Abstract
In the primate retina, ‘blue cone’ bipolar cells make invaginating synaptic contacts exclusively with short (S) wavelength sensitive cones1. This pathway is the origin of excitatory S-ON input to the blue-yellow opponent small bistratified ganglion cell type2. An S-OFF pathway has been characterized in the lateral geniculate nucleus (LGN)3 but its retinal origin has remained contentious4,5. The question was apparently answered when serial EM reconstruction in macaque retina found that S cones made basal contacts with OFF-midget bipolars, establishing an S-OFF midget pathway6. However, a later study failed to confirm this connection in marmoset7, and recent LGN recordings suggested that S-OFF signals do not originate from midget pathway cells8.
Here we use serial block-face scanning electron microscopy to reconstruct S-cone connectivity in a patch of macaque foveal retina. We identified 17 S cones in a patch of 169 cone pedicles. S cones were identified by a lack of telodendritic contacts with neighboring cones and confirmed by showing that all ON bipolar contacts arise from distinct ‘blue-cone’ bipolar cells. All S cone pedicles were also densely contacted by OFF bipolar cells. The great majority of these OFF contacts arose from midget bipolar cells. We found each S cone presynaptic to a single OFF-midget bipolar, which in turn was presynaptic to an OFF midget ganglion cell, unequivocally establishing an OFF-midget circuit for each S cone.
We conclude that the S-OFF midget pathway is the origin of S-OFF signals observed at higher synaptic levels9 and utilized in the detection of S cone decrements10.
Meeting abstract presented at the 2016 OSA Fall Vision Meeting