In Vivo development of outer retinal synapses in the absence of glial contact

Philip R. Williams, Sachihiro C. Suzuki, Takeshi Yoshimatsu, Owen T. Lawrence, Steven J. Waldron, Michael J. Parsons, Michael L. Nonet, Rachel O L Wong

Research output: Contribution to journalArticle

Abstract

Astroglia secrete factors that promote synapse formation and maintenance. In culture, glial contact has also been shown to facilitate synaptogenesis. Here, we examined whether glial contact is important for establishing circuits in vivo by simultaneously monitoring differentiation of glial cells and local synaptogenesis over time. Photoreceptor circuits of the vertebrate retina are particularly suitable for this study because of the relatively simple, laminar organization of their connectivity with their target neurons, horizontal cells and bipolar cells. Also, individual photoreceptor terminals are ensheathed within the outer plexiform layer (OPL) by the processes of one type of glia, Müller glia cells (MGs). Weconducted in vivo time-lapse multiphoton imaging of the rapidly developing and relatively transparent zebrafish retina to ascertain the time course of MG development relative to OPL synaptogenesis. The emergence of synaptic triads, indicative of functional photoreceptor circuits, and structural association with glial processes were also examined across ages by electron microscopy. We first show that MG processes form territories that tile within the inner and outer synaptic layers. We then demonstrate that cone photoreceptor synapses are assembled before the elaboration of MG processes in the OPL. Using a targeted cell ablation approach, we also determined whether the maintenance of photoreceptor synapses is perturbed when local MGs are absent. We found that removal of MGs had no appreciable effect on the stability of newly formed cone synapses. Thus, in contrast to other CNS circuits, contact from glia is not necessary for the formation or immediate stabilization of outer retinal synapses.

Original languageEnglish (US)
Pages (from-to)11951-11961
Number of pages11
JournalJournal of Neuroscience
Volume30
Issue number36
DOIs
StatePublished - Sep 8 2010

Fingerprint

Neuroglia
Synapses
Retina
Maintenance
Time-Lapse Imaging
Retinal Cone Photoreceptor Cells
Vertebrate Photoreceptor Cells
Zebrafish
Astrocytes
Electron Microscopy
Neurons

ASJC Scopus subject areas

  • Neuroscience(all)
  • Medicine(all)

Cite this

Williams, P. R., Suzuki, S. C., Yoshimatsu, T., Lawrence, O. T., Waldron, S. J., Parsons, M. J., ... Wong, R. O. L. (2010). In Vivo development of outer retinal synapses in the absence of glial contact. Journal of Neuroscience, 30(36), 11951-11961. https://doi.org/10.1523/JNEUROSCI.3391-10.2010

In Vivo development of outer retinal synapses in the absence of glial contact. / Williams, Philip R.; Suzuki, Sachihiro C.; Yoshimatsu, Takeshi; Lawrence, Owen T.; Waldron, Steven J.; Parsons, Michael J.; Nonet, Michael L.; Wong, Rachel O L.

In: Journal of Neuroscience, Vol. 30, No. 36, 08.09.2010, p. 11951-11961.

Research output: Contribution to journalArticle

Williams, PR, Suzuki, SC, Yoshimatsu, T, Lawrence, OT, Waldron, SJ, Parsons, MJ, Nonet, ML & Wong, ROL 2010, 'In Vivo development of outer retinal synapses in the absence of glial contact', Journal of Neuroscience, vol. 30, no. 36, pp. 11951-11961. https://doi.org/10.1523/JNEUROSCI.3391-10.2010
Williams PR, Suzuki SC, Yoshimatsu T, Lawrence OT, Waldron SJ, Parsons MJ et al. In Vivo development of outer retinal synapses in the absence of glial contact. Journal of Neuroscience. 2010 Sep 8;30(36):11951-11961. https://doi.org/10.1523/JNEUROSCI.3391-10.2010
Williams, Philip R. ; Suzuki, Sachihiro C. ; Yoshimatsu, Takeshi ; Lawrence, Owen T. ; Waldron, Steven J. ; Parsons, Michael J. ; Nonet, Michael L. ; Wong, Rachel O L. / In Vivo development of outer retinal synapses in the absence of glial contact. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 36. pp. 11951-11961.
@article{2432ebe711e84969a92414842a3e966c,
title = "In Vivo development of outer retinal synapses in the absence of glial contact",
abstract = "Astroglia secrete factors that promote synapse formation and maintenance. In culture, glial contact has also been shown to facilitate synaptogenesis. Here, we examined whether glial contact is important for establishing circuits in vivo by simultaneously monitoring differentiation of glial cells and local synaptogenesis over time. Photoreceptor circuits of the vertebrate retina are particularly suitable for this study because of the relatively simple, laminar organization of their connectivity with their target neurons, horizontal cells and bipolar cells. Also, individual photoreceptor terminals are ensheathed within the outer plexiform layer (OPL) by the processes of one type of glia, M{\"u}ller glia cells (MGs). Weconducted in vivo time-lapse multiphoton imaging of the rapidly developing and relatively transparent zebrafish retina to ascertain the time course of MG development relative to OPL synaptogenesis. The emergence of synaptic triads, indicative of functional photoreceptor circuits, and structural association with glial processes were also examined across ages by electron microscopy. We first show that MG processes form territories that tile within the inner and outer synaptic layers. We then demonstrate that cone photoreceptor synapses are assembled before the elaboration of MG processes in the OPL. Using a targeted cell ablation approach, we also determined whether the maintenance of photoreceptor synapses is perturbed when local MGs are absent. We found that removal of MGs had no appreciable effect on the stability of newly formed cone synapses. Thus, in contrast to other CNS circuits, contact from glia is not necessary for the formation or immediate stabilization of outer retinal synapses.",
author = "Williams, {Philip R.} and Suzuki, {Sachihiro C.} and Takeshi Yoshimatsu and Lawrence, {Owen T.} and Waldron, {Steven J.} and Parsons, {Michael J.} and Nonet, {Michael L.} and Wong, {Rachel O L}",
year = "2010",
month = "9",
day = "8",
doi = "10.1523/JNEUROSCI.3391-10.2010",
language = "English (US)",
volume = "30",
pages = "11951--11961",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "36",

}

TY - JOUR

T1 - In Vivo development of outer retinal synapses in the absence of glial contact

AU - Williams, Philip R.

AU - Suzuki, Sachihiro C.

AU - Yoshimatsu, Takeshi

AU - Lawrence, Owen T.

AU - Waldron, Steven J.

AU - Parsons, Michael J.

AU - Nonet, Michael L.

AU - Wong, Rachel O L

PY - 2010/9/8

Y1 - 2010/9/8

N2 - Astroglia secrete factors that promote synapse formation and maintenance. In culture, glial contact has also been shown to facilitate synaptogenesis. Here, we examined whether glial contact is important for establishing circuits in vivo by simultaneously monitoring differentiation of glial cells and local synaptogenesis over time. Photoreceptor circuits of the vertebrate retina are particularly suitable for this study because of the relatively simple, laminar organization of their connectivity with their target neurons, horizontal cells and bipolar cells. Also, individual photoreceptor terminals are ensheathed within the outer plexiform layer (OPL) by the processes of one type of glia, Müller glia cells (MGs). Weconducted in vivo time-lapse multiphoton imaging of the rapidly developing and relatively transparent zebrafish retina to ascertain the time course of MG development relative to OPL synaptogenesis. The emergence of synaptic triads, indicative of functional photoreceptor circuits, and structural association with glial processes were also examined across ages by electron microscopy. We first show that MG processes form territories that tile within the inner and outer synaptic layers. We then demonstrate that cone photoreceptor synapses are assembled before the elaboration of MG processes in the OPL. Using a targeted cell ablation approach, we also determined whether the maintenance of photoreceptor synapses is perturbed when local MGs are absent. We found that removal of MGs had no appreciable effect on the stability of newly formed cone synapses. Thus, in contrast to other CNS circuits, contact from glia is not necessary for the formation or immediate stabilization of outer retinal synapses.

AB - Astroglia secrete factors that promote synapse formation and maintenance. In culture, glial contact has also been shown to facilitate synaptogenesis. Here, we examined whether glial contact is important for establishing circuits in vivo by simultaneously monitoring differentiation of glial cells and local synaptogenesis over time. Photoreceptor circuits of the vertebrate retina are particularly suitable for this study because of the relatively simple, laminar organization of their connectivity with their target neurons, horizontal cells and bipolar cells. Also, individual photoreceptor terminals are ensheathed within the outer plexiform layer (OPL) by the processes of one type of glia, Müller glia cells (MGs). Weconducted in vivo time-lapse multiphoton imaging of the rapidly developing and relatively transparent zebrafish retina to ascertain the time course of MG development relative to OPL synaptogenesis. The emergence of synaptic triads, indicative of functional photoreceptor circuits, and structural association with glial processes were also examined across ages by electron microscopy. We first show that MG processes form territories that tile within the inner and outer synaptic layers. We then demonstrate that cone photoreceptor synapses are assembled before the elaboration of MG processes in the OPL. Using a targeted cell ablation approach, we also determined whether the maintenance of photoreceptor synapses is perturbed when local MGs are absent. We found that removal of MGs had no appreciable effect on the stability of newly formed cone synapses. Thus, in contrast to other CNS circuits, contact from glia is not necessary for the formation or immediate stabilization of outer retinal synapses.

UR - http://www.scopus.com/inward/record.url?scp=77956588977&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77956588977&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.3391-10.2010

DO - 10.1523/JNEUROSCI.3391-10.2010

M3 - Article

C2 - 20826659

AN - SCOPUS:77956588977

VL - 30

SP - 11951

EP - 11961

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 36

ER -