Brett A. Szmajda

Retinal ganglion cell inputs to the koniocellular pathway

To understand the transmission of sensory signals in visual pathways we studied the morphology and central projection of ganglion cell populations in marmoset monkeys. Retinal ganglion cells were labeled by photofilling following injections of retrograde tracer in the lateral geniculate nucleus (LGN), or by intracellular injection with neurobiotin. Ganglion cell morphology was analyzed using hierarchical cluster analysis. In addition to midget and parasol ganglion cells, this method distinguished three main clusters of wide‐field cells that correspond to small bistratified, sparse, and broad thorny cells identified previously. The small bistratified and sparse cells occupy neighboring positions on the hierarchical (linkage distance) tree. These cell types are presumed to carry signals originating in short‐wavelength sensitive (S or “blue”) cones in the retina. The linkage distance from these putative S‐cone pathway ganglion cells to other wide‐field cells is similar to the linkage distance from midget cells to parasol cells, suggesting that S‐cone cells form a distinct functional subgroup of ganglion cells. Small bistratified cells and large sparse cells were the most commonly labeled wide‐field cells following LGN injections in koniocellular layer K3. This is consistent with physiological evidence that the role of this layer includes transmission of S‐cone signals to the visual cortex. Other wide‐field cell types were also labeled following injections including K3, and other koniocellular LGN layers; these cell types may correspond to “non‐blue koniocellular” receptive fields recorded in physiological studies. J. Comp. Neurol. 510:251–268, 2008.

Receptive field asymmetries produce color-dependent direction selectivity in primate lateral geniculate nucleus

Blue-on receptive fields recorded in primate retina and lateral geniculate nucleus are customarily described as showing overlapping blue-on and yellow-off receptive field components. However, the retinal pathways feeding the blue-on and yellow-off subfields arise from spatially discrete receptor populations, and recent studies have given contradictory accounts of receptive field structure of blue-on cells. Here we analyzed responses of blue-on cells to drifting gratings, in single-cell extracellular recordings from the dorsal lateral geniculate nucleus in marmosets. We show that most blue-on cells exhibit selectivity for the drift direction of achromatic gratings. The standard concentric difference-of-Gaussians (DOG) model thus cannot account for responses of these cells. We apply a simple, anatomically plausible, extension of the DOG model. The model incorporates temporally offset elliptical two-dimensional Gaussian subfields. The model can predict color-contingent direction and spatial tuning. Because direction tuning in blue-on cells depends on stimulus chromaticity, spatial frequency, and temporal frequency, this property is of little value as a general mechanism for image movement detection. It is possible that anatomical wiring for color selectivity has constrained the capacity of blue-on cells to contribute to spatial and motion vision.

Geniculocortical relay of blue-off signals in the primate visual system

A fundamental dichotomy in the subcortical visual system exists between on- and off-type neurons, which respectively signal increases and decreases of light intensity in the visual environment. In primates, signals for red-green color vision are carried by both on- and off-type neurons in the parvocellular division of the subcortical pathway. It is thought that on-type signals for blue-yellow color vision are carried by cells in a distinct, diffusely projecting (koniocellular) pathway, but the pathway taken by blue-off signals is not known. Here, we measured blue-off responses in the subcortical visual pathway of marmoset monkeys. We found that the cells exhibiting blue-off responses are largely segregated to the koniocellular pathway. The blue-off cells show relatively large receptive fields, sluggish responses to maintained contrast, little sign of an inhibitory receptive-field surround mechanism, and negligible functional input from an intrinsic (melanopsin-based) phototransductive mechanism. These properties are consistent with input from koniocellular or “W-like” ganglion cells in the retina and suggest that blue-off cells, as previously shown for blue-on cells, could contribute to cortical mechanisms for visual perception via the koniocellular pathway.

Transmission of blue (S) cone signals through the primate lateral geniculate nucleus

This study concerns the transmission of short‐wavelength‐sensitive (S) cone signals through the primate dorsal lateral geniculate nucleus. The principal cell classes, magnocellular (MC) and parvocellular (PC), are traditionally segregated into on‐ and off‐subtypes on the basis of the sign of their response to luminance variation. Cells dominated by input from S‐cones (‘blue‐on and blue‐off’) are less frequently encountered and their properties are less well understood. Here we characterize the spatial and chromatic properties of a large sample of blue‐on and blue‐off neurons and contrast them with those of PC and MC neurons. The results confirm that blue‐on and blue‐off cells have larger receptive fields than PC and MC neurons at equivalent eccentricities. Relative to blue‐on cells, blue‐off cells are less sensitive to S‐cone contrast, have larger receptive fields, and show more low‐pass spatial frequency tuning. Thus, blue‐on and blue‐off neurons lack the functional symmetry characteristic of on‐ and off‐subtypes in the MC and PC pathways. The majority of MC and PC cells received no detectible input from S‐cones. Where present, input from S‐cones tended to provide weak inhibition to PC cells. All cell types showed evidence of a suppressive extra‐classical receptive field driven largely or exclusively by ML‐cones. These data indicate that S‐cone signals are isolated to supply the classical receptive field mechanisms of blue‐on and blue‐off cells in the LGN, and that the low spatial precision of S‐cone vision has origins in both classical and extraclassical receptive field properties of subcortical pathways.

Specificity of M and L Cone Inputs to Receptive Fields in the Parvocellular Pathway: Random Wiring with Functional Bias

Many of the parvocellular pathway (PC) cells in primates show red–green spectral selectivity (cone opponency), but PC ganglion cells in the retina show no anatomical signs of cone selectivity. Here we asked whether responses of PC cells are compatible with “random wiring” of cone inputs. We measured long-wavelength-sensitive (L) and medium-wavelength-sensitive (M) cone inputs to PC receptive fields in the dorsal lateral geniculate of marmosets, using discrete stimuli (apertures and annuli) to achieve functional segregation of center and surround. Receptive fields between the fovea and 30° eccentricity were measured. We show that, in opponent PC cells, the center is dominated by one (L or M) cone type, with normally <20% contribution from the other cone type (high “cone purity”), whereas non-opponent cells have mixed L and M cone inputs to the receptive field center. Furthermore, opponent response strength depends on the overall segregation of L and M cone inputs to center and surround rather than exclusive input from one cone type to either region. These data are consistent with random wiring. The majority of PC cells in both foveal (<8°) and peripheral retina nevertheless show opponent responses. This arises because cone purity in the receptive field surround is at least as high as in the center, and the surround in nearly all opponent PC cells is dominated by the opposite cone type to that which dominates the center. These functional biases increase the proportion of opponent PC cells, but their anatomical basis is unclear.

Transmission of colour and acuity signals by parvocellular cells in marmoset monkeys

Non‐technical summary  Colour gets a free ride, according to our study of visual nerve cell responses in marmoset monkeys. All male marmosets are red–green colour‐blind (dichromatic), but most female marmosets have normal trichromatic colour vision. It is known that signals for high‐acuity daytime vision are carried in the parvocellular (P) pathway, and the P pathway also carries signals for red–green colour vision in trichromats. Here we compared P cell responses with patterned stimuli in dichromatic and trichromatic marmosets, and found no detectable difference in resolving power for fine patterns. These results indicate that red–green colour vision does not come at a cost for spatial vision. The ‘piggyback ride’ for colour signals in the P pathway may have encouraged the evolution of full colour vision in primates, including great apes, monkeys and humans.