Humans and old world primates have trichromatic color vision based on three spectral types of cone [long-wavelength (L-), middle-wavelength (M-), and short-wavelength (S-) cones]. All other placental mammals are dichromats, and their color vision depends on the comparison of L- and S-cone signals; however, their cone-selective retinal circuitry is still unknown. Here, we identified the S-cone-selective (blue cone) bipolar cells of the mouse retina. They were labeled in a transgenic mouse expressing Clomeleon, a chloride-sensitive fluorescent protein, under the control of the thy1 promoter. Blue-cone bipolar cells comprise only 1-2% of the bipolar cell population, and their dendrites selectively contact S-opsin-expressing cones. In the dorsal half of the mouse retina, only 3-5% of the cones express S-opsin, and they are all contacted by blue-cone bipolar cells, whereas all L-opsin-expressing cones (∼95%) are avoided. In the ventral mouse retina, the great majority of cones express both S- and L-opsin. They are not contacted by blue-cone bipolar cells. A minority of ventral cones express S-opsin only, and they are selectively contacted by blue-cone bipolar cells. We suggest that these are genuine S-cones. In contrast to the other cones, their pedicles contain only low amounts of cone arrestin. The blue-cone bipolar cells of the mouse retina and their cone selectivity are closely similar to primate blue-cone bipolars, and we suggest that they both represent the phylogenetically ancient color system of the mammalian retina.

The Primordial, Blue Cone Color System of the Mouse Retina

The vertebrate retina first evolved some 500 million years ago in ancestral marine chordates. Since then, the eyes of different species have been tuned to best support their unique visuoecological lifestyles. Visual specializations in eye designs, large-scale inhomogeneities across the retinal surface and local circuit motifs mean that all species' retinas are unique. Computational theories, such as the efficient coding hypothesis, have come a long way towards an explanation of the basic features of retinal organization and function; however, they cannot explain the full extent of retinal diversity within and across species. To build a truly general understanding of vertebrate vision and the retina's computational purpose, it is therefore important to more quantitatively relate different species' retinal functions to their specific natural environments and behavioural requirements. Ultimately, the goal of such efforts should be to build up to a more general theory of vision.

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Understanding the retinal basis of vision across species.

Cell types and cell circuits in human and non-human primate retina.

Electrical synapses are found in vertebrate and invertebrate nervous systems. The cellular basis of these synapses is the gap junction, a group of intercellular channels that mediate direct communication between adjacent neurons. Similar to chemical synapses, electrical connections are modifiable and their variations in strength provide a mechanism for reconfiguring neural circuits. In addition, electrical synapses dynamically regulate neural circuits through properties without equivalence in chemical transmission. Because of their continuous nature and bidirectionality, electrical synapses allow electrical currents underlying changes in membrane potential to leak to ‘coupled’ partners, dampening neuronal excitability and altering their integrative properties. Remarkably, this effect can be transiently alleviated when comparable changes in membrane potential simultaneously occur in each of the coupled neurons, a phenomenon that is dynamically dictated by the timing of arriving signals such as synaptic potentials. By way of this mechanism, electrical synapses influence synaptic integration and action potential generation, imparting an additional layer of dynamic complexity to neural circuits. Electrical synapses comprise intercellular channels termed gap junctions and are found in vertebrate and invertebrate nervous systems. In this Review, Pepe Alcami and Alberto Pereda examine the properties of electrical synapses that influence neural circuit dynamics without modifying gap junction conductance.

Beyond plasticity: the dynamic impact of electrical synapses on neural circuits

Synaptic interactions to extract information about wavelength, and thus color, begin in the vertebrate retina with three classes of light-sensitive cells: rod photoreceptors at low light levels, mu...

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Diverse Cell Types, Circuits, and Mechanisms for Color Vision in the Vertebrate Retina.

Neural Mechanisms Mediating Motion Sensitivity in Parasol Ganglion Cells of the Primate Retina

A Color Vision Circuit for Non-Image-Forming Vision in the Primate Retina

Midget retinal ganglion cells make up the majority of foveal ganglion cells in the primate retina. The receptive fields of midget ganglion cells exhibit both spectral and spatial opponency and are implicated in both color and achromatic form vision, yet the exact mechanisms linking their responses to visual perception remain unclear. Efforts to develop color vision models that accurately predict all the features of human color and form vision based on midget ganglion cells provide a case study connecting experimental and theoretical neuroscience, drawing on diverse research areas such as anatomy, physiology, psychophysics, and computer vision. Recent technological advances have allowed researchers to test some predictions of color vision models in new and precise ways, producing results that challenge traditional views. Here, we review the progress in developing models of color-coding receptive fields that are consistent with human psychophysics, the biology of the primate visual system and the response properties of midget retinal ganglion cells.

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Reconciling Color Vision Models With Midget Ganglion Cell Receptive Fields.

Midget retinal ganglion cells (RGCs) are the most common RGC type in the primate retina. Their responses have been proposed to mediate both color and spatial vision, yet the specific links between midget RGC responses and visual perception are unclear. Previous research on the dual roles of midget RGCs has focused on those comparing long (L) vs. middle (M) wavelength sensitive cones. However, there is evidence for several other rare midget RGC subtypes receiving S-cone input, but their role in color and spatial vision is uncertain. Here, we confirm the existence of the single S-cone center OFF midget RGC circuit in the central retina of macaque monkey both structurally and functionally. We investigated the receptive field properties of the S-OFF midget circuit with single cell electrophysiology and 3D electron microscopy reconstructions of the upstream circuitry. Like the well-studied L vs. M midget RGCs, the S-OFF midget RGCs have a center-surround receptive field consistent with a role in spatial vision. While spectral opponency in a primate RGC is classically assumed to contribute to hue perception, a role supporting edge detection is more consistent with the S-OFF midget RGC receptive field structure and studies of hue perception.

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Sara S. Patterson

Papers

Neural Mechanisms Mediating Motion Sensitivity in Parasol Ganglion Cells of the Primate Retina

A Color Vision Circuit for Non-Image-Forming Vision in the Primate Retina

Reconciling Color Vision Models With Midget Ganglion Cell Receptive Fields.

An S-cone circuit for edge detection in the primate retina

Another Blue-ON ganglion cell in the primate retina.