Dataset Information

Efficient Coding by Midget and Parasol Ganglion Cells in the Human Retina.

ABSTRACT: In humans, midget and parasol ganglion cells account for most of the input from the eyes to the brain. Yet, how they encode visual information is unknown. Here, we perform large-scale multi-electrode array recordings from retinas of treatment-naive patients who underwent enucleation surgery for choroidal malignant melanomas. We identify robust differences in the function of midget and parasol ganglion cells, consistent asymmetries between their ON and OFF types (that signal light increments and decrements, respectively) and divergence in the function of human versus non-human primate retinas. Our computational analyses reveal that the receptive fields of human midget and parasol ganglion cells divide naturalistic movies into adjacent spatiotemporal frequency domains with equal stimulus power, while the asymmetric response functions of their ON and OFF types simultaneously maximize stimulus coverage and information transmission and minimize metabolic cost. Thus, midget and parasol ganglion cells in the human retina efficiently encode our visual environment.

SUBMITTER: Soto F

PROVIDER: S-EPMC7442669 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Publications

Efficient Coding by Midget and Parasol Ganglion Cells in the Human Retina.

Soto Florentina F Hsiang Jen-Chun JC Rajagopal Rithwick R Piggott Kisha K Harocopos George J GJ Couch Steven M SM Custer Philip P Morgan Josh L JL Kerschensteiner Daniel D

Neuron 20200612 4

In humans, midget and parasol ganglion cells account for most of the input from the eyes to the brain. Yet, how they encode visual information is unknown. Here, we perform large-scale multi-electrode array recordings from retinas of treatment-naive patients who underwent enucleation surgery for choroidal malignant melanomas. We identify robust differences in the function of midget and parasol ganglion cells, consistent asymmetries between their ON and OFF types (that signal light increments and ...[more]

PMID: 32533915

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Project description:In the trichromatic primate retina, the "midget" retinal ganglion cell is the classical substrate for red-green color signaling, with a circuitry that enables antagonistic responses between long (L)- and medium (M)-wavelength-sensitive cone inputs. Previous physiological studies showed that some OFF midget ganglion cells may receive sparse input from short (S)-wavelength-sensitive cones, but the effect of S-cone inputs on the chromatic tuning properties of such cells has not been explored. Moreover, anatomical evidence for a synaptic pathway from S cones to OFF midget ganglion cells through OFF midget bipolar cells remains ambiguous. In this study, we address both questions for the macaque monkey retina. First, we used serial block-face electron microscopy to show that every S cone in the parafoveal retina synapses principally with a single OFF midget bipolar cell, which in turn forms a private-line connection with an OFF midget ganglion cell. Second, we used patch electrophysiology to characterize the chromatic tuning of OFF midget ganglion cells in the near peripheral retina that receive combined input from L, M, and S cones. These "S-OFF" midget cells have a characteristic S-cone spatial signature, but demonstrate heterogeneous color properties due to the variable strength of L, M, and S cone input across the receptive field. Together, these findings strongly support the hypothesis that the OFF midget pathway is the major conduit for S-OFF signals in primate retina and redefines the pathway as a chromatically complex substrate that encodes color signals beyond the classically recognized L versus M and S versus L+M cardinal mechanisms.SIGNIFICANCE STATEMENT The first step of color processing in the visual pathway of primates occurs when signals from short (S)-, middle (M)-, and long (L)-wavelength-sensitive cone types interact antagonistically within the retinal circuitry to create color-opponent pathways. The midget (L versus M or "red-green") and small bistratified (S vs L+M, or "blue-yellow") ganglion cell pathways appear to provide the physiological origin of the cardinal axes of human color vision. Here we confirm the presence of an additional S-OFF midget circuit in the macaque monkey fovea with scanning block-face electron microscopy and show physiologically that a subpopulation of S-OFF midget cells combine S, L, and M cone inputs along noncardinal directions of color space, expanding the retinal role in color coding.

Dataset Information

Efficient Coding by Midget and Parasol Ganglion Cells in the Human Retina.

Publications

Efficient Coding by Midget and Parasol Ganglion Cells in the Human Retina.

Similar Datasets

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