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The Journal of Neuroscience, July 25, 2007, 27(30):8149-8156; doi:10.1523/JNEUROSCI.0511-07.2007

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Development/Plasticity/Repair
Protracted Synaptogenesis after Activity-Dependent Spinogenesis in Hippocampal Neurons

U. Valentin Nägerl,¹ German Köstinger,² John C. Anderson,² Kevan A. C. Martin,² and Tobias Bonhoeffer¹

¹Max Planck Institute of Neurobiology, 82152 München-Martinsried, Germany, and ²Institute for Neuroinformatics, University of Zürich and Eidgenössische Technische Hochschule Zürich, CH-8057 Zürich, Switzerland

Correspondence should be addressed to U. Valentin Nägerl, Max Planck Institute of Neurobiology, Am Klopferspitz 18, 82152 München-Martinsried, Germany. Email: naegerl{at}neuro.mpg.de

Activity-dependent morphological plasticity of neurons is central to understanding how the synaptic network of the CNS becomes reconfigured in response to experience. In recent years, several studies have shown that synaptic activation that leads to the induction of long-term potentiation also drives the growth of new dendritic spines, raising the possibility that new synapses are made. We examine this directly by correlating time-lapse two-photon microscopy of newly formed spines on CA1 pyramidal neurons in organotypic hippocampal slices with electron microscopy. Our results show that, whereas spines that are only a few hours old rarely form synapses, older spines, ranging from 15 to 19 h, consistently have ultrastructural hallmarks typical of synapses. This is in agreement with a recent in vivo study that showed that, after a few days, new spines consistently form functional synapses. In addition, our study provides a much more detailed understanding of the first few hours after activity-dependent spinogenesis. Within tens of minutes, physical contacts are formed with existing presynaptic boutons, which slowly, over the course of many hours, mature into new synapses.

Key words: synaptic plasticity; two-photon imaging; correlated electron microscopy; theta-burst stimulation; LTP; spines

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Received Feb. 5, 2007; revised May 18, 2007; accepted June 16, 2007.

Correspondence should be addressed to U. Valentin Nägerl, Max Planck Institute of Neurobiology, Am Klopferspitz 18, 82152 München-Martinsried, Germany. Email: naegerl{at}neuro.mpg.de

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