Amacrine cell inputs to OFF midget ganglion cells in macaque retina

Abstract

In primates, the OFF midget retinal ganglion cells (OFF mRGCs) have a high spatial density and small dendritic arbors. Their axons provide input to the parvocellular pathway mediating both colour vision and the highest-acuity spatial vision. This study aimed to understand the basis for their light responses by identifying the presynaptic amacrine and bipolar cells. Retinal tissue from an adult macaque was processed for serial block-face scanning electron microscopy, and a volume of images of the inner retina located 2 mm temporal to the centre of the fovea was analysed. Ten OFF mRGCs and many of their presynaptic cells were reconstructed. Both midget and diffuse types of bipolar cells provided excitatory, glutamatergic input. Axons and long dendrites of wide-field amacrine cells made synapses, and we propose that these mediate tonic, GABAergic inhibition. Narrow-field amacrine cells also made synapses onto the OFF mRGCs, and we propose that most of them are glycinergic, inhibitory synapses. One presynaptic narrow-field amacrine cell was the knotty bistratified type 1 (KB1), which contains immunoreactive glycine and vesicular glutamate transporter 3. We propose that they enlarge the receptive field centers of OFF mRGCs via direct, excitatory synapses. The KB1 cell studied most extensively was presynaptic to some of the same types of amacrine cells that made inhibitory synapses onto OFF mRGCs. We propose that the knotty bistratifed type 1cells release glycine at those synapses and disinhibit responses of OFF mRGCs. KEY POINTS: In primates, OFF midget ganglion cells have the highest spatial density of any projection neurons, and they mediate high acuity vision. Ten of these cells and the neurons providing their inputs were reconstructed from a volume of serial ultrathin sections taken 2 mm temporal to the centre of the macaque fovea. They received the majority of their inputs from amacrine cells, local circuit neurons that are typically inhibitory. One of the presynaptic amacrine cells resembled those containing vesicular glutamate transporter 3, and we propose that they provide excitatory input that enlarges the receptive field centers of OFF midget ganglion cells. They also receive excitatory input from both midget and diffuse bipolar cells. The results provide an explanation for some apparent contradictions between anatomical and physiological studies and are potentially important for understanding the etiology of retinal diseases.

Keywords: amacrine; bipolar; connectomics; dual‐neurotransmitter interneuron; electron microscopy; primate; vesicular glutamate transporter 3 (vGluT3).