Spike-Timing–Dependent Synaptic Plasticity and Synaptic Democracy in Dendrites

Abstract

Gidon A, Segev I. Spike-timing-dependent synaptic plasticity and synaptic democracy in dendrites. J Neurophysiol 101: 3226 -3234, 2009. First published April 8, 2009 doi:10.1152/jn.91349.2008. We explored in a computational study the effect of dendrites on excitatory synapses undergoing spike-timing-dependent plasticity (STDP), using both cylindrical dendritic models and reconstructed dendritic trees. We show that even if the initial strength, g peak , of distal synapses is augmented in a location independent manner, the efficacy of distal synapses diminishes following STDP and proximal synapses would eventually dominate. Indeed, proximal synapses always win over distal synapses following linear STDP rule, independent of the initial synaptic strength distribution in the dendritic tree. This effect is more pronounced as the dendritic cable length increases but it does not depend on the dendritic branching structure. Adding a small multiplicative component to the linear STDP rule, whereby already strong synapses tend to be less potentiated than depressed (and vice versa for weak synapses) did partially "save" distal synapses from "dying out." Another successful strategy for balancing the efficacy of distal and proximal synapses following STDP is to increase the upper bound for the synaptic conductance (g max ) with distance from the soma. We conclude by discussing an experiment for assessing which of these possible strategies might actually operate in dendrites. Hebb (1949) introduced his famous postulate for the mechanism that may underlie activity-dependent synaptic plasticity 60 years ago. In the last 10 years, experimental studies have begun to unravel the operation of such a mechanism and it has been shown that, in many neuron types, the precise timing of the pre-versus the postsynaptic spikes play a critical role in determining the efficacy of the synaptic connection between neurons [spike-timing-dependent plasticity (STDP)] (Bell et al. 1997;Bi and Poo 1998;Debanne et al. 1998;Markram et al. 1997;Zhang et al. 1998; reviews by Poo 2006 andNelson 2000). This specific type of synaptic plasticity operates within a time window of tens of milliseconds, and its direction and magnitude are critically determined by the temporal order of the pre-versus the postsynaptic spike. If a synapse is active before the postsynaptic neuron fired a spike (pre before post), the efficacy of this synapse is enhanced; the synapse is weakened for the reverse temporal order (post before pre). Outside of the critical temporal window for STDP, the efficacy of the synapse remains unchanged.These experimental studies were followed by theoretical efforts to understand the biophysical foundation of STDP (Shouval et al. 2002) One interesting question regarding STDP is its role in selectively "configuring" the synaptic efficacy at different dendritic locations. Because neurons are inhomogeneous in their morphology and membrane properties, synaptic contacts at different locations on the dendrite would be influenced by different specific dendr...

Dendritic synapse location and neocortical spike-timing-dependent plasticity

“…In terms of synaptic organization, anti-Hebbian STDP provides a mechanism for retention of distal inputs, re-scaling synaptic strengths in proportion to electrotonic distance and preserving total excitatory drive. This can also be achieved with Hebbian STDP (Gidon and Segev, 2009) if formulated multiplicatively (Figure 5B, top) or if distal synapses have larger maximal peak conductances (Figure 5B, bottom), similar to reported experimental findings in CA1 hippocampal pyramidal cells (Magee and Cook, 2000). …”

Interregional synaptic competition in neurons with multiple STDP-inducing signals

“…2, B and D). This is due to cable filtering, whereby synapses close to the initiation site are more effective at initiating spikes compared with synapses located further away from it (Gidon and Segev 2009).…”

“…Another possible mechanism for achieving synaptic democracy is the anti-Hebbian STDP mechanism as suggested by Rumsey andAbbott (2004, 2006). Synaptic democracy could also be maintained throughout the dendritic tree by scaling the upper limit of synaptic conductance with distance from the soma (Gidon and Segev 2009) or by having different forms of metaplasticity (Abraham and Bear 1996) at different cell regions.…”

The Languages of Neurons: An Analysis of Coding Mechanisms by Which Neurons Communicate, Learn and Store Information

“…As such, synapses are particularly important sites in information transfer. However, it has been proposed that it is not synapses alone, but the entire dendritic-synaptic-dendritic field between neurons that plays an important role in inter-neuronal communication [24][25][26][27][28]. If only one dendritic pathway and one synapse were involved between two neurons, the original message might be received by the efferent neuron in its original spike-pause encoded word form, but even in such a case, since the dendritic-synaptic interface is a dynamic and continuously regenerating system, it could also be modulated by changes in single pathway elements.…”

“…This inter-neuronal modulation step is of importance in that it allows brain activities of all kinds and at all levels, whether from external sensors such as eyes and ears, or internally generated as "thought processes" to result in changes in neuronal words in response to increased or decreased use of particular neuronal pathways. The concept of the diversity of dendritic excitability that arise from variations in dendrite morphology and channel distribution between neurons as illustrated in Figure 3, and the potential role of such diversity in information processing and memory storage in neuronal networks have been considered in detail [24,25,27,28] and extensively reviewed [26].…”