Synaptic Origins of Color and Luminance Coding in the Primate Retina
The profound and seamless unity of our visual experience arises not from a simple, point-by-point reproduction of an image optically projected onto the retina, but instead from interactions among a myriad of neurons, circuits and synapses to form a precise set of parallel pathways that extract information, piecemeal, from the rain of photons continuously bombarding our eyes. These 'parallel pathways' for the unique color-coding, trichromatic primate, an ideal model for its human counterpart, have been defined anatomically, setting the stage for understanding how neural structure gives rise to function in one particularly accessible outpost of the central visual system, the neural retina (Chapter 1). My thesis work applies extra- and intracellular physiology together with pharmacological manipulation to a unique in vitro macaque monkey retina and represents the first use of sophisticated visual stimuli, which can isolate spectrally distinct photoreceptor signals, to tease apart the synaptic basis for chromatic and luminance pathways. My work begins with the key outstanding questions about the three best-studied visual pathways in the primate. The 'midget' pathway transmits a 'red-green' and a critical, lumiance signal that sets the limit on visual acuity: I directly address for the first time, the synaptic mechanisms that give rise to this unique 'double-duty' performance. Specifically I test the hypothesis for color selective inhibition and define a new type of 'spatio-chromatic' receptive field structure critical for understanding how opponency and luminance coding arise from a single circuit (Chapter 2). A 'blue-yellow' pathway originates from a distinctive 'bistratified' ganglion cell: I directly test for the first time, and dramatically confirm, the ON-OFF pathway excitatory hypothesis for color-coding (Chapter 3). The 'parasol' pathway transmits an achromatic signal but its role in object motion has been controversial; I found that parasols cells show non-linear spatial summation, a critical property for higher order motion detection (Chapter 4). Finally, I characterize a new, achromatic visual pathway, the 'smooth monostratified' cell (Chapter 5); the similarities of the smooth with the parasol pathway leads to a new hypothesis about how and why the retina utilizes a plurality of parallel visual pathways.