Distribution of vesicle pools in cerebellar parallel fibre terminals after depression of ectopic transmission.

At parallel fibre terminals in the cerebellar cortex, glutamate released outside of the active zone can activate AMPA receptors on juxtaposed Bergmann glial cell processes. This process is termed "ectopic" release, and allows for directed transmission to astroglial cells that is functional...

Full description

Bibliographic Details
Main Authors: Katharine L Dobson, Zoe H Smith, Tomas C Bellamy
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0200937
id doaj-04ebd98fc8034119bbe5131f16fed906
record_format Article
spelling doaj-04ebd98fc8034119bbe5131f16fed9062021-03-03T19:46:30ZengPublic Library of Science (PLoS)PLoS ONE1932-62032018-01-01137e020093710.1371/journal.pone.0200937Distribution of vesicle pools in cerebellar parallel fibre terminals after depression of ectopic transmission.Katharine L DobsonZoe H SmithTomas C BellamyAt parallel fibre terminals in the cerebellar cortex, glutamate released outside of the active zone can activate AMPA receptors on juxtaposed Bergmann glial cell processes. This process is termed "ectopic" release, and allows for directed transmission to astroglial cells that is functionally independent of synaptic transmission to postsynaptic Purkinje neurons. The location of ectopic sites in presynaptic terminals is uncertain. Functional evidence suggests that stimulation of parallel fibres at 1 Hz exhausts ectopic transmission due to a failure to rapidly recycle vesicles to the ectopic pool, and so would predict a loss of vesicles in the near vicinity of extrasynaptic glial processes. In this study we used this stimulation protocol to investigate whether the distribution of vesicles within the presynaptic terminal is altered after suppression of ectopic release. Stimulation at 1 Hz had only a minor impact on the distribution of vesicles in presynaptic terminals when analysed with electron microscopy. Vesicle number and terminal size were unaffected by 1 Hz stimulation, but the relative abundance of vesicles in close proximity to the active zone was marginally reduced. In contrast, the fraction of vesicles facing glial membranes was unchanged after suppression of ectopic transmission. 1 Hz stimulation also resulted in a small but statistically-significant increase in the distance between glial membrane and presynaptic terminal, suggesting withdrawal of glial membranes from synapses is detectable in ultrastructural anatomy within minutes. These results raise doubts about the location of ectopic release sites, but indicate that neuron-glial association varies on a dynamic time scale.https://doi.org/10.1371/journal.pone.0200937
collection DOAJ
language English
format Article
sources DOAJ
author Katharine L Dobson
Zoe H Smith
Tomas C Bellamy
spellingShingle Katharine L Dobson
Zoe H Smith
Tomas C Bellamy
Distribution of vesicle pools in cerebellar parallel fibre terminals after depression of ectopic transmission.
PLoS ONE
author_facet Katharine L Dobson
Zoe H Smith
Tomas C Bellamy
author_sort Katharine L Dobson
title Distribution of vesicle pools in cerebellar parallel fibre terminals after depression of ectopic transmission.
title_short Distribution of vesicle pools in cerebellar parallel fibre terminals after depression of ectopic transmission.
title_full Distribution of vesicle pools in cerebellar parallel fibre terminals after depression of ectopic transmission.
title_fullStr Distribution of vesicle pools in cerebellar parallel fibre terminals after depression of ectopic transmission.
title_full_unstemmed Distribution of vesicle pools in cerebellar parallel fibre terminals after depression of ectopic transmission.
title_sort distribution of vesicle pools in cerebellar parallel fibre terminals after depression of ectopic transmission.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2018-01-01
description At parallel fibre terminals in the cerebellar cortex, glutamate released outside of the active zone can activate AMPA receptors on juxtaposed Bergmann glial cell processes. This process is termed "ectopic" release, and allows for directed transmission to astroglial cells that is functionally independent of synaptic transmission to postsynaptic Purkinje neurons. The location of ectopic sites in presynaptic terminals is uncertain. Functional evidence suggests that stimulation of parallel fibres at 1 Hz exhausts ectopic transmission due to a failure to rapidly recycle vesicles to the ectopic pool, and so would predict a loss of vesicles in the near vicinity of extrasynaptic glial processes. In this study we used this stimulation protocol to investigate whether the distribution of vesicles within the presynaptic terminal is altered after suppression of ectopic release. Stimulation at 1 Hz had only a minor impact on the distribution of vesicles in presynaptic terminals when analysed with electron microscopy. Vesicle number and terminal size were unaffected by 1 Hz stimulation, but the relative abundance of vesicles in close proximity to the active zone was marginally reduced. In contrast, the fraction of vesicles facing glial membranes was unchanged after suppression of ectopic transmission. 1 Hz stimulation also resulted in a small but statistically-significant increase in the distance between glial membrane and presynaptic terminal, suggesting withdrawal of glial membranes from synapses is detectable in ultrastructural anatomy within minutes. These results raise doubts about the location of ectopic release sites, but indicate that neuron-glial association varies on a dynamic time scale.
url https://doi.org/10.1371/journal.pone.0200937
work_keys_str_mv AT katharineldobson distributionofvesiclepoolsincerebellarparallelfibreterminalsafterdepressionofectopictransmission
AT zoehsmith distributionofvesiclepoolsincerebellarparallelfibreterminalsafterdepressionofectopictransmission
AT tomascbellamy distributionofvesiclepoolsincerebellarparallelfibreterminalsafterdepressionofectopictransmission
_version_ 1714825622568566784