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The Journal of Neuroscience, May 4, 2005, 25(18):4605-4615; doi:10.1523/JNEUROSCI.3803-04.2005

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Development/Plasticity/Repair
Activation of Early Silent Synapses by Spontaneous Synchronous Network Activity Limits the Range of Neocortical Connections

Thomas Voigt, Thoralf Opitz, and Ana Dolabela de Lima

Department of Developmental Physiology, Otto-von-Guericke University, Institute of Physiology, 39120 Magdeburg, Germany

During the early development of neocortical networks, many glutamatergic synapses lack AMPA receptors and are physiologically silent. We show in neocortical cultures that spontaneous synchronous network activity is able to convert silent synapses to active synapses by the incorporation of AMPA receptors into synaptic complexes throughout the network within a few minutes. To test the effect of synaptic activation on the connectivity of neuronal populations, we created separated neuronal networks that could innervate each other. We allowed outgrowing axons to invade the neighboring network either before or after the onset of synchronous network activity. In the first case, both subnetworks connected to each other and synchronized their activity, whereas in the second case, axonal connections failed to form and network activity did not synchronize between compartments. We conclude that early spontaneous synchronous network activity triggers a global AMPAfication of immature synapses, which in turn prevents later-arriving axons from forming afferent connections. This activity-dependent process may set the range of corticocortical connections during early network development before experience-dependent mechanisms begin elaborating the mature layout of the neocortical connections and modules.

Key words: cerebral cortex; cell culture; development; glutamate receptors; silent synapses; synchronous activity

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Received Sep 14, 2004; revised March 23, 2005; accepted March 26, 2005.

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