Glutamate spillover between mammalian cone photoreceptors.

Cone photoreceptors transmit signals at high temporal frequencies and mediate fine spatial vision. High-frequency transmission requires a high rate of glutamate release, which could promote spillover to neighboring cells, whereas spatial vision requires that cones within a tightly packed array signal light to postsynaptic bipolar cells with minimal crosstalk. Glutamate spread from the cone terminal is thought to be limited by presynaptic transporters and nearby glial processes. In addition, there is no ultrastructural evidence for chemical synapses between mammalian cones, although such synapses have been described in lower vertebrate retinas. We tested for cone-cone glutamate diffusion by recording from adjacent cone pairs in the ground squirrel retina, and instead found that the glutamate released by one cone during electrical stimulation activates glutamate transporter Cl(-) conductances on neighboring cones. Unlike in other systems, where crosstalk is diminished by increasing the temperature and by moving to a more intact preparation, glutamate spread persisted at physiological temperatures (37°C) and in retinal flat mounts. The glutamate-gated anion conductance in cones has a reversal potential of ∼-30 mV compared with a cone resting potential of ∼-50 mV; thus, crosstalk should have a depolarizing effect on the cone network. Cone-cone glutamate spread is regulated by the physiological stimulus, light, and under physiological conditions can produce a response of ∼2 mV, equivalent to 13-20% of a cone's light response. We conclude that in the absence of discrete chemical synapses, glutamate flows between cones during a light response and may mediate a spatially distributed positive feedback.

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

The red-green axis of colour vision evolved recently in primate evolutionary history. Signals serving red-green colour vision travel together with signals serving spatial vision, in the parvocellular (PC) division of the subcortical visual pathway. However, the question of whether receptive fields of PC pathway cells are specialized to transmit red-green colour signals remains unresolved. We addressed this question in single-cell recordings from the lateral geniculate nucleus of anaesthetized marmosets. Marmosets show a high proportion of dichromatic (red-green colour-blind) individuals, allowing spatial and colour tuning properties of PC cells to be directly compared in dichromatic and trichromatic visual systems. We measured spatial frequency tuning for sine gratings that provided selective stimulation of individual photoreceptor types. We found that in trichromatic marmosets, the foveal visual field representation is dominated by red-green colour-selective PC cells. Colour selectivity of PC cells is reduced at greater eccentricities, but cone inputs to centre and surround are biased to create more selectivity than predicted by a purely 'random wiring' model. Thus, one-to-one connections in the fovea are sufficient, but not necessary, to create colour-selective responses. The distribution of spatial tuning properties for achromatic stimuli shows almost complete overlap between PC cells recorded in dichromatic and trichromatic marmosets. These data indicate that transmission of red-green colour signals has been enabled by centre-surround receptive fields of PC cells, and has not altered the capacity of PC cells to serve high-acuity vision at high stimulus contrast.

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.

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.

Color signals in the primary visual cortex of marmosets.

This study concerns the input from short-wavelength sensitive (S) cone photoreceptors to the primary visual cortex (striate cortex, Brodmann area 17, area V1) in marmosets. Signals from S-cones are thought to reach V1 by way of the koniocellular layers of the dorsal lateral geniculate nucleus. However, it is not known whether the S-cone afferent signals cause selective activation of cytochrome oxidase-rich cortical "blob" domains. To address this question, intrinsic optical signals and extracellular responses of V1 neurons were recorded. Stimuli consisted of drifting achromatic gratings and gratings that stimulated selectively either the S-cones or the medium-long wavelength sensitive (ML) cones. All stimuli produced contrast-dependent activation throughout the imaged regions of V1. The S- and ML-cone-selective stimuli produced activation levels of respectively 30% and 80% of that to achromatic gratings. No spatial variation in the strength of S-cone activation was apparent, and the ratio of S to ML activation was constant across all imaged regions. Consistently, in all of the single neurons recorded from V1, the functional input from S-cones was weaker than the input from ML-cones. We conclude that in the primary visual cortex of marmosets, S-cone signals are uniformly distributed.

First order connections of the visual sector of the thalamic reticular nucleus in marmoset monkeys (Callithrix jacchus).

The thalamic reticular nucleus (TRN) supplies an important inhibitory input to the dorsal thalamus. Previous studies in non-primate mammals have suggested that the visual sector of the TRN has a lateral division, which has connections with first-order (primary) sensory thalamic and cortical areas, and a medial division, which has connections with higher-order (association) thalamic and cortical areas. However, the question whether the primate TRN is segregated in the same manner is controversial. Here, we investigated the connections of the TRN in a New World primate, the marmoset (Callithrix jacchus). The topography of labeled cells and terminals was analyzed following iontophoretic injections of tracers into the primary visual cortex (V1) or the dorsal lateral geniculate nucleus (LGNd). The results show that rostroventral TRN, adjacent to the LGNd, is primarily connected with primary visual areas, while the most caudal parts of the TRN are associated with higher order visual thalamic areas. A small region of the TRN near the caudal pole of the LGNd (foveal representation) contains connections where first (lateral TRN) and higher order visual areas (medial TRN) overlap. Reciprocal connections between LGNd and TRN are topographically organized, so that a series of rostrocaudal injections within the LGNd labeled cells and terminals in the TRN in a pattern shaped like rostrocaudal overlapping "fish scales." We propose that the dorsal areas of the TRN, adjacent to the top of the LGNd, represent the lower visual field (connected with medial LGNd), and the more ventral parts of the TRN contain a map representing the upper visual field (connected with lateral LGNd).

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.

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 degrees 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 degrees) 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.

Mosaic properties of midget and parasol ganglion cells in the marmoset retina.

We measured mosaic properties of midget and parasol ganglion cells in the retina of a New World monkey, the common marmoset Callithrix jacchus . We addressed the functional specialization of these populations for color and spatial vision, by comparing the mosaic of ganglion cells in dichromatic ("red-green color blind") and trichromatic marmosets. Ganglion cells were labelled by photolytic amplification of retrograde marker ("photofilling") following injections into the lateral geniculate nucleus, or by intracellular injection in an in vitro retinal preparation. The dendritic-field size, shape, and overlap of neighboring cells were measured. We show that in marmosets, both midget and parasol cells exhibit a radial bias, so that the long axis of the dendritic field points towards the fovea. The radial bias is similar for parasol cells and midget cells, despite the fact that midget cell dendritic fields are more elongated than are those of parasol cells. The dendritic fields of midget ganglion cells from the same (ON or OFF) response-type array show very little overlap, consistent with the low coverage of the midget mosaic in humans. No large differences in radial bias, or overlap, were seen on comparing retinae from dichromatic and trichromatic animals. These data suggest that radial bias in ganglion cell populations is a consistent feature of the primate retina. Furthermore, they suggest that the mosaic properties of the midget cell population are associated with high spatial resolution rather than being specifically associated with trichromatic color vision.