Target-cell-specific short-term plasticity in local circuits

Abstract

Short-term plasticity (STP) denotes changes in synaptic strength that last up to tens of seconds. It is generally thought that STP impacts information transfer across synaptic connections and may thereby provide neurons with, for example, the ability to detect input coherence, to maintain stability and to promote synchronization. STP is due to a combination of mechanisms, including vesicle depletion and calcium accumulation in synaptic terminals. Different forms of STP exist, depending on many factors, including synapse type. Recent evidence shows that synapse dependence holds true even for connections that originate from a single presynaptic cell, which implies that postsynaptic target cell type can determine synaptic short-term dynamics. This arrangement is surprising, since STP itself is chiefly due to presynaptic mechanisms. Target-specific synaptic dynamics in addition imply that STP is not a bug resulting from synapses fatiguing when driven too hard, but rather a feature that is selectively implemented in the brain for specific functional purposes. As an example, target-specific STP results in sequential somatic and dendritic inhibition in neocortical and hippocampal excitatory cells during high-frequency firing. Recent studies also show that the Elfn1 gene specifically controls STP at some synapse types. In addition, presynaptic NMDA receptors have been implicated in synapse-specific control of synaptic dynamics during high-frequency activity. We argue that synapse-specific STP deserves considerable further study, both experimentally and theoretically, since its function is not well known. We propose that synapse-specific STP has to be understood in the context of the local circuit, which requires combining different scientific disciplines ranging from molecular biology through electrophysiology to computer modeling.

Differential cortical activation of the striatal direct and indirect pathway cells: reconciling the anatomical and optogenetic results by using a computational method

“…Synaptic response to repetitive inputs can generally evolve through short-term synaptic plasticity (Buonomano and Maass 2009;Sussillo et al 2007), and as a result, synapses that show negligible response to a single spike can nevertheless show quite strong responses to multiple spikes (Kapfer et al 2007;Silberberg and Markram 2007). Moreover, the nature of short-term plasticity can dramatically differ depending on presynaptic (Beierlein and Connors 2002) and postsynaptic neuron types (Blackman et al 2013;Markram et al 1998). Therefore, to understand how information flows between cortex and striatum, it is crucial to know the overall time-dependent impacts of multiple IT or PT inputs on dMSNs and iMSNs.…”

Muscles innervated by a single motor neuron exhibit divergent synaptic properties on multiple time scales

“…Additionally, postsynaptic contributions such as a longer time constant in the summating muscle shape distinct muscle responses (Katz et al, 1993). Other studies also point to predominantly presynaptic mechanisms underlying differences in target cell-specific short-term plasticity (Blackman et al, 2013;Reyes et al, 1998;Scanziani et al, 1998). Although the functions may not yet be identified, distinct short-term plasticity at different presynaptic terminals of the same neuron suggests that this plasticity has specific functions appropriate for each target.…”

“…This leads to a prediction that the postsynaptic neuron could play some role in determining plasticity. In fact, genetic manipulations at central and peripheral synapses indicate that retrograde signals from postsynaptic cells specifically regulate transmitter release from their partner presynaptic compartment (Blackman et al, 2013;Davis and Goodman, 1998). Thus, changes in presynaptic release probability may be the dominant means by which target cell-specific plasticity is determined.…”

“…From cortical to neuromuscular synapses, a neuron can express different plasticity at distinct axon terminals and thus influence multiple targets in different ways (Atwood, 1967;Blackman et al, 2013;Crider and Cooper, 2000;Davis and Goodman, 1998;Katz et al, 1993;Reyes et al, 1998;Scanziani et al, 1998). Thus far, distinctions have been identified in short-term plasticity sensitive to the timing of inter-spike intervals.…”

Target-specific regulation of presynaptic release properties at auditory nerve terminals in the avian cochlear nucleus

“…Target cell-dependent specificity of synaptic plasticity has been described in numerous brain regions, and evidence has been mounting in support of the specific regulation of presynaptic properties depending on the identity and molecular signature of the postsynaptic target (Blackman et al 2013). In the mammalian ventral cochlear nucleus, a recent study measured short-term depression and MK801 blockade at nerve inputs to bushy cells (Yang and Xu-Friedman 2012).…”