Synapse-type-specific plasticity in local circuits

doi:10.1016/j.conb.2015.08.001

Current Opinion in Neurobiology

Volume 35, December 2015, Pages 127-135

https://doi.org/10.1016/j.conb.2015.08.001 Get rights and content

Highlights

•
Induction and expression of long-term plasticity is specific to synapse type.
•
Synaptic dynamics is also connection-type specific.
•
The presynaptic NMDAR is a prime example of a determinant of synapse-type-specific plasticity.
•
Synapse-type-specific plasticity has implications for microcircuit function in health and disease.
•
The resulting increase in complexity makes local circuits more powerful, but also harder to study.

Neuroscientists spent decades debating whether synaptic plasticity was presynaptically or postsynaptically expressed. It was eventually concluded that plasticity depends on many factors, including cell type. More recently, it has become increasingly clear that plasticity is regulated at an even finer grained level; it is specific to the synapse type, a concept we denote synapse-type-specific plasticity (STSP). Here, we review recent developments in the field of STSP, discussing both long-term and short-term variants and with particular emphasis on neocortical function. As there are dozens of neocortical cell types, there is a multiplicity of forms of STSP, the vast majority of which have never been explored. We argue that to understand the brain and synaptic diseases, we have to grapple with STSP.

Section snippets

A definition of synapse-type-specific plasticity

Here, we define synapse-type-specific plasticity (STSP) as plasticity that varies with synapse type. STSP comes in different forms (Figure 1). Different synapses originating from the same presynaptic cell can have different forms of plasticity depending upon the on postsynaptic target, here termed divergent STSP. Conversely, plasticity may differ for the same postsynaptic cell depending on the type of input, which we denote convergent STSP. While more difficult to distinguish experimentally,

Synapse-type-specific short-term plasticity

Short-term plasticity (STP) refers to a depression or facilitation of synaptic efficacy that last on the order of seconds [2]. The mechanisms underlying STP are typically presynaptic, including changes in the readily releasable vesicle pool size, changes in the number of release sites, and alterations in presynaptic calcium dynamics [3]. Early evidence that STP could be synapse-type-specific came from observations that the magnitude and variability of calcium influx in response to single action

Synapse-type-specific long-term plasticity

Long-term plasticity refers to activity-dependent changes in synaptic efficacy that last for minutes up to days [49]. Long-term plasticity is typically mechanistically distinct from STP and includes processes such as Hebbian and homeostatic plasticity. Long-lasting increases or decreases in synaptic strength — long-term potentiation (LTP) or depression (LTD), respectively — are believed to be critical to circuit and memory formation [50]. Synapse-type-specific long-term plasticity may thus be

Conclusions and future directions

In this review, we have discussed recent research on STSP learning rules and synaptic dynamics, as well as their potential functional roles (summarized in Table 1). We argue that STSP may have evolved of necessity to enable more complex computations in local circuits. The existence of STSP is furthermore expected, since the nodes of biological neuronal networks are made up of dozens of different cell types [70, 71, 72]. Presumably, these different cell types need to be governed by distinct

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgements

We thank Alanna Watt, Ben Philpot, Ole Paulsen, Abhishek Banerjee, Txomin Lalanne, Elvis Cela, Therese Abrahamsson, Arne Blackman, and Rui P. Costa for help and useful discussions. R.S.L. was funded by the Allen Institute for Brain Science and wishes to thank the Allen Institute founders, Paul G. Allen and Jody Allen, for their vision, encouragement, and support. P.J.S. was funded by CFI LOF 28331, CIHR OG 126137, CIHR NIA 288936, and NSERC DG 418546-2.

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Citation Excerpt :
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View full text

Synapse-type-specific plasticity in local circuits

Highlights

Section snippets

A definition of synapse-type-specific plasticity

Synapse-type-specific short-term plasticity

Synapse-type-specific long-term plasticity

Conclusions and future directions

References and recommended reading

Acknowledgements

Neuron

Neuron

Neuron

J Neurosci

J Neurosci

Trends Neurosci

J Neurosci

J Neurosci

Nature

J Neurosci

Front Synaptic Neurosci

Neuron

J Physiol

bioRxiv

Neuroscientist

Physiol Rep

Nat Neurosci

Dendritic excitability and synaptic plasticity

Physiol Rev

Short-term presynaptic plasticity

Cold Spring Harb Perspect Biol

Fluctuations in intracellular calcium responses to action potentials in single en passage presynaptic boutons of layer V neurons in neocortical slices

Learn Mem

Target cell-dependent normalization of transmitter release at neocortical synapses

Science

Independent regulation of basal neurotransmitter release efficacy by variable Ca(2)+ influx and bouton size at small central synapses

PLoS Biol

Intrinsic variability in Pv, RRP size, Ca(2+) channel repertoire, and presynaptic potentiation in individual synaptic boutons

Front Synaptic Neurosci

CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices

J Physiol

Differential signaling via the same axon of neocortical pyramidal neurons

Proc Natl Acad Sci U S A

Examining size–strength relationships at hippocampal synapses using an ultrastructural measurement of synaptic release probability

J Struct Biol

Elfn1 regulates target-specific release probability at CA1-interneuron synapses

Science

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

Front Synaptic Neurosci

Essential cooperation of N-cadherin and neuroligin-1 in the transsynaptic control of vesicle accumulation

Proc Natl Acad Sci U S A

Cadherin regulates dendritic spine morphogenesis

Neuron

Selective capability of SynCAM and neuroligin for functional synapse assembly

J Neurosci

Alpha2delta expression sets presynaptic calcium channel abundance and release probability

Nature

RIM determines Ca(2)+ channel density and vesicle docking at the presynaptic active zone

Neuron

Control and plasticity of the presynaptic action potential waveform at small CNS nerve terminals

Neuron

Control of inhibitory synaptic outputs by low excitability of axon terminals revealed by direct recording

Neuron

Experience-dependent switch in sign and mechanisms for plasticity in layer 4 of primary visual cortex

J Neurosci

Presynaptic development at L4 to l2/3 excitatory synapses follows different time courses in visual and somatosensory cortex

J Neurosci

Developmental changes in short-term plasticity at the rat calyx of Held synapse

J Neurosci

Developmental changes in release properties of the CA3-CA1 glutamate synapse in rat hippocampus

J Neurophysiol

Synapse-specific control of experience-dependent plasticity by presynaptic NMDA receptors

Neuron