Nanoscale remodeling of functional synaptic vesicle pools in Hebbian plasticity

Rey, Stephanie, Marra, Vincenzo, Smith, Catherine and Staras, Kevin (2020) Nanoscale remodeling of functional synaptic vesicle pools in Hebbian plasticity. Cell Reports, 30 (6). pp. 2006-2017. ISSN 2211-1247

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Abstract

Vesicle pool properties are known determinants of synaptic efficacy, but their potential role as modifiable substrates in forms of Hebbian plasticity is still unclear. Here, we investigate this using a nanoscale readout of functionally recycled vesicles in natively wired hippocampal CA3→CA1 circuits undergoing long-term potentiation (LTP). We show that the total recycled vesicle pool is larger after plasticity induction, with the smallest terminals exhibiting the greatest relative expansion. Changes in the spatial organization of vesicles accompany potentiation including a specific increase in the number of recycled vesicles at the active zone, consistent with an ultrastructural remodeling component of synaptic strengthening. The cAMP-PKA pathway activator, forskolin, selectively mimics some features of LTP-driven changes, suggesting that distinct and independent modules of regulation accompany plasticity expression. Our findings provide evidence for a presynaptic locus of LTP encoded in the number and arrangement of functionally recycled vesicles, with relevance for models of long-term plasticity storage.

Item Type: Article
Keywords: Neuron, vesicle, synapse, hippocampus, electron microscopy
Schools and Departments: School of Life Sciences > Neuroscience
Research Centres and Groups: Sussex Neuroscience
Subjects: Q Science > QP Physiology > QP0351 Neurophysiology and neuropsychology > QP0361 Nervous system
Q Science > QP Physiology > QP0351 Neurophysiology and neuropsychology > QP0361 Nervous system > QP0364 Synapses
Q Science > QP Physiology > QP0351 Neurophysiology and neuropsychology > QP0361 Nervous system > QP0364.5 Neural transmission
Depositing User: Kevin Staras
Date Deposited: 17 Feb 2020 09:45
Last Modified: 17 Feb 2020 09:45
URI: http://sro.sussex.ac.uk/id/eprint/89942

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Project NameSussex Project NumberFunderFunder Ref
Functional synaptic vesicle pool remodelling as a basis for plasticity and control of complex behaviourG2521BBSRC-BIOTECHNOLOGY & BIOLOGICAL SCIENCES RESEARCH COUNCILBB/S00310X/1