Heterosynaptic plasticity-induced modulation of synapses

Abstract

Plasticity is a common feature of synapses that is stated in different ways and occurs through several mechanisms. The regular action of the brain needs to be balanced in several neuronal and synaptic features, one of which is synaptic plasticity. The different homeostatic processes, including the balance between excitation/inhibition or homeostasis of synaptic weights at the single-neuron level, may obtain this. Homosynaptic Hebbian-type plasticity causes associative alterations of synapses. Both homosynaptic and heterosynaptic plasticity characterize the corresponding aspects of adjustable synapses, and both are essential for the regular action of neural systems and their plastic synapses.In this review, we will compare homo- and heterosynaptic plasticity and the main factors affecting the direction of plastic changes. This review paper will also discuss the diverse functions of the different kinds of heterosynaptic plasticity and their properties. We argue that a complementary system of heterosynaptic plasticity demonstrates an essential cellular constituent for homeostatic modulation of synaptic weights and neuronal activity.

Keywords: Dynamics; Heterosynaptic plasticity; Homosynaptic plasticity; Synaptic weight.

Fig. 1

Multiple types of plasticity in neural synapses. A A schematic illustration of plasticity induction with its homo- and heterosynaptic pathways. Homosynaptic LTP (blue) induced by tetanus of input is associated with heterosynaptic LTD (black). B Heterosynaptic plasticity induction by postsynaptic tetanus, evoked by depolarizing pulses without pre-synaptic stimulation. C Mexican-hat profile of plasticity shows LTP induction by tetanus + postsynaptic depolarization at a set of synapses associated with a weaker heterosynaptic LTP at adjacent inputs and heterosynaptic LTD at inputs farther away (from Turrigiano et al., 1998)

Fig. 2

Persistent synaptic plasticity triggered by theta-burst stimulation (TBS). The schematic diagram of TBS application at synapses between layer 2/3 and corticogeniculate cells (CG) of layer 6 (A) and at synapses of white matter to CG cells in the visual cortex (B). C The graphs represent Hom-LTP of L2/3-evoked EPSPs (top) and het-LTD of WM-evoked EPSPs (bottom) triggered by TBS of the LII/III site. The means of EPSP slopes have been normalized to the control values 10–0 min before TBS for 14 cells as plotted against time. Circles and vertical bars indicate mean ± SEM. SEMs smaller than circles are not represented. The arrowheads below each plot exhibit the timing of TBS. D The graphs represent Hom-LTP of WM-evoked EPSPs initiated by TBS of the WM site and het-LTD of L2/3-evoked EPSPs (from Arami et al. [23])

Fig. 3

Determinants of the direction of synaptic plasticity. A The high and low frequency of tetanization determines the kind of plasticity. B Activation of the synapses 10–20 ms before or after the firing of the postsynaptic cell leads to the induction of LTP or LTD, respectively. C High and minor augmentation of [Ca²⁺]_in could induce LTP and LTD, respectively. D Weak inputs (light green input) with low initial release probability (RP) were classically potentiated, while strong inputs (dark green input) with a high initial release probability were typically depressed or did not alter (from Turrigiano et al., 1998)

Fig. 4

The effect of spatial distribution and sign of homosynaptic plasticity on the direction of synaptic plasticity. A Inducing LTP at a fraction of synapses was associated with a weaker heterosynaptic LTP at adjacent distances and heterosynaptic LTD at more distant inputs. B Heterosynaptic plasticity with the same homosynaptic plasticity is induced at short distances, while those of opposite signs have been induced further away from the focus of activation

Fig. 5

History-dependency of synaptic plasticity. Weak synaptic inputs with low release probability which have undergone depression in the past have a stronger disposition for potentiation. Strong synapses with a high release probability, which have been potentiated recently, show a higher tendency for depression

Fig. 6

Homosynaptic and heterosynaptic changes in long-lasting plasticity. A All the required events for synaptic strengthening or weakening arise from the same synapse in homosynaptic plasticity. These alterations may cause an enhancement (homosynaptic facilitation) or a reduction in synaptic strength (homosynaptic depression). B The firing of a third neuron, a modulatory interneuron whose terminals end on the synapse, can adjust the strength of the specific synapse. These alterations may cause a rise (heterosynaptic, modulatory facilitation) or a decline (heterosynaptic inhibition) in synaptic strength (from Bailey et al. [77])