Dendritic Spine Dynamics Regulate the Long-Term Stability of Synaptic Plasticity

Abstract

Long-term synaptic plasticity requires postsynaptic influx of Ca 2ϩ and is accompanied by changes in dendritic spine size. Unless Ca 2ϩ influx mechanisms and spine volume scale proportionally, changes in spine size will modify spine Ca 2ϩ concentrations during subsequent synaptic activation. We show that the relationship between Ca 2ϩ influx and spine volume is a fundamental determinant of synaptic stability. If Ca 2ϩ influx is undercompensated for increases in spine size, then strong synapses are stabilized and synaptic strength distributions have a single peak. In contrast, overcompensation of Ca 2ϩ influx leads to binary, persistent synaptic strengths with double-peaked distributions. Biophysical simulations predict that CA1 pyramidal neuron spines are undercompensating. This unifies experimental findings that weak synapses are more plastic than strong synapses, that synaptic strengths are unimodally distributed, and that potentiation saturates for a given stimulus strength. We conclude that structural plasticity provides a simple, local, and general mechanism that allows dendritic spines to foster both rapid memory formation and persistent memory storage.

Soft-bound Synaptic Plasticity Increases Storage Capacity

“…Interestingly, the spine volume grows substantially as the synapse undergoes potentiation [42]. At first glance this suggests that the spine readies itself for potential further strengthening, but it has been suggested that actually the increase in spine volume reduces the calcium transients, limiting further potentiation, and therefore giving rise to soft-bound plasticity [43], [44].…”

Spine Head Calcium as a Measure of Summed Postsynaptic Activity for Driving Synaptic Plasticity

“…In addition, spine geometry can provide a local control of pCa, such that different synapses will indeed experience different pCa for the same barrage of synaptic input. Changes in spine geometry can act as a modulating factor to synaptic learning, with increasing spine size following LTP acting to stabilize synaptic weights by decreasing pCa at already potentiated synapses (O'Donnell, Nolan, & van Rossum, 2011 …”

Network Control Mechanisms

“…87 Synaptic strength is proposed to be determined, in part, by postsynaptic influx of Ca 2þ , leading to changes in dendritic spine size, 88 and, if these changes are sustained, this can result in long-term synaptic plasticity. 89 "Weak" synapses, such as those found in "conditional multireceptive" brain regions (see Chapter 28), can undergo a much greater degree of increase than synapses that are more stable, such as those seen in primary sensory and motor networks. 90 …”