A Synaptic Basis for Small World Network Design in the ON Inner Plexiform Layer of the Rabbit Retina

Bipolar cells_

This abstract was presented today at the 2014 Association for Research in Vision and Opthalmology (ARVO) meetings in Orlando, Florida by J Scott Lauritzen, Noah T. Nelson, Crystal L. Sigulinsky, Nathan Sherbotie, John Hoang, Rebecca L. PfeifferJames R. Anderson, Carl B. Watt, Bryan W. Jones and Robert E. Marc.

Purpose: Converging evidence suggests that large- and intermediate-scale neural networks throughout the nervous system exhibit small world’ design characterized by high local clustering of connections yet short path length between neuronal modules (Watts & Strogatz 1998 Nature; Sporns et al.2004 Trends in Cog Sci). It is suspected that this organizing principle scales to local networks (Ganmor et al. 2011 J Neurosci; Sporns 2006 BioSystems) but direct observation of synapses and local network topologies mediating small world design has not been achieved in any neuronal tissue. We sought direct evidence for synaptic and topological substrates that instantiate small world network architectures in the ON inner plexiform layer (IPL) of the rabbit retina. To test this we mined ≈ 200 ON cone bipolar cells (BCs) and ≈ 500 inhibitory amacrine cell (AC) processes in the ultrastructural rabbit retinal connectome (RC1).

Methods: BC networks in RC1 were annotated with the Viking viewer and explored via graph visualization of connectivity and 3D rendering (Anderson et al. 2011 J Microscopy). Small molecule signals embedded in RC1 e.g. GABA glycine and L-glutamate combined with morphological reconstruction and connectivity analysis allow for robust cell classification. MacNeil et al. (2004 J Comp Neurol) BC classification scheme used for clarity.

Results: Homocellular BC coupling (CBb3::CBb3 CBb4::CBb4 CBb5::CBb5) and within-class BC inhibitory networks (CBb3 → AC –| CBb3 CBb4 → AC –| CBb4 CBb5 → AC –| CBb5) in each ON IPL strata form laminar-specific functional sheets with high clustering coefficients. Heterocellular BC coupling (CBb3::CBb4 CBb4::CBb5 CBb3::CBb5) and cross-class BC inhibitory networks (CBb3 → AC –| CBb4 CBb4 → AC –| CBb3 CBb4 → AC –| CBb5 CBb5 → AC –| CBb4 CBb3 → AC –| CBb5 CBb5 → AC –| CBb3) establish short synaptic path lengths across all ON IPL laminae.

Conclusions: The retina contains a greater than expected number of synaptic hubs that multiplex parallel channels presynaptic to ganglion cells. The results validate a synaptic basis (ie. direct synaptic connectivity) and local network topology for the small world architecture indicated at larger scales providing neuroanatomical plausibility of this organization for local networks and are consistent with small world design as a fundamental organizing principle of neural networks on multiple spatial scales.

Support:  NIH EY02576 (RM), NIH EY015128 (RM), NSF 0941717 (RM), NIH EY014800 Vision Core (RM), RPB CDA (BWJ), Thome AMD Grant (BWJ).

Interesting: The Spatial Organization Of Cholinergic Mosaics In The Adult Mouse Retina

Cholinergic Strettoi

This Short Communication published in the European Journal of Neuroscience back in 2000 by Lucia Galli-Resta, Elena Novelli, Maila Volpini and Enrica Strettoi was a paper I did not know existed.  That said, I ran into it the other day looking for some reference material and found it to be quite useful.  This communication represents an analysis of the cholinergic amacrine cell mosaics in the C57Bl6/J murine retina.  It served as a useful baseline for cell positioning, and cell mosaicing in both cholinergic arrays of the retina and is a nice analysis that should serve as a reference point for future genetic analysis studies in normal and pathological retinal tissues.  Enrica Strettoi’s laboratory has been carefully exploring the functional organization of the retina for some time now in the normal and pathological states and its always a joy to discover her work in the literature, even if it is 13 years old.


Light-Evoked Synaptic Activity of Retinal Ganglion and Amacrine Cells is Regulated in Developing Mouse Retina

This paper by Q. He, Wang P and Ning Tian characterizes the developmental profiles of the light evoked excitatory and inhibitory synaptic inputs from ON and OFF synaptic pathways in the retina, the light evoked synaptic outputs and the sensitivity of the light evoked synaptic inputs and outputs to light deprivation of retinal ganglion cells (RGCs) and displaced amacrine cells (ACs) of developing mouse retina.  The results strongly suggest that spontaneous and light-evoked synaptic activities of RGCs and ACs are regulated by different synaptic mechanisms.

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