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Robert E. Marc, S. James Lauritzen, Bryan W. Jones, Carl B. Watt, Shoeb Mohammed, James R. Anderson; The Retinal Connectome: Amacrine-Amacrine Networks. Invest. Ophthalmol. Vis. Sci. 2011;52(14):1607.
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© ARVO (1962-2015); The Authors (2016-present)
Chains of amacrine cell (AC) synapses are abundant in the retinal inner plexiform layer (IPL). We sought to discover the cellular networks using these chains and explore the topologies of their signal processing roles by connectomics.
AC networks in the ultrastructural rabbit retinal connectome RC1 were annotated with the Viking viewer and explored by 3D rendering and graph visualization of connectivity (Anderson et al. 2011 The Viking viewer for connectomics: scalable multi-user annotation and summarization of large volume data sets. J Microscopy: [doi: 10.1111/j.1365-2818.2010.03402.x]). RC1 contains embedded small molecule signals, e.g. 4-aminobutyrate (γ) and glycine (G), enabling robust amacrine cell classification. Multiplicative gain was used to assess potency for each motif.
Inhibitory AC-AC chains form at least four fundamental motifs. (1) Crossover is the major AC-AC motif and occurs between rod and cone as well as ON and OFF channels, involving over 30 crossover configurations, 80% of which engage GACs, including AI > AII AC and starburst AC (SAC) > AII AC chains. These data show that AI and AII cells have more complex interactions than previously reported. (2) Nested feedback is prominent within channels in cone bipolar cell (BC) networks where two different γACs are postsynaptic to a BC and at least one is presynaptic to the other AC. (3) Veto channels are formed by GAC and giant γAC synapses on AI AC dendrites in the OFF layer of the IPL. This architecture suggests global control of AI ACs at the near-somatic level. (4) Deeply nested, dense SAC > SAC chains are abundant. If they are inhibitory, they would constrain lateral signal propagation in the SAC network.
Complex AC-AC chains are a central mechanism in fine-grain control of receptive field networks. Crossover networks are abundant and heavily engage GACs. Nested feedback is common in cone but not rod-driven networks, suggesting that they are associated with tuning bipolar cell dynamics. Veto channel architectures, so far, are unique to OFF cone channels targeting AI ACs. Deep homocellular nesting by SACs may play a role in restricting excitation spread. These motifs account for the majority of AC-AC chains.
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