S-cone pathways
[General characteristics]
[Blue cones]
[S-cone bipolar cell]
[S-cone horizontal cell]
[S-cone ganglion cell]
[Circuits for the S-cone pathways]
[References]
1. General characteristics.
Over the last few years, psychophysicists, electrophysiologists,
geneticists and anatomists have concluded that there is something unique
about
the short wavelength system compared with the two longer wavelength
systems in
the visual system.
There are differences in the genetic structure and locus of
the S-cone visual pigment compared with the L- and M-cone pigments
(Nathans et
al., 1986), yet the S-cones are common to all vertebrate retinas and
always
form a consistent 8-10% of the cone photoreceptor population (Marc, 1982;
Kolb
and Lipetz, 1991).The S-cones are however, very few in the fovea center
so
causing a so-called S-cone blind spot (Williams et al., 1981) but they
peak in
number on the foveal slope at about 12% of the population (Fig. 2).
The pathways for transmitting information from the short wavelength cones to ganglion cells appears to be different from the midget pathways for the medium and long wavelength cones. As we have discussed in a previous chapter, the latter two chromatic pathways are via midget bipolar and midget ganglion cells connections related to a single spectral type of cone, either L- or M-cones.
2. Blue cones.
Of the three spectral types of cone found in the normal human retina,
only the
S-cone or blue cone can be distinguished from the others in the mosaic.
Using special antibodies generated against cone opsins, which are the visual
pigments contained within the cone, it is possible to selectively stain the short wavelength sensitive pigment- (or blue pigment) bearing cones (Fig. 3) (Szell et al., 1988; Ahnelt and Kolb, 2000).
They are distinguished from other cones in the fovea by their
larger inner segment diameter and their occurrence in a different mosaic than
the the more numerous hexagonally packed L- and M-cones. Thus the S-cones seem to
break up the regular hexagonal array into small distorted patches of the other
cones (Fig. 1).
 Fig. 4. Blue cone in a vertical section through human retina (59 K jpeg image) |
 Fig. 5. Schematic drawing of a blue cone (59 K jpeg image) |
In vertical sections of human retina the S-cone is recognized by having a longer inner segment that sticks further into subretinal space than neighboring cones (Fig. 4). It also has a narrower "waist" at the outer limiting membrane than neighboring cones and often sits adjacent to another cone cell body without intervening rods. Pedicles belonging to S-cones project deeper into the outer plexiform layer (OPL) and have a smaller or unusual shaped pedicle compared with other cone pedicles (Figs. 4 and 5) (Ahnelt and Kolb, 1994; Kolb et al.,1997).
In peripheral retina. S-cone pedicles are bilobed in shape, with synaptic invaginations and ribbons separated to the two lobes (Fig. 6). They do not exhibit the long telodendria typical of other cone pedicles so they remain rather isolated from gap junction contacts with L- or M-cones at the level of the outerplexiform layer (Kolb et al., 1997).
Fig. 6. 3D computer reconstructions of an S-cone pedicle (59 K jpeg image)
3. S-cone bipolar cell.
The S-cone pedicle is only contacted by a special S-cone bipolar cell,
that was originally described by Mariani (1984) and shown later to be
selectively stainable with antibodies to the peptide cholecystokinin (Kouyama and Marshak,1992). This bipolar is not like other midget bipolar cells, although in the central retina it is related mostly to a single S-cone (Kouyama and Marshak,1992). It differs primarily in its axonal ending in the inner plexiform layer, from the regular midget bipolar cells that contact M- and L-cones. The S-cone bipolar axon ends deep in the IPL with a long ranging terminal that runs amongst the rod bipolar axon terminals in stratum 5 (Fig. 7).
The S-cone bipolar cell makes an invaginating ribbon junction with the cone pedicle as well as a basal junction type of contact (Fig. 6, violet profile, sb). A small number of additional fine bipolar dendrites make basal junction contacts only (Fig. 6. green profile, fb), and so belong to some other kind of diffuse bipolar type, possibly one called GBB: a giant bistratified type (Fig. 7) (Mariani, 1983). The HII horizontal cells make many of the lateral element contacts with the S-cone in both lobes (Fig. 6, orange profiles, HII). A small number of contacts come from HI cells (Fig. 6, red profiles, HI) (Ahnelt and Kolb, 1994).
4. S-cone horizontal cell
Originally there was thought to be only one type of horizontal cell in the primate retina; a long-axoned cell type that connected with cones at its dendrites and rods at its axonal endings (Polyak, 1941, Boycott and Dowling, 1969; Kolb, 1970). However, in 1980 a second type of horizontal cell was described (Kolb et al., 1980) and proposed to be more concerned with S-cones than the original long-axoned HI type. The HII cell was distinguished on its bushy dendritic tree with fine irregular dendrites and without clear clusters destined for cones (Fig. 8a, compare H1 and H2 cells morphology). Electron microscopy finally showed that the HII type of horizontal cell indeed sent many dendritic processes to the few S-cones in its dendritic field and lesser concentrations of processes to overlying M- and L-cones. The short axons of these HII cells contact S-cones exclusively (Fig. 8b) (Ahnelt and Kolb, 1994). Intracellular recordings from H2 horizontal cells in monkey retina have proved conclusively that this horizontal cell is blue sensitive and an important element of the S-cone pathway in the primate retina (Dacey et al., 1996).
 Fig. 8a. Comparisons of HI and HII cells in primate retina. Golgi staining. (59 K jpeg image) |
 Fig. 8b. Schematic of the S-cone specific HII horizontal cell in primate retina. (59 K jpeg image) |
It has been demonstrated that horizontal cells produce negative feedback
to cones (Baylor et al., 1971; Fuortes and Simon, 1974; Burkhardt, 1993) and
are engaged in center surround generation in bipolar cells, and color
opponent responses in horizontal cells of animals with good color vision (Fourtes and Simon 1974). In the case of the HI and HII horizontal cells of the
primate retina. it has been difficult to demonstrated color opponency in
intracellular recording and dye-markings (Dacey et al., 1996) although anatomically we know there is color selectivity of their contacts (Ahnelt and Kolb, 1994). Dacey and coauthors (1996) concluded that HII cells, which of course make contact with L- and M-cones too, but are primarily concerned with S-cones, do not engage in feedback signals with the longer wavelength cones. However, it is possible that HII cells feed-back only to their S-cones, thereby forming opponency in the S-cones themselves and their S-cone bipolar cells. This should result in an opponent
S-cone bipolar S-ON, L-/M-OFF (blue ON/yellow OFF) channel that could be
carried straight to the ganglion cells (Fig. 9).
5. S-cone ganglion cell.
Early electrophysiological investigation of monkey retinal ganglion
cells indicated that blue/yellow opponency was carried primarily by a S-cone ON center ganglion cell type with a much larger receptive field center than is typical of the L- or M-cone color and spatially opponent midget ganglion cells (Gouras 1984). The S-cone ganglion cell did not appear to have a spatially antagonistic receptive field structure. Instead the yellow opponency was coextensive with the center of the receptive field. Interestingly there are very few recordings of the opposite type of ganglion cell i.e. yellow-ON and blue-OFF.
Fig. 10. Physiology of S-cone ganglion cell (59 K jpeg image)
The morphology of the blue ON/yellow OFF ganglion cell has been known since Dacey and Lee (1994) made intracellular recordings and staining of these ganglion cells in monkey retina. It turns out to be a relatively small-field bistratified ganglion cell (Dacey, 1993) with its major dendritic branching in stratum 5 of the IPL and a small tier of dendrites in stratum 1 of the IPL (Fig. 10).
6. Circuits for the S-cone pathways in the primate retina.
Hypothetical wiring diagrams of the S-cone pathway through the primate
retina in comparison with the L- and M-cone midget pathways are shown in Figure 11. The S-cone bipolar would carry ON signals to the lower dendrites of the bistratified ganglion cell which may be the dominant input. It is possible, though that the bipolar is already S-ON and yellow-OFF, in response due to the HII cell influence as mentioned above. Then both ON and OFF spectrally antagonistic components would drive the ganglion cell. However, the yellow OFF response could also be complimented by an OFF bipolar, that contacts L- and M-cones as well, making synapses upon the upper dendrites of the bistratified ganglion cell (Fig. 11).
Fig. 11. Hypothetical wiring diagrams of the S-cone pathways (59 K jpeg image)
7. References.
Ahnelt, P.K., Kolb, H. and Pflug, R. (1987) Identification of a subtype
of cone
photoreceptor, likely to be blue sensitive, in the human retina. J. Comp.
Neurol. 255, 18-34.
Ahnelt, P. and Kolb, H. (1994) Horizontal cells and cone photoreceptors
in human retina: a Golgi-electron microscopic study of spectral
connectivity. J. Comp. Neurol. 343, 406-427.
Ahnelt, P. and Kolb, H. (2000) The mammalian photoreceptor mosaic- adaptive design. Prog. Ret. & Eye Res. 19, 711-777.
Baylor, D.A., Fuortes, M.G.F. and O'Bryan, P.M. (1971) Receptive fields
of the cones in the retina of the turtle. J. Physiol., (Lond.) 214,
265-294.
Boycott, B.B. and Dowling, J.E. (1969) Organization of the primate retina: Light microscopy. Phil. Trans. Roy. Soc. (Lond) B, 255, 109-184.
Dacey, D.M. (1993) Morphology of a small-field bistratified ganglion
cell type in the macaque and human retina. Vis. Neurosci. 10, 1081-1089.
Dacey, D.M. and Lee, B.B. (1994) The 'blue-on' opponent pathways in
primate
retina originates from a distinct bistratified ganglion cell. Nature
367, 731-735.
Dacey, D.M., Lee, B.B., Stafford, D.K., Pokorny, J. and Smith, V.C.
(1996)
Horizontal cells of the primate retina: cone specificity without spectral
opponency. Science 271, 656-659.
Dacey, D.M., Peterson, B.B., Gamlin, P.D. and Robinson, F.R. (2001) Retrograde photofilling reveals the complete morphology of diverse new ganglion cell types that project to the lateral geniculate nucleus in macaque monkey. Invest. Ophthal. Vis. Sci. ARVO abstr. 42, p.
Fuortes, M.G.F. and Simon, E.J. (1974) Interactions leading to horizontal
cell
responses in the turtle retina. J. Physiol (Lond) 240, 177-199.
Gouras, P. (1968) Identification of cone mechanisms in monkey ganglion
cells.
J. Physiol. (Lond.) 199, 533-547.
Gouras, P. (1992) Retinal circuitry and its relevance to diagnostic
psychophysics and electrophysiology. Current Opin. Ophthalmol. 3,
803-812.
Gouras, P. and Zrenner, E. (1981) Color vision: A review from a
neurophysiological perspective. In "Progress in Sensory Physiology"
1,
(Autrum, H., Ottoson, D., Perl, E.R. and Schmidt, R.F., Eds),
Springer-Verlag,
Berlin Heidelberg New York pp.139-179.
Humanski, R.A. and Wilson, H.R. (1992) Spatial frequency mechanisms with
short-wavelength-sensitive cone inputs. Vision Res. 32,
549-560.
Kolb, H. 1970 Organization of the outer plexiform layer of the primate retina: Electron microscopy of Golgi-impregnated cells. Phil. Trans. Roy. Soc. (Lond) B, 258, 261-283.
Kolb, H., Mariani, A. and Gallego, A. (1980) A second type of horizontal cell in the monkey retina. J. Comp. Neurol., 189, 31-44.
Kolb, H. and Lipetz, L.E. (1991) The anatomical basis for colour vision
in the
vertebrate retina. In :Vision and Visual Dysfunction volume 6: "The
Perception
of Colour". (Ed. Gouras, P.) Macmillan Press Ltd., London. 6, 128-145.
Kolb, H., Goede, P. Roberts, S., McDermott, R. and Gouras, P. (1997) The
uniqueness of the S-cone pedicle in the human retina and consequences for
color
processing. J. Comp. Neurol. submitted.
Kouyama, N. and Marshak, D.W. (1992) Bipolar cells specific for blue
cones in
the macaque retina. J. Neurosci. 12, 1233-1252.
Lennie, P. (1984) Recent developments in the physiology of color vision.
Trends
in Neurosci. 5, 243-248.
Marc, R.E. (1982) Chromatic organization of the retina. In "Cell Biology
of the
Eye" (M. LaVail and J. Hollyfield, Eds), Academic Press, New York. pp.
435-473.
Mariani, A.P. (1983) Giant bistratified bipolar cells in the monkey
retina.
Anat. Rec. 206, 215-220.
Mariani, A.P. (1984) Bipolar cells in monkey retina selective for cones
likely
to be blue-sensitive. Nature 308, 184-186.
Nathans, J., Thomas, D. and Hogness, D.S. 1986 Molecular genetics of
human
color vision: The genes encoding the blue, green and red pigments.
Science,
232, 193-202.
Polyak, S.L. (1941) The Retina. University of Chicago Press, Chicago.
Rodieck, R.W. (1991) In "From pigments to perception" (Eds. Valberg, A.
and
Lee, B.B.), Plenum, New York, pp. 83-94.
Stockman, A., MacLeod, D.I.A. and DePriest, D.D. (1991) The temporal
properties
of the human short-wave photoreceptors and their associated pathways.
Vision
Res. 31, 189-208.
Szel, A., Diamanstein, T. and Röhlich, P. (1988) Identification of
blue-sensitive cones in the mammalian retina by antivisual pigment
antibody. J.
Comp. Neurol. 273, 593-602.
Williams, D.R., MacLeod, D.I.A. and Hayhoe, M. (1981) Punctate
sensitivity of
the blue-sensitive mechanisms. Vision Res. 21, 1357-1375.
[General characteristics]
[Blue cones]
[S-cone bipolar cell]
[S-cone horizontal cell]
[S-cone ganglion cell]
[Circuits for the S-cone pathways]
[References]
