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This Article Full Text Full Text (PDF) Supplemental Data All Versions of this Article: 585/3/759    most recent jphysiol.2007.138453v1 Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Williams, S. R. Articles by Atkinson, S. E. Search for Related Content PubMed PubMed Citation Articles by Williams, S. R. Articles by Atkinson, S. E. Related Collections Neuroscience

¹ Medical Research Council Laboratory of Molecular Biology, Hills Road, Cambridge CB2 0QH, UK

Information processing in neuronal networks is determined by the use-dependent dynamics of synaptic transmission. Here we characterize the dynamic properties of excitatory synaptic transmission in two major intracortical pathways that target the output neurons of the neocortex, by recording unitary EPSPs from layer 5 pyramidal neurons evoked in response to action potential trains of increasing complexity in presynaptic layer 2/3 or layer 5 pyramidal neurons. We find that layer 2/3 to layer 5 synaptic transmission is dominated by frequency-dependent depression when generated at fixed frequencies of > 10 Hz. Synaptic depression evolved on a spike-by-spike basis in response to action potential trains that possessed a broad range of interspike intervals, but a low mean frequency (10 Hz). Layer 2/3 to layer 2/3 and layer 2/3 to layer 5 synapses were incapable of sustained release during prolonged, complex trains of presynaptic action potential firing (mean frequency, 48 Hz). By contrast, layer 5 to layer 5 synapses operated effectively across a wide range of frequencies, exhibiting increased efficacy at frequencies > 10 Hz. Furthermore, layer 5 to layer 5 synapses sustained release throughout the duration of prolonged, complex spike trains. The use-dependent properties of synaptic transmission could be modulated by pharmacologically changing the probability of release and by induction of long-term depression. The dynamic properties of intracortical excitatory synapses are therefore pathway-specific. We suggest that the synaptic output of layer 5 pyramidal neurons is ideally suited to control the neocortical network across a wide range of frequencies and for sustained periods of time, a behaviour that helps to explain the pivotal role played by layer 5 neurons in the genesis of periods of network ‘up’ states and epileptiform activity in the neocortex.

(Received 12 June 2007; accepted after revision 16 October 2007; first published online 18 October 2007)
Corresponding author S. R. Williams: Neurobiology Division, MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 0QH, UK. Email: srw{at}mrc-lmb.cam.ac.uk