Spikes in Mammalian Bipolar Cells Support Temporal Layering of the Inner Retina

  • Light-driven calcium changes were recorded in mouse bipolar cell axon terminals
  • Bipolar cells cluster into ≥eight functional types, which match anatomical types
  • Fast and slow bipolar cells project to the inner retina in an organized manner
  • The fastest bipolar cells generate clear all-or-nothing spikes

In the mammalian retina, 10–12 different cone bipolar cell (BC) types decompose the photoreceptor signal into parallel channels [ 1–8 ], providing the basis for the functional diversity of retinal ganglion cells (RGCs) [ 9 ]. BCs differing in their temporal properties appear to project to different strata of the retina’s inner synaptic layer [ 10, 11 ], based on somatic recordings of BCs [ 1, 2, 4, 12–14 ] and excitatory synaptic currents measured in RGCs [ 10 ]. However, postsynaptic currents in RGCs are influenced by dendritic morphology [ 15, 16 ] and receptor types [ 17 ], and the BC signal can be transformed at the axon terminals both through interactions with amacrine cells [ 18, 19 ] and through the generation of all-or-nothing spikes [ 20–24 ]. Therefore, the temporal properties of the BC output have not been analyzed systematically across different types of mammalian BCs. We recorded calcium signals directly within axon terminals using two-photon imaging [ 25, 26 ] and show that BCs can be divided into ≥eight functional clusters. The temporal properties of the BC output were directly reflected in their anatomical organization within the retina’s inner synaptic layer: faster cells stratified closer to the border between ON and OFF sublamina. Moreover, ≥three fastest groups generated clear all-or-nothing spikes. Therefore, the systematic projection pattern of BCs provides distinct temporal “building blocks” for the feature extracting circuits of the inner retina.