Key Points
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Synaptic efficacy is regulated by many forms of short-term plasticity during physiological patterns of activity. Here we discuss the distinct functional consequences of short-term plasticity at two powerful synapses. The climbing fibre to cerebellar Purkinje cell synapse and the retinal ganglion cell to thalamocortical neuron (retinogeniculate) synapse share some common synaptic features. However, the climbing fibre evokes a consistent, stereotyped response in the Purkinje cell, whereas the response of the thalamocortical cell to retinal ganglion cell input is more variable.
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Several features of transmission at the climbing fibre to Purkinje cell synapse minimize depression and allow the climbing fibre to evoke a consistent response in the Purkinje cell during physiological patterns of activity. First, postsynaptic receptor desensitization does not contribute to depression at this synapse even at short interstimulus intervals. Second, calcium that enters during the action potential accelerates recovery from depression. Finally, multivesicular release and receptor saturation make the Purkinje cell less sensitive to decreases in the amount of neurotransmitter released by the climbing fibre.
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The retinogeniculate synapse contains both AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid) and NMDA (N-methyl-D-aspartate) receptors, which have distinct forms of plasticity. Desensitization and depression of AMPA currents limit their efficacy, particularly during high-frequency activity. Although NMDA currents are limited by saturation, the long duration of NMDA currents results in summation and a greater NMDA contribution during sustained activity.
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The two currents at the retinogeniculate synapse influence postsynaptic firing in distinct ways. AMPA currents elicit short-latency precisely timed action potentials. NMDA currents, however, elicit longer-latency action potentials and can elicit multiple spikes per presynaptic spike, which results in amplification. Consequently, responses can vary during the course of a train of activity and can differ between thalamocortical neurons on the basis of the relative amplitudes of AMPA and NMDA currents. So, the retinogeniculate synapse dynamically regulates transmission through the two receptor types and their distinct forms of plasticity.
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The synapses discussed here illustrate that, despite initial similarities, synapses are specialized to serve distinct functional roles. Future work aimed at determining the contributions of multiple forms of plasticity at different synapses and how these interact with intrinsic cellular properties will be necessary to fully understand how short-term synaptic plasticity contributes to the function of synapses in the brain.
Abstract
During physiological patterns of activity, synaptic activity is regulated by many forms of short-term plasticity. Here, we compare the functional consequences of such plasticity at the synapse from the climbing fibre to the Purkinje cell in the cerebellum and at the synapse between the retinal ganglion cell and the thalamocortical relay neuron in the lateral geniculate nucleus. Despite superficial similarities between these two powerful synapses, they have distinctive synaptic plasticity. The climbing fibre synapse is highly reliable but accomplishes this through many synaptic specializations. However, the retinogeniculate synapse dynamically regulates the flow of visual information by using two types of receptor that have different types of plasticity. These synapses illustrate the important functional consequences of synaptic plasticity.
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D.M.B. and K.A.F. contributed equally in the preparation of this review.
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Encyclopedia of Life Sciences
Synaptic Plasticity: Short Term
Glossary
- READILY RELEASABLE POOL
-
A pool of synaptic vesicles that is available for rapid fusion with the presynaptic membrane on arrival of a nerve impulse. The vesicles are docked to the membrane and have been biochemically primed for release.
- PAIRED-PULSE DEPRESSION
-
A decrease in the amplitude of the second of two closely timed excitatory postsynaptic currents. It can result presynaptically from a decrease in the amount of neurotransmitter released or postsynaptically as a result of desensitization.
- BERGMANN GLIA
-
Astrocytes that are located in the cerebellum with their cell bodies close to a Purkinje cell. They extend radial fibres along the dendritic tree of the Purkinje cell and ensheath synapses made by the climbing fibre and parallel fibres.
- DYNAMIC-CLAMP
-
A technique to introduce artificial synaptic or voltage-gated conductance into a neuron. The time course, voltage dependence and reversal potential are measured under voltage-clamp conditions and are used to determine the appropriate current to be injected to mimic the synaptic conductance by the dynamic-clamp technique, in current-clamp recording mode.
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Blitz, D., Foster, K. & Regehr, W. Short-term synaptic plasticity: a comparison of two synapses. Nat Rev Neurosci 5, 630–640 (2004). https://doi.org/10.1038/nrn1475
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DOI: https://doi.org/10.1038/nrn1475
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