Synapses formed by identified retinogeniculate axons during the segregation of eye input - PubMed (original) (raw)
Synapses formed by identified retinogeniculate axons during the segregation of eye input
G Campbell et al. J Neurosci. 1992 May.
Abstract
The synaptic organization of identified retinogeniculate axons was studied during the prenatal development of eye-specific layers in the LGN of the cat. During this period, retinogeniculate axons undergo stereotyped morphological changes. Retinogeniculate axons originating from one eye and passing through LGN territory destined to be solely innervated by the other eye (inappropriate territory) initially give rise to many side branches. As the eye-specific layers emerge, these axons elaborate extensive terminal arbors within territory appropriate to their eye of origin and concurrently retract their side branches from inappropriate territory (Sretavan and Shatz, 1986). These transient side branches may therefore represent a morphological substrate for the observed functional convergence of inputs from the two eyes onto common LGN neurons during prenatal development (Shatz and Kirkwood, 1984). This possibility was investigated by examining whether identified axons and their side branches form synapses in inappropriate territory. Three retinogeniculate axons from two fetuses aged embryonic day 53 (E53) and E57 were filled with HRP in an in vitro preparation, prior to being processed for electron microscopy (EM). The HRP-filled axons, originating from the contralateral eye, were first reconstructed at the light microscope level. The portion of axon passing through the center of ipsilaterally innervated layer A1 was then serially sectioned and reconstructed by EM. Two sets of 450 serial EM sections revealed that all three contralateral axons established synaptic contacts in ipsilateral territory. Many of these synapses were made by side branches and a few were even formed by the main axon trunks. Both side branches and trunks formed mainly en passant asymmetrical contacts that were associated with spherical synaptic vesicles and that were apposed to immature dendritic elements and dendritic shafts. For comparison, a portion of the same E53 axon within the future contralateral layer A was also serially sectioned and reconstructed for EM. Within this contralateral zone, the E53 axon formed synaptic contacts similar to those established in the ipsilateral region, except that in the appropriate zone they contained significantly more synaptic vesicles. These results demonstrate that axons from the contralateral eye can establish synapses in territory simultaneously innervated by the ipsilateral eye, both via side branches and by means of contacts along the main axon trunk. Thus, the development of eye-specific layers is accompanied by the formation and subsequent elimination of synapses that almost certainly represent a morphological substrate for the known transient functional convergence of inputs from the two eyes.
Similar articles
- Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat's lateral geniculate nucleus.
Sretavan DW, Shatz CJ. Sretavan DW, et al. J Neurosci. 1986 Jan;6(1):234-51. doi: 10.1523/JNEUROSCI.06-01-00234.1986. J Neurosci. 1986. PMID: 3944621 Free PMC article. - Prenatal development of cat retinogeniculate axon arbors in the absence of binocular interactions.
Sretavan DW, Shatz CJ. Sretavan DW, et al. J Neurosci. 1986 Apr;6(4):990-1003. doi: 10.1523/JNEUROSCI.06-04-00990.1986. J Neurosci. 1986. PMID: 3701418 Free PMC article. - Development of the mammalian retinogeniculate pathway: target finding, transient synapses and binocular segregation.
So KF, Campbell G, Lieberman AR. So KF, et al. J Exp Biol. 1990 Oct;153:85-104. doi: 10.1242/jeb.153.1.85. J Exp Biol. 1990. PMID: 2280230 Review. - Competitive interactions between retinal ganglion cells during prenatal development.
Shatz CJ. Shatz CJ. J Neurobiol. 1990 Jan;21(1):197-211. doi: 10.1002/neu.480210113. J Neurobiol. 1990. PMID: 2181063 Review. - Axon trajectories and pattern of terminal arborization during the prenatal development of the cat's retinogeniculate pathway.
Sretavan DW, Shatz CJ. Sretavan DW, et al. J Comp Neurol. 1987 Jan 15;255(3):386-400. doi: 10.1002/cne.902550306. J Comp Neurol. 1987. PMID: 3819020
Cited by
- Epigenetic signature in neural plasticity: the journey so far and journey ahead.
Nayak M, Das D, Pradhan J, Ahmed RG, Laureano-Melo R, Dandapat J. Nayak M, et al. Heliyon. 2022 Dec 19;8(12):e12292. doi: 10.1016/j.heliyon.2022.e12292. eCollection 2022 Dec. Heliyon. 2022. PMID: 36590572 Free PMC article. Review. - Identifying long-range synaptic inputs using genetically encoded labels and volume electron microscopy.
Ayuso-Jimeno IP, Ronchi P, Wang T, Gallori CE, Gross CT. Ayuso-Jimeno IP, et al. Sci Rep. 2022 Jun 17;12(1):10213. doi: 10.1038/s41598-022-14309-4. Sci Rep. 2022. PMID: 35715545 Free PMC article. - Low Frequency Ultrasound With Injection of NMO-IgG and Complement Produces Lesions Different From Experimental Autoimmune Encephalomyelitis Mice.
Xiang W, Xie C, Luo J, Zhang W, Zhao X, Yang H, Cai Y, Ding J, Wang Y, Hao Y, Zhang Y, Guan Y. Xiang W, et al. Front Immunol. 2021 Oct 14;12:727750. doi: 10.3389/fimmu.2021.727750. eCollection 2021. Front Immunol. 2021. PMID: 34721390 Free PMC article. - Activity Shapes Neural Circuit Form and Function: A Historical Perspective.
Pan Y, Monje M. Pan Y, et al. J Neurosci. 2020 Jan 29;40(5):944-954. doi: 10.1523/JNEUROSCI.0740-19.2019. J Neurosci. 2020. PMID: 31996470 Free PMC article. Review. - Neurexin directs partner-specific synaptic connectivity in C. elegans.
Philbrook A, Ramachandran S, Lambert CM, Oliver D, Florman J, Alkema MJ, Lemons M, Francis MM. Philbrook A, et al. Elife. 2018 Jul 24;7:e35692. doi: 10.7554/eLife.35692. Elife. 2018. PMID: 30039797 Free PMC article.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Medical
Research Materials
Miscellaneous