables in the maturation of cerebral cortex tissue cultured in vitro: A review of activity-dependent studies in live ‘model’ systems for the development of intrinsically generated bioelectric slow-wave sleep patterns
Corner, M. A. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.08.001 · Cited by 37 · see citing works
Minireview: Food for Thought: Regulation of Synaptic Function by Metabolic Hormones
McGregor, G., Malekizadeh, Y., & Harvey, J. (2014) · Molecular Endocrinology · doi:10.1210/me.2014-1328 · Cited by 33 · see citing works
A Developmental Approach to Predicting Neuronal Connectivity from Small Biological Datasets: A Gradient-Based Neuron Growth Model
Borisyuk, R. M., Azad, A. K. A., Conte, D., Roberts, A., & Soffe, S. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089461 · Cited by 33 · see citing works
Chronic activation of the D2 dopamine autoreceptor inhibits synaptogenesis in mesencephalic dopaminergic neurons in vitro
Fasano, C., Poirier, A., DesGroseillers, L., & Trudeau, L. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06450.x · Cited by 32 · see citing works
Network stability through homeostatic scaling of excitatory and inhibitory synapses following inactivity in CA3 of rat organotypic hippocampal slice cultures
Buckby, L. E., Jensen, T. P., Smith, P. J. E., & Empson, R. M. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.01.009 · Cited by 32 · see citing works
Physiological consequences of selective suppression of synaptic transmission in developing cerebral cortical networks in vitro: Differential effects on intrinsically generated bioelectric discharges in a living ‘model’ system for slow-wave sleep activity
Corner, M. A., Baker, R. E., & VANPELT, J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.06.008 · Cited by 29 · see citing works
Syncrip/hnRNP Q is required for activity-induced Msp300/Nesprin-1 expression and new synapse formation
Titlow, J., Robertson, F., Järvelin, A. I., Ish‐Horowicz, D., Smith, C., Gratton, E., & Davis, I. (2020) · The Journal of Cell Biology · doi:10.1083/jcb.201903135 · Cited by 29 · see citing works
Neuronal networks and synaptic plasticity: understanding complex system dynamics by interfacing neurons with silicon technologies
Colicos, M. A., & Syed, N. I. (2006) · Journal of Experimental Biology · doi:10.1242/jeb.02163 · Cited by 28 · see citing works
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Transcriptional repression of PTEN in neural cells using CRISPR/dCas9 epigenetic editing
Moses, C., Hodgetts, S. I., Nugent, F., Ben-Ary, G., Park, K. K., Blancafort, P., & Harvey, A. R. (2020) · Scientific Reports · doi:10.1038/s41598-020-68257-y · Cited by 27 · see citing works
Mitotically heritable effects of BMAA on striatal neural stem cell proliferation and differentiation
Pierozan, P., & Karlsson, O. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1710-2 · Cited by 27 · see citing works
State of the art paper Deep brain stimulation for refractory epilepsy
Tykocki, T., Mandat, T. S., Kornakiewicz, A., Koziara, H. M., & Nauman, P. (2012) · Archives of Medical Science · doi:10.5114/aoms.2012.31135 · Cited by 26 · see citing works
Long-term Exposure to Local but Not Inhalation Anesthetics Affects Neurite Regeneration and Synapse Formation between Identified Lymnaea Neurons
Onizuka, S., Takasaki, M., & Syed, N. I. (2005) · Anesthesiology · doi:10.1097/00000542-200502000-00018 · Cited by 26 · see citing works
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Trophic Factor-Induced Intracellular Calcium Oscillations Are Required for the Expression of Postsynaptic Acetylcholine Receptors during Synapse Formation betweenLymnaeaNeurons
Xu, F., Hennessy, D. A., Lee, T. K. M., & Syed, N. I. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4682-08.2009 · Cited by 25 · see citing works
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Inhibition of Neurotransmitter Release by a Nonphysiological Target Requires Protein Synthesis and Involves cAMP-Dependent and Mitogen-Activated Protein Kinases
Ghirardi, M., Benfenati, F., Giovedı̀, S., Fiumara, F., Milanese, C., & Montarolo, P. G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5671-03.2004 · Cited by 22 · see citing works
MicroRNAs and synapse turnover in Alzheimer’s disease
Dalal, S., Ramirez-Gomez, J., Sharma, B., Devara, D., & Kumar, S. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102377 · Cited by 21 · see citing works
In vitro formation and activity-dependent plasticity of synapses between Helix neurons involved in the neural control of feeding and withdrawal behaviors
Fiumara, F., Leitinger, G., Milanese, C., Montarolo, P. G., & Ghirardi, M. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.021 · Cited by 21 · see citing works
Rational Design and Acoustic Assembly of Human Cerebral Cortex‐Like Microtissues from hiPSC‐Derived Neural Progenitors and Neurons
Wang, J., Qiao, H., Wang, Z., Zhao, W., Chen, T., Li, B., Zhu, L., Chen, S., Gu, L., Wu, Y., et al. (2023) · Advanced Materials · doi:10.1002/adma.202210631 · Cited by 20 · see citing works
Recordings of cultured neurons and synaptic activity using patch-clamp chips
Martina, M., Luk, C., Py, C., Martinez, D., Comas, T., Monette, R., Denhoff, M. W., Syed, N. I., & Mealing, G. A. R. (2011) · Journal of Neural Engineering · doi:10.1088/1741-2560/8/3/034002 · Cited by 19 · see citing works
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Fluorescence imaging of synapse dynamics in normal circuit maturation and in developmental disorders
Okabe, S. (2017) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.93.029 · Cited by 19 · see citing works
The Role of Dynamic miRISC During Neuronal Development
Nawalpuri, B., Ravindran, S., & Muddashetty, R. S. (2020) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2020.00008 · Cited by 19 · see citing works
Identification of neurotoxicology (NT)/developmental neurotoxicology (DNT) adverse outcome pathways and key event linkages with in vitro DNT screening assays
Pitzer, E. M., Shafer, T. J., & Herr, D. W. (2023) · NeuroToxicology · doi:10.1016/j.neuro.2023.10.007 · Cited by 18 · see citing works
Neuropsychological approaches to epileptic encephalopathies
Filippini, M., Arzimanoglou, A. A., & Gobbi, G. (2013) · Epilepsia · doi:10.1111/epi.12422 · Cited by 17 · see citing works
Molluscan neurons in culture: shedding light on synapse formation and plasticity
Schmold, N., & Syed, N. I. (2012) · Journal of Molecular Histology · doi:10.1007/s10735-012-9398-y · Cited by 16 · see citing works
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Maternal dietary loads of alpha-tocopherol increase synapse density and glial synaptic coverage in the hippocampus of adult offspring
Salucci, S., Ambrogini, P., Lattanzi, D., Betti, M., Gobbi, P., Galati, C., Galli, F., Cuppini, R., & Minelli, A. (2014) · European Journal of Histochemistry · doi:10.4081/ejh.2014.2355 · Cited by 16 · see citing works
Possible interplay between the theories of pharmacoresistant epilepsy
Juvale, I. I. A., & Has, A. T. C. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.15079 · Cited by 15 · see citing works
Neuronal growth and synaptogenesis are inhibited by prenatal methamphetamine exposure leading to memory impairment in adolescent and adult mice
Benya-aphikul, H., Pongrakhananon, V., Chetprayoon, P., Sooksawate, T., & Rodsiri, R. (2021) · Toxicology Letters · doi:10.1016/j.toxlet.2021.08.012 · Cited by 14 · see citing works
Anatomically Detailed and Large-Scale Simulations Studying Synapse Loss and Synchrony Using NeuroBox
Breit, M., Stepniewski, M., Grein, S., Gottmann, P., Reinhardt, L., & Queisser, G. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00008 · Cited by 12 · see citing works
Adverse Outcome Pathway on chronic binding of antagonist to N-methyl-D-aspartate receptors (NMDARs) during brain development induces impairment of learning and memory abilities
Sachana, M., Munn, S., & Bal‐Price, A. (2016) · OECD series on adverse outcome pathways · doi:10.1787/5jlsqs5hcrmq-en · Cited by 11 · see citing works
Adverse Outcome Pathway on inhibition of Na+/I- symporter (NIS) leads to learning and memory impairment
Rolaki, A., Pistollato, F., Munn, S., & Bal‐Price, A. (2019) · OECD series on adverse outcome pathways · doi:10.1787/7ca86a34-en · Cited by 11 · see citing works
Spatial transcriptomics map of the embryonic mouse brain – a tool to explore neurogenesis
Marco, B. D., Vázquez-Marín, J., Monyer, H., Centanin, L., & Alfonso, J. (2023) · Biology Open · doi:10.1242/bio.060151 · Cited by 8 · see citing works
Neuronal Somata and Extrasomal Compartments Play Distinct Roles during Synapse Formation betweenLymnaeaNeurons
Xu, F., Luk, C., Wiersma-Meems, R., Baehre, K., Herman, C., Zaidi, W., Wong, N., & Syed, N. I. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1651-14.2014 · Cited by 7 · see citing works
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Identification of amino acid residues of nerve growth factor important for neurite outgrowth in human dorsal root ganglion neurons
Dahlström, M., Nordvall, G., Sundström, E., Åkesson, E., Tegerstedt, G., Eriksdotter, M., & Forsell, P. K. A. L. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14513 · Cited by 7 · see citing works
Molecular Physiology of the Neuronal Synapse
Ramírez-Expósito, M. J., Cueto-Ureña, C., & Martínez-Martos, J. M. (2026) · Current Issues in Molecular Biology · doi:10.3390/cimb48010088 · Cited by 6 · see citing works
“The homophilic adhesion molecules cadherins are involved in target recognition and synaptic specificity [79].”
Transplantation and restoration of functional synapses between an identified neuron and its targets in the intact brain of Lymnaea stagnalis
Lee, T. K. M., & Syed, N. I. (2003) · Synapse · doi:10.1002/syn.10295 · Cited by 6 · see citing works
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Appearance of LFA-1 in the initial stage of synaptogenesis of developing hippocampal neurons
Wakabayashi, Y., Tsujimura, A., Matsuda, K., Yoshimura, N., & Kawata, M. (2008) · Archivum histologicum japonicum · doi:10.1679/aohc.71.23 · Cited by 6 · see citing works
In Vitro Assays of Neurite Outgrowth and Synapse Formation Using Thermoplasmonic Ablation Technique
Hong, N., & Nam, Y. (2023) · BioChip Journal · doi:10.1007/s13206-023-00121-3 · Cited by 5 · see citing works
Characterization of a Fatty Acid Amide Hydrolase (FAAH) in Hirudo Verbana
Kabeiseman, E. J., Paulsen, R. T., & Burrell, B. D. (2024) · Neurochemical Research · doi:10.1007/s11064-024-04216-7 · Cited by 5 · see citing works
Dexmedetomidine Pre-Treatment of Neonatal Rats Prevents Sevoflurane-Induced Deficits in Learning and Memory in the Adult Animals
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Authors: Munno, D. W., & Syed, N. I.
Affiliations: University of Calgary (CA)
Corresponding author: Syed, Naweed I.
ORCID: Syed, Naweed I.
Venue: The Journal of Physiology
Publisher: Wiley
Published: 2003-10
Volume: 552
Issue: 1
Pages: 1-11
ISSN: 0022-3751 (ISSN-L)
1469-7793
DOI: 10.1113/jphysiol.2003.045062
PMC: PMC2343306
OpenAlex: W2161440653
Cited by: 86
References: 122
Citations by year: 2026: 1 · 2025: 2 · 2024: 4 · 2023: 6 · 2022: 1 · 2021: 2 · 2020: 10 · 2019: 6 · 2018: 1 · 2017: 3 · 2016: 2 · 2015: 3 · 2014: 4 · 2013: 4 · 2012: 6
FWCI: 0.38
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Physiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: synaptogenesis, central nervous system development, synaptic plasticity, growth cones, synapse refinement, neural circuit wiring, brain development, vertebrates, invertebrates
MeSH terms: Animals, Central Nervous System, Humans, Neural Pathways, Neurons, Synapses

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Synaptogenesis in the CNS: An Odyssey from Wiring Together to Firing Together

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