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Presynaptic Efficacy Directs Normalization of Synaptic Strength in Layer 2/3 Rat Neocortex After Paired Activity

¹The University Laboratory of Physiology, Oxford University, Oxford; ²The School of Biosciences, Cardiff University, Cardiff; and ³Centre for Neuroscience Research, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, United Kingdom

Submitted 22 December 2006; accepted in final form 25 January 2007

Paired neuronal activity is known to induce changes in synaptic strength that result in the synapse in question having different properties to unmodified synapses. Here we show that in layer 2/3 excitatory connections in young adult rat cortex paired activity acts to normalize the strength and quantal parameters of connections. Paired action potential firing produces long-term potentiation in only a third of connections, whereas a third remain with their amplitude unchanged and a third exhibit long-term depression. Furthermore, the direction of plasticity can be predicted by the initial strength of the connection: weak connections potentiate and strong connections depress. A quantal analysis reveals that changes in synaptic efficacy were predominantly presynaptic in locus and that the key determinant of the direction and magnitude of synaptic modification was the initial release probability (P_r) of the synapse, which correlated inversely with change in P_r after pairing. Furthermore, distal synapses also exhibited larger potentiations including postsynaptic increases in efficacy, whereas more proximal inputs did not. This may represent a means by which distal synapses preferentially increase their efficacy to achieve equal weighting at the soma. Paired activity thus acts to normalize synaptic strength, by both pre- and postsynaptic mechanisms.

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