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The Journal of Neuroscience, September 22, 2004, 24(38):8366-8378; doi:10.1523/JNEUROSCI.1063-04.2004

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Behavioral/Systems/Cognitive
Evidence That Each S Cone in Macaque Fovea Drives One Narrow-Field and Several Wide-Field Blue-Yellow Ganglion Cells

Stan Schein,^1,2 Peter Sterling,³ Ivy Tran Ngo,¹ Teresa M. Huang,¹ and Steve Herr¹

¹Department of Psychology, University of California, Los Angeles (UCLA), Los Angeles, California 90095-1563, ²Brain Research Institute, UCLA, Los Angeles, California 90095-1761, and ³Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104

A rule of retinal wiring is that many receptors converge onto fewer bipolar cells and still fewer ganglion cells. However, for each S cone in macaque fovea, there are two S-cone ON bipolar cells and two blue-yellow (BY) ganglion cells. To understand this apparent rule reversal, we reconstructed synaptic patterns of divergence and convergence and determined the basic three-tiered unit of connectivity that repeats across the retina. Each foveal S cone diverges to four S-cone ON bipolar cells but contacts them unequally, providing 1–16 ribbon synapses per cell. Next, each bipolar cell diverges to two BY ganglion cells and also contacts them unequally, providing 14 and 28 ribbon synapses per cell. Overall, each S cone diverges to approximately six BY ganglion cells, dominating one and contributing more modestly to the others. Conversely, of each pair of BY ganglion cells, one is dominated by a single S cone and one is diffusely driven by several. This repeating circuit extracts blue/yellow information on two different spatiotemporal scales and thus parallels the circuits for achromatic, spatial vision, in which each cone dominates one narrow-field ganglion cell (midget) and contributes some input to several wider-field ganglion cells (parasol). Finally, because BY ganglion cells have coextensive +S and –(L+M) receptive fields, and each S cone contributes different weights to different BY ganglion cells, the coextensive receptive fields must be already present in the synaptic terminal of the S cone. The S-cone terminal thus constitutes the first critical locus for BY color vision.

View larger version (85K): [in this window] [in a new window]   Figure 1. Foveal S-coneterminals express more than 20 active zones and contact more than 30 S-cone ON bipolar cell dendrites provided by four or five bipolar cells. In these stereo reconstructions of the synaptic surfaces of two foveal S cones, each cluster of yellow spheres indicate the site where a synaptic ribbon anchored to the presynaptic membrane. Thus, each cluster marks an active zone (numbered) where synaptic vesicles were released. Each active zone was presynaptic to a triad of postsynaptic processes, but the regions occupied by horizontal cell spines were excised (see Materials and Methods). Here, we show only the central processes (i.e., the ON bipolar cell dendrites) as colored patches. A, Terminal 35 contained 24 active zones that were presynaptic to 31 central elements from four different S-cone ON bipolar cells. Each color codes for a different bipolar cell, with each bipolar cell providing the number of central elements indicated in Figure 2 (see also Herr et al., 2003, their Table 2A). B, Terminal 52 (modified from Herr et al., 2003, their Fig. 9B) contained 25 active zones that were presynaptic to 43 central elements from five different S-cone ON bipolar cells, with numbers provided in Figure 2. Of five (orange) triad-associated contacts, 1, 2, 1, and 1 are provided by the bipolar cells colored green, blue, yellow, and cyan, respectively; two of these contacts are visible in this view.

 

Key words: retina; vision; cone; retinal ganglion cell; synapse; color vision; ribbon synapses; short-wavelength-sensitive cones

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Received March 22, 2004; revised August 11, 2004; accepted August 11, 2004.

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