Horizontal cells and cone photoreceptors in human retina: A Golgi‐electron microscopic study of spectral connectivity

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Abstract
Connections of the three human horizontal cell (HC) types with overlying cone pedicles have been studied via electron microscopy (EM). Because blue cones (B‐cones) can be recognized on distinctive morphological criteria, we could determine their presence by light microscopy (LM) in the mosaic overlying HC dendritic trees. Then we could confirm the presence or absence of dendritic contacts to B‐cone pedicles by examining EM serial sections and making reconstructions of examples of the three HC types.Three HI cells have been reconstructed. Their dendritic terminals ended as lateral elements of ribbon synapses in green and red cone pedicles (G‐ and R‐cones) primarily. B‐cones pedicles in HI cell dendritic fields received no more than one or two contacts. Six reconstructed HII cells were found to contact all the pedicles within their dendritic field. However, their dendritic reached especially for B‐cones pedicles and innervated them with disproportionately large number of terminals compared with G‐ and R‐cines. HII axons appeared to contact B‐cones exclusively. The four reconstructed HIII cells were found to avoid completely B‐cones in their dendritic fields.Data have been collected on synaptic ribbon lengths at HII and HIII lateral elements in the B‐cone as compared with G‐ and R‐cone pedicles. HIII dendritic terminals end almost exclusively at the smaller ribbons and HI dendrites at the large ribbons. The number of dendritic terminals provided by the HCs to G‐and R‐cone pedicles as compared B‐cone pedicles has been more accurately quantitated than was possible in the LM analysis (accompanying paper).New findings on the morphology of B‐cone pedicles in peripheral retina have revealed that 1) B‐cone pedicles end further vitread in the outer plexiform layer (OPL) than other cone pedicles, thereby forming a sublayer of the OPL neuropil, here named OPLb, in comparison to OPLa, where the G‐ and R‐cone pedicles end; 2) B‐cone pedicles have very few telodentrial connections; and 3) in peripheral retina (probably beyond 8 mm from the fovea to the ora serrata), they are bi‐ or trilobed, with each lobe containing separate synaptic invaginations. The vitread position and unique morphology of B‐cone pedicles appear to relate directly to the unique morphology and unusual connectivity patterns of both their B‐cone‐specific bipolar and B‐cone‐related horizontal cell, the HII cell. Taken together with the LM and quantitative data of our two preceding papers, these findings provide morphological evidence that a chromatically selective weighting pattern in HCs and could play a role in color‐opponent surround formation in the human retina.