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Quantitative analysis of synaptogenesis in the inner plexiform layer of macaque monkey fovea
J Crooks1, M Okada, A E Hendrickson
1Department of Biological Structure, University of Washington, Seattle 98195, USA.
Insights
In the developing Macaca monkey fovea, bipolar cell synapse formation precedes amacrine cell synapse formation. This developmental sequence differs from rod-dominated retinas, highlighting photoreceptor type
Area of Science:
- Neuroscience
- Developmental Biology
- Ophthalmology
Background:
- Synaptogenesis, the formation of synapses, is crucial for neural circuit development.
- The inner plexiform layer (IPL) of the retina is a key site for visual information processing.
- Understanding the sequence of synaptogenesis in different retinal regions is vital for comprehending visual system development.
Purpose of the Study:
- To quantitatively track synaptogenesis in the inner plexiform layer (IPL) of the developing Macaca monkey fovea.
- To compare the developmental timing of bipolar and amacrine cell synapse formation.
- To investigate the influence of photoreceptor type on retinal synaptogenesis sequences.
Main Methods:
- Quantitative electron microscopy was employed to analyze retinal tissue from fetal day (Fd) 55 to Fd132.
- Vesicle-containing profiles were classified based on the presence of a ribbon (bipolar origin) or junction formation (amacrine/bipolar/unknown).
- Synaptic densities were calculated per 100 square microns at various developmental stages.
Main Results:
- Bipolar cell synaptogenesis begins early (Fd55) and rapidly increases by Fd88, with densities remaining stable by Fd132.
- Amacrine cell synaptogenesis is initially rare but increases significantly by Fd88 and continues to Fd132.
- Bipolar ribbon synapses initially appear in the outer IPL and progress to the inner IPL and throughout, suggesting OFF pathways form before ON pathways.
Conclusions:
- In the Macaca fovea, bipolar synaptogenesis precedes amacrine synaptogenesis.
- The cone-dominated fovea exhibits a distinct synaptogenesis sequence compared to rod-dominated retinas.
- Photoreceptor type likely dictates the synaptic developmental sequence in retinal regions and species.
Abstract:
Synaptogenesis has been tracked by using quantitative electron microscopic methods in the inner plexiform layer (IPL) of the developing Macaca monkey fovea from fetal day (Fd) 55 to Fd132. Vesicle-containing profiles were classified according to whether (1) they contained a ribbon indicating that they originated from a bipolar cell, or (2) the profile formed a junction. Group 2 was further subdivided by morphological characteristics into (2a) amacrine, (2b) bipolar, or (2c) unknown profiles. Ribbon-containing bipolar profiles are clearly identifiable at Fd55 when they occur at a density of 0.9/100 microns2. Bipolar synapses increase rapidly to 4.7/100 microns2 by Fd88, similar to their density at Fd132. Identifiable amacrine profiles forming a junction are rare at Fd55-68. By Fd88, amacrine synaptic density has jumped to 6.7/100 microns2 and continues to increase to 9.5/100 microns2 at Fd132. These quantitative data strongly suggest that, at the Macaca fovea, bipolar synaptogenesis both begins and ends before amacrine synaptogenesis. The large number of immature amacrine synaptic profiles and densities at Fd132 suggests that amacrine synapses continue to form after Fd132. This study confirms that cone-dominated monkey fovea has a different sequence of synaptogenesis than the rod-dominated peripheral retina (Nishimura and Rakic, [1985] J. Comp. Neurol 241:420-434). The data support the concept that synaptic developmental sequence is determined by the type of photoreceptor which dominates a particular retinal region or species. Bipolar ribbon synapses are observed in the outer half of the IPL at Fd55, are present in the inner IPL at Fd60, and then, with increasing age, are found throughout the IPL. This pattern strongly suggests that vertical OFF bipolar pathways form earlier than ON pathways in the IPL. In contrast, amacrine profiles are found throughout the IPL at the youngest ages, with an adult-like banding pattern present by Fd132.