Distinct Target-Specific Mechanisms Homeostatically Stabilize Transmission at Pre- and Post-synaptic Compartments

Neurons must establish and stabilize connections made with diverse targets, each with distinct demands and functional characteristics. At Drosophila neuromuscular junctions (NMJs), synaptic strength remains stable in a manipulation that simultaneously induces hypo-innervation on one target and hyper...

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Main Authors: Pragya Goel, Samantha Nishimura, Karthik Chetlapalli, Xiling Li, Catherine Chen, Dion Dickman
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fncel.2020.00196/full
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author Pragya Goel
Samantha Nishimura
Karthik Chetlapalli
Xiling Li
Catherine Chen
Dion Dickman
author_facet Pragya Goel
Samantha Nishimura
Karthik Chetlapalli
Xiling Li
Catherine Chen
Dion Dickman
author_sort Pragya Goel
collection DOAJ
description Neurons must establish and stabilize connections made with diverse targets, each with distinct demands and functional characteristics. At Drosophila neuromuscular junctions (NMJs), synaptic strength remains stable in a manipulation that simultaneously induces hypo-innervation on one target and hyper-innervation on the other. However, the expression mechanisms that achieve this exquisite target-specific homeostatic control remain enigmatic. Here, we identify the distinct target-specific homeostatic expression mechanisms. On the hypo-innervated target, an increase in postsynaptic glutamate receptor (GluR) abundance is sufficient to compensate for reduced innervation, without any apparent presynaptic adaptations. In contrast, a target-specific reduction in presynaptic neurotransmitter release probability is reflected by a decrease in active zone components restricted to terminals of hyper-innervated targets. Finally, loss of postsynaptic GluRs on one target induces a compartmentalized, homeostatic enhancement of presynaptic neurotransmitter release called presynaptic homeostatic potentiation (PHP) that can be precisely balanced with the adaptations required for both hypo- and hyper-innervation to maintain stable synaptic strength. Thus, distinct anterograde and retrograde signaling systems operate at pre- and post-synaptic compartments to enable target-specific, homeostatic control of neurotransmission.
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spelling doaj.art-3cc414f994d44abbbd3d82c54eff8a7b2022-12-21T23:10:17ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022020-06-011410.3389/fncel.2020.00196552367Distinct Target-Specific Mechanisms Homeostatically Stabilize Transmission at Pre- and Post-synaptic CompartmentsPragya GoelSamantha NishimuraKarthik ChetlapalliXiling LiCatherine ChenDion DickmanNeurons must establish and stabilize connections made with diverse targets, each with distinct demands and functional characteristics. At Drosophila neuromuscular junctions (NMJs), synaptic strength remains stable in a manipulation that simultaneously induces hypo-innervation on one target and hyper-innervation on the other. However, the expression mechanisms that achieve this exquisite target-specific homeostatic control remain enigmatic. Here, we identify the distinct target-specific homeostatic expression mechanisms. On the hypo-innervated target, an increase in postsynaptic glutamate receptor (GluR) abundance is sufficient to compensate for reduced innervation, without any apparent presynaptic adaptations. In contrast, a target-specific reduction in presynaptic neurotransmitter release probability is reflected by a decrease in active zone components restricted to terminals of hyper-innervated targets. Finally, loss of postsynaptic GluRs on one target induces a compartmentalized, homeostatic enhancement of presynaptic neurotransmitter release called presynaptic homeostatic potentiation (PHP) that can be precisely balanced with the adaptations required for both hypo- and hyper-innervation to maintain stable synaptic strength. Thus, distinct anterograde and retrograde signaling systems operate at pre- and post-synaptic compartments to enable target-specific, homeostatic control of neurotransmission.https://www.frontiersin.org/article/10.3389/fncel.2020.00196/fullactive zonehomeostasissynaptic plasticityDrosophilaneuromuscular junction
spellingShingle Pragya Goel
Samantha Nishimura
Karthik Chetlapalli
Xiling Li
Catherine Chen
Dion Dickman
Distinct Target-Specific Mechanisms Homeostatically Stabilize Transmission at Pre- and Post-synaptic Compartments
Frontiers in Cellular Neuroscience
active zone
homeostasis
synaptic plasticity
Drosophila
neuromuscular junction
title Distinct Target-Specific Mechanisms Homeostatically Stabilize Transmission at Pre- and Post-synaptic Compartments
title_full Distinct Target-Specific Mechanisms Homeostatically Stabilize Transmission at Pre- and Post-synaptic Compartments
title_fullStr Distinct Target-Specific Mechanisms Homeostatically Stabilize Transmission at Pre- and Post-synaptic Compartments
title_full_unstemmed Distinct Target-Specific Mechanisms Homeostatically Stabilize Transmission at Pre- and Post-synaptic Compartments
title_short Distinct Target-Specific Mechanisms Homeostatically Stabilize Transmission at Pre- and Post-synaptic Compartments
title_sort distinct target specific mechanisms homeostatically stabilize transmission at pre and post synaptic compartments
topic active zone
homeostasis
synaptic plasticity
Drosophila
neuromuscular junction
url https://www.frontiersin.org/article/10.3389/fncel.2020.00196/full
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AT xilingli distincttargetspecificmechanismshomeostaticallystabilizetransmissionatpreandpostsynapticcompartments
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