Synaptic plasticity depends on dendritic location and input origin in layer 5 neurons
Per Jesper Sjöström*, Kazuo Kitamura, and Michael Hausser
Wolfson Institute for Biomedical Research, University College London, London WC1E 6BT, UK
Backpropagating action potentials (BPAPs) and dendritic spikes propagate decrementally, creating functional dendritic compartments. The importance of BPAPs for the induction of synaptic plasticity suggests that the rules for plasticity induction may depend on dendritic location. We compared synaptic plasticity for inputs at different locations on the dendritic tree of cortical layer 5 (L5) pyramidal neurons.
Quadruple somatic recordings were used to find connections between L5 and L2/3 pyramidal cells at 34°C in visual cortical slices. As expected, unitary L2/3-to-L5 synapses were more distal than L5-to-L5 synapses, as determined by EPSP 20-80% risetime: 2.0±0.4 ms vs 1.4±0.2 ms respectively (p<0.01). L5-L5 connections exhibited robust timing-dependent LTP (after/before = 150±9%, n = 13; tLTP: 5 spikes at 50 Hz, +10 ms interval). The same protocol, however, evoked no LTP at the more distal L2/3-to-L5 synapses (110±5%, n = 7, p<0.05).
To see if sufficiently large EPSPs rescue distal tLTP, we stimulated extracellularly in cortical L1 to evoke distal EPSPs (rise time 4.7±0.4 ms) of either indistinguishable (0.5±0.1 mV, n=5, p=0.8) or significantly larger (2.6±0.3 mV, n=7, p<0.05) amplitude than unitary L2/3-to-L5 connections (0.6±0.3 mV, n=7). Large (140±9%, p<0.05), but not small (90±8%), EPSPs gave rise to LTP. Large distal EPSPs did not produce LTP on their own (73±5%, n = 3; p<0.01): BPAPs are thus necessary but not sufficient for distal dendritic tLTP.
In conclusion, tLTP induction and input cooperativity depend on dendritic location. Our findings may be explained by supralinear interactions between EPSPs and BPAPs in the distal apical dendrite. Since proximal inputs onto basal dendrites originate locally, but distal tuft inputs originate from higher cortical areas, our results also demonstrate an input dependence of LTP that may have important functional implications.
Supported by the Wellcome Trust, EU, JSPS and Gatsby Foundation.