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.