Color-opponent Cells Research Articles

Vision: Space and colour meet in the fly optic lobes

Colour vision involves colour-opponent cells, which are excited and inhibited by different wavelengths. Synaptic interconnections between Drosophila Dm8 cells are required for forming spatio-chromatic receptive fields with a center and surround of opposing polarity which can invert, depending on the stimulus.

Short Wavelengths Contribution to Light-induced Responses and Irradiance Coding in the Rat Dorsal Lateral Geniculate Nucleus – An In vivo Electrophysiological Approach

The dorsal lateral geniculate nucleus (dLGN) is the main neuronal station en route to higher visual areas. It receives information about environmental light from retinal photoreceptors whose sensitivity peaks are distributed across a visible spectrum. Here, using electrophysiological multichannel recordings in vivo combined with different light stimulations, we investigated short wavelength contribution to the dLGN responses to light and irradiance coding. The results showed that the majority of dLGN cells responded evenly to almost all wavelengths from the 340 to 490 nm spectrum; however, some cells representing extremes of unimodal distribution of Blue-UV index were specialised in the reception of blue or UV light. Moreover, by using alternate yellow and monochromatic light stimuli from blue - UV range, we also assessed the relative spectral contribution to rat dLGN responses to light. Finally, we observed no clear changes in the irradiance coding property of short wavelength-deficient light stimuli, however we noticed a distortion of the coding curves manifested by a significant drop in measure of fit after using short wavelength blocking filter. In conclusion, our data provide the first electrophysiological report on dLGN short wavelength-induced responses under changing light conditions and suggest the presence of colour opponent cells in the rat dLGN.

A new transformation of cone responses to opponent color responses

It is widely agreed that the color vision process moves quickly from cone receptors to opponent color cells in the retina and lateral geniculate nucleus. Many workers have proposed the transformation or coding of long, medium, short (LMS) cone responses to r − g, y − b opponent color chromatic responses (unique hues) on the following basis: That L, M, S cones represent Red, Green, and Blue hues, with Yellow represented by (L + M), while r − g and y − b represent the opponent pairs of unique hues. The traditional coding from cones to opponent colors is that L − M gives r − g, while (L + M) − S gives y − b. This convention is open to several criticisms, and a new coding is required. A literature search produced 16 studies of cone responses LMS and 15 studies of spectral (i.e., ygb) opponent color chromatic responses, in terms of response wavelength peaks. Comparative analysis of the two sets of studies shows the means are almost identical (within 3 nm; i.e., L = y, M = g, S = b). Further, the response curves of LMS are very similar shapes to ygb. In sum, each set can directly transform to the other on this proposed coding: (S + L) − M gives r − g, while L − S gives y − b. This coding activates neural operations in the cardinal directions r − g and y − b.

Neural circuits in the mouse retina support color vision in the upper visual field

Color vision is essential for an animal’s survival. It starts in the retina, where signals from different photoreceptor types are locally compared by neural circuits. Mice, like most mammals, are dichromatic with two cone types. They can discriminate colors only in their upper visual field. In the corresponding ventral retina, however, most cones display the same spectral preference, thereby presumably impairing spectral comparisons. In this study, we systematically investigated the retinal circuits underlying mouse color vision by recording light responses from cones, bipolar and ganglion cells. Surprisingly, most color-opponent cells are located in the ventral retina, with rod photoreceptors likely being involved. Here, the complexity of chromatic processing increases from cones towards the retinal output, where non-linear center-surround interactions create specific color-opponent output channels to the brain. This suggests that neural circuits in the mouse retina are tuned to extract color from the upper visual field, aiding robust detection of predators and ensuring the animal’s survival.

Receptive Field Properties of Color Opponent Neurons in the Cat Lateral Geniculate Nucleus

Most nonprimate mammals possess dichromatic ("red-green color blind") color vision based on short-wavelength-sensitive (S) and medium/long-wavelength-sensitive (ML) cone photoreceptor classes. However, the neural pathways carrying signals underlying the primitive "blue-yellow" axis of color vision in nonprimate mammals are largely unexplored. Here, we have characterized a population of color opponent (blue-ON) cells in recordings from the dorsal lateral geniculate nucleus of anesthetized cats. We found five points of similarity to previous descriptions of primate blue-ON cells. First, cat blue-ON cells receive ON-type excitation from S-cones, and OFF-type excitation from ML-cones. We found no blue-OFF cells. Second, the S- and ML-cone-driven receptive field regions of cat blue-ON cells are closely matched in size, consistent with specialization for detecting color contrast. Third, the receptive field center diameter of cat blue-ON cells is approximately three times larger than the center diameter of non-color opponent receptive fields at any eccentricity. Fourth, S- and ML-cones contribute weak surround inhibition to cat blue-ON cells. These data show that blue-ON receptive fields in cats are functionally very similar to blue-ON type receptive fields previously described in macaque and marmoset monkeys. Finally, cat blue-ON cells are found in the same layers as W-cells, which are thought to be homologous to the primate koniocellular system. Based on these data, we suggest that cat blue-ON cells are part of a "blue-yellow" color opponent system that is the evolutionary homolog of the blue-ON division of the koniocellular pathway in primates.

Visual signal processing in the macaque lateral geniculate nucleus

Comparisons of S- or prepotential activity, thought to derive from a retinal ganglion cell afferent, with the activity of relay cells of the lateral geniculate nucleus (LGN) have sometimes implied a loss, or leak, of visual information. The idea of the "leaky" relay cell is reconsidered in the present analysis of prepotential firing and LGN responses of color-opponent cells of the macaque LGN to stimuli varying in size, relative luminance, and spectral distribution. Above a threshold prepotential spike frequency, called the signal transfer threshold (STT), there is a range of more than 2 log units of test field luminance that has a 1:1 relationship between prepotential- and LGN-cell firing rates. Consequently, above this threshold, the LGN cell response can be viewed as an extension of prepotential firing (a "nonleaky relay cell"). The STT level decreased when the size of the stimulus increased beyond the classical receptive field center, indicating that the LGN cell is influenced by factors other than the prepotential input. For opponent ON cells, both the excitatory and the inhibitory response decreased similarly when the test field size increased beyond the center of the receptive field. These findings have consequences for the modeling of LGN cell responses and transmission of visual information, particularly for small fields. For instance, for LGN ON cells, information in the prepotential intensity-response curve for firing rates below the STT is left to be discriminated by OFF cells. Consequently, for a given light adaptation, the STT improves the separation of the response range of retinal ganglion cells into "complementary" ON and OFF pathways.

Physiology and Morphology of Color-Opponent Ganglion Cells in a Retina Expressing a Dual Gradient of S and M Opsins

Most mammals are dichromats, having short-wavelength-sensitive (S) and middle-wavelength-sensitive (M) cones. Smaller terrestrial species commonly express a dual gradient in opsins, with M opsin concentrated superiorly and declining inferiorly, and vice-versa for S opsin. Some ganglion cells in these retinas combine S- and M-cone inputs antagonistically, but no direct evidence links this physiological opponency with morphology; nor is it known whether opponency varies with the opsin gradients. By recording from >3000 ganglion cells in guinea pig, we identified small numbers of color-opponent cells. Chromatic properties were characterized by responses to monochromatic spots and/or spots produced by mixtures of two primary lights. Superior retina contained cells with strong S+/M- and M+/S- opponency, whereas inferior retina contained cells with weak opponency. In superior retina, the opponent cells had well-balanced M and S weights, while in inferior retina the weights were unbalanced, with the M weights being much weaker. The M and S components of opponent cell receptive fields had approximately the same diameter. Opponent cells injected with Lucifer yellow restricted their dendrites to the ON stratum of the inner plexiform layer and provided sufficient membrane area (approximately 2.1 x 10(4) microm(2)) to collect approximately 3.9 x 10(3) bipolar synapses. Two bistratified cells studied were nonopponent. The apparent decline in S/M opponency from superior to inferior retina is consistent with the dual gradient and a model where photoreceptor signals in both superior and inferior retina are processed by the same postreceptoral circuitry.

Color properties of movement detectors in the Carassius gibelio (Bloch, 1782) tectum opticum studied by selective stimulation of different cone types

and takes part in orienting responses revealed in rapid eye, head, and/or body movemements. This function can proceed without taking into account information about color, and the superior colliculus in mammals is color-blind (Michael, 1973). In the frog, the system carrying chromatic information also originates as a channel separate from the tectal pathway, providing the main information needed for the frog’s reactions to moving objects (Maximov et al., 1985). Color blindness of movement detectors projecting to the fish tectum was proved in color-matching experiments for both orientation-selective (Maximova, 1999) and direction-selective (Maximova et al., 2005) units. Recent experiments using selective stimulation of different cone types revealed new features of these projections. The color vision of Prussian carp (Carassius gibelio Bloch, 1782) adults is determined by three types of cones: long-wavelength (L), middle-wavelength (M), and short-wavelength (�), con taining three A2-based visual pigments that absorb maximally at about 622, 545, and 434 nm, respectively (Maximova et al., 2005). Color opponent cells were presented at different levels of the fish visual system, and single-unit extracellular recordings from the C. gibelio tectum opticum were made in order to examine the possible role of action potential timing in coding chromatic stimuli.

On the Coding of Negative Quantities in Cortical Circuits

AbstractMullers Law of specific nerve energies introduced the idea that nerves transmit information about specific sensory features. This concept has been refined by the notion of 'labeled lines,' specific cells that capture sub-features of a sensory or motor stimulus, such as Hubel and Weisel's opponent color cells. Such features can be visualized as coding a signed quantity that has positive and negative components that are encoded with separate nerve cells. We show that there are two important consequences when learning receptive field using signed codings in circuits. The first is that in feedback circuits even simple operations need to be distributed across multiple distinct pathways. The second consequence is that such pathways are necessarily dynamic. Synaptic weights change during learning and must break and grow new circuit connections because the weights need to change sign during receptive field formation.

Passion for pathology: beauty is in the eye of the beholder

Dear Editor, We read with great interest the editorial by G. Bussolati on the mental processes that lead to pathological diagnoses [2], which is the first published approach to this process. We would like to stress/add a few points that we think are of great importance. Besides the perception of form, color is important for detecting objects and patterns that would otherwise not be noticed. We all know from experience that black and white microscopic figures loose much of their information content. A haematoxylin–eosin-stained glass slide makes us look twice if it is over-stained with haematoxylin, since we have unconsciously associated “bluish” with hypercellular/suspicious lesions. Color opponency, simultaneous color contrast and color constancy are the key features of color vision. Color is coded in the retina and in the lateral geniculate nucleus by color-opponent cells and processed in the cortex by concentric double-opponent cells in the blob zones (area V1 of the cortex) [3].

Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L.

The honeybee, Apis mellifera L., is one of the living creatures that has its colour vision proven through behavioural tests. Previous studies of honeybee colour vision has emphasized the relationship between the spectral sensitivities of photoreceptors and colour discrimination behaviour. The current understanding of the neural mechanisms of bee colour vision is, however, rather limited. The present study surveyed the patterns of chromatic information processing of visual neurons in the lobula of the honeybee, using intracellular recording stimulated by three light-emitting diodes, whose emission spectra approximately match the spectral sensitivity peaks of the honeybee. The recorded visual neurons can be divided into two groups: non-colour opponent cells and colour opponent cells. The non-colour opponent cells comprise six types of broad-band neurons and four response types of narrow-band neurons. The former might detect brightness of the environment or function as chromatic input channels, and the latter might supply specific chromatic input. Amongst the colour opponent cells, the principal neural mechanism of colour vision, eight response types were recorded. The receptive fields of these neurons were not centre surround as observed in primates. Some recorded neurons with tonic post-stimulus responses were observed, however, suggesting temporal defined spectral opponency may be part of the colour-coding mechanisms.

Homogeneity and diversity of color-opponent horizontal cells in the turtle retina: Consequences for potential wavelength discrimination.

Color information processing in fish and turtles starts with the transformation of the tetra-chromatic cone system into two types of color-opponent horizontal cells (C-type). Few studies reported on large variability between C-type horizontal cells of the same class, suggesting it might improve color vision. However, such variability is contradictory with the tight coupling between horizontal cells that tends to average intercellular differences. We addressed this apparent discrepancy, and studied the spectral properties of C-type horizontal cells in the turtle retina. Photoresponses were recorded in the eyecup preparation, using light stimuli of different wavelengths and intensities. The spectral properties of each cell were defined by the neutral points (wavelengths at which response polarity reversed), which were derived from sensitivity data and from large-amplitude photoresponses. For each C-type horizontal cell, a linear relationship between log stimulus intensity needed for polarity reversal and wavelength was found. With this definition, homologous C-type horizontal cells from the same retina were practically identical in their spectral properties, indicating that the averaging effects of the horizontal cell syncytium eliminated any intercellular variability. In contrast, C-type horizontal cells of the same class exhibited large inter-retina variability. We tested the potential for wavelength discrimination by applying the line element theory to the action spectra of the two chromatic (Red/Green & Yellow/Blue) horizontal cell channels, and found good agreement with behavioral data from a similar species of turtles.

Color-opponent responses of small and giant bipolar cells in the carp retina.

The physiological and morphological properties of color-opponent bipolar cells in the carp retina were studied. Fifty nine OFF-center bipolar cells and 63 ON-center bipolar cells out of about 500 total bipolar cells recorded showed color-opponent responses. The OFF-center color-opponent bipolar cells were classified into three subgroups according to their spectral and spatial responses. Fifty OFF-center color-opponent cells responded with depolarization to a blue light spot and with hyperpolarization to a red spot in the receptive-field center. The polarity of the surround response was opposite to that of center response at each wavelength. Therefore these cells were classified as OFF double-opponent cells (OFF-DO). Eight cells responded with hyperpolarization to a blue and green spot and with depolarization to a red spot. The surround responses of those cells were depolarizing at any wavelength (R+G- cell). One responded with hyperpolarization to a blue and red spot and with depolarization to a green spot. The surround response showed a different spectral characteristic from that of the center response. It responded with depolarization to a blue and green annulus and with hyperpolarization to a red annulus (R-G+B- cell). The ON-center color-opponent bipolar cells were similarly classified into three subgroups. Sixty of ON-center color-opponent cells were the double color-opponent type (ON-DO cell), showing the responses of opposite polarity to the OFF-DO cells. Two cells were classified as R- G+ cell, and one cell as R+G-B+ cell. Both OFF- and ON-DO cells were identified by their morphology as Cajal's giant bipolar cells, and R+G-, R-G+, R-G+B-, and R+G-B+ cells as Cajal's small bipolar cells. The analysis of the latency and the ionic mechanisms of their responses suggest that DO cells under light-adapted conditions receive direct inputs from long-wavelength (red) cones, RG cells from middle-wavelength (green) cones, and RGB cells from short-wavelength (blue) cones. Possible mechanisms of the opponent inputs to these bipolar cells are discussed.

Evidence that blue-on cells are part of the third geniculocortical pathway in primates.

Colour vision in primates is mediated by cone opponent ganglion cells in the retina, whose axons project to the dorsal lateral geniculate nucleus in the visual thalamus. It has long been assumed that cone opponent ganglion cells project to the parvocellular layers of the geniculate. Here, we examine the role of a third subdivision of the geniculocortical pathway: the interlaminar or koniocellular geniculate relay cells. We made extracellular recordings in the dorsal lateral geniculate nucleus of the common marmoset Callithrix jacchus, a New World monkey in which the interlaminar cells are well segregated from the parvocellular layers. We found that one group of colour opponent cells, the blue-on cells, was largely segregated to the interlaminar zone. This segregation was common to dichromatic ('red-green colour-blind') and trichromatic marmosets. The result calls into question the traditional notion that all colour information passes through the parvocellular division of the retino-geniculo-cortical pathway in primates.

A Dissociation Between Brain Activity and Perception: Chromatically Opponent Cortical Neurons Signal Chromatic Flicker that is not Perceived

When two isoluminant colors alternate at frequencies > 10 Hz, we perceive only one fused color with a minimal sensation of brightness flicker. In spite of the perception of color fusion, color opponent (CO) cells at early stages of the visual pathway are known to respond to chromatic flicker at frequencies far exceeding the perceptual fusion frequency. To explain color fusion, several groups have predicted that CO cells in V1-unlike the retina and lateral geniculate nucleus-should not follow high-frequency flicker. To test this prediction we recorded from 12 CO cells in various V1 layers. We found, contrary to expectations, that these neurons follow high frequency flicker well above heterochromatic fusion frequencies. All followed 15 Hz flicker and 10/12 followed 30 Hz flicker. For three cells, we tested 60 Hz luminance flicker and found clear responses. We thus present evidence of cortical activity in alert, trained monkeys that is clearly representing visual stimulation, yet is not perceived. Our data call into question explanations of perceptual phenomena that invoke a low temporal frequency cut-off of CO cells in V1 to account for the failure to perceive fast temporal changes in the chromatic domain.

Dynamics in Parvocellular and Magnocellular Pathways: Consequences for Luminance and Colour Processing Streams

An achromatic neuromorphic model of the vertebrate retina has already accounted for X and Y pathways (Beaudot and Hérault, 1994 Perception23 Supplement, 25) and has shown a temporal ‘coarse-to-fine’ processing of spatial information (Beaudot et al, 1995 Perception24 Supplement, 93). This model has been extended to colour vision. By taking into account the chromatic sensitivities of cones, functional properties of the parvocellular pathway are modelled. Approximating the responses of colour-opponent cells, the model provides a spatial multiplexing of luminance and chrominance information: sustained responses show spatial band-pass behaviour to luminance variations and low-pass behaviour to equiluminant colour changes. In addition the spatiotemporal inseparability for luminance in the parvocellular model leads to a temporal multiplexing of spatial luminance information: at higher temporal frequencies the spatial filtering is low-pass, conveying only luminance information. Demultiplexing this mixed information suggests interactions between retinal channels. By locally combining additive and subtractive mechanisms between opposite parvocellular pathways (eg G+/ R−± R+/ G−), and an inhibition from the magnocellular pathway, the existence of at least three functional subchannels is predicted: (i) a transient, spatially low-pass channel, (ii) a sustained, spatially band-pass channel, dedicated to the analysis of luminance information in a spatiotemporally separable way (eg moving shadows and static textures), and (iii) a spatiotemporally low-pass, colour-opponent channel leading to colour induction, which is little affected by the presence of shadows and is more representative of objects. This hypothesis of spatiotemporal demultiplexing of luminance and chrominance information, which should presumably occur at an early cortical level, is in accordance with the multiple-processing-streams organisation of the primate visual system.

Acquisition of color opponent representation by a three-layered neural network model.

This paper discusses color representation in the visual system by analysis of a three-layered neural network model. The model incorporates physiological knowledge of color representation at the sensor level (broad-band trichromatic representation by cones) and the higher level (narrow-band color representation by color-coded cells in V4). We trained the model to perform a mapping between these color representations by the back propagation algorithm and analyzed the acquired characteristics of the hidden units. It turned out that the hidden units learned characteristics similar to those of the color opponent cells found in the visual system. It was concluded that the R-G and Y-B color opponent representations reflect the efficiency of the color representation in the visual system from investigations on the efficiency of color representation in the hidden layer and on the capability of the color recognition task of the model.

Isoluminant stimuli may not expose the full contribution of color to visual functioning: Spatial contrast sensitivity measurements indicate interaction between color and luminance processing

Visual performance is greatly impaired when tested with heterochromatic isoluminant stimuli. It is thus concluded that the chromatic system contribution to many visual tasks is limited. We suggest that unless color and luminance are shown to be processed independently, such experiments do not demonstrate shortcomings of the chromatic system but rather the inadequacy of using isoluminant stimuli for isolating that system. We hypothesize that color vision has evolved not only to encode color per se but also to enhance luminance-based visual processing, so that for color information to be fully effective, luminance as well as chromatic variations should be present in the stimulus. The hypothesis was tested by studying the contribution of color to spatial vision. The human contrast sensitivity function (CSF) was studied using luminance, isoluminance (color) and combined luminance/color sinusoidal gratings. It is found that luminance contrast sensitivity is enhanced when luminance contrast is accompanied by color contrast and vice versa. The nature of the interaction is best described by an additive single analyzer model. Color opponent cells which respond to both chromatic and achromatic stimuli may be identified as the analyzer.

Effects of excitatory amino acids and their antagonists on the light response of luminosity and color-opponent horizontal cells in the turtle (Pseudemys scripta elegans) retina

Both kainic acid (KA) and N-methyl-d-aspartatic acid (NMDA) depolarize luminosity-type horizontal cells (L-type H cells) in normal turtle retina. The presence of both NMDA and non-NMDA receptors for excitatory amino acids (EAAs) on these cells was highlighted by an unusual effect of the noncompetitive NMDA-antagonist, MK-801. In retinas that had been exposed to MK-801, the action of NMDA was irreversibly altered to one of hyperpolarization, while the depolarizing effect of KA was unaltered. The aim of the present study was to further characterize these receptors on L-type H cells and to extend the investigation to color-opponent H cells (C-type H cells). Intracellular recording was used to study the effects of KA, NMDA, MK-801, the competitive NMDA antagonists, 2-amino-5-phosphonopentanoic acid (AP5) and 2-amino-7-phosphonoheptanoic acid (AP7), and the nonspecific EAA antagonist, kynurenic acid (KYN) on the light responses of L-type and C-type H cells in turtle retina. The effects of combinations of these drugs were also studied. In L-type H cells the agonists caused depolarization and loss of light response, KYN caused hyperpolarization and loss of light response, and MK-801, AP5 or AP7 had no direct effect. However, application of NMDA following MK-801, AP5 or AP7, but not KYN, caused hyperpolarization and loss of light response. The depolarizing effect of KA was unaltered by these antagonists. These data confirm the presence of an unusual NMDA receptor on L-type H cells. In the case of red/green C-type H cells, application of KA caused loss of responses to both red and green light, with loss of green responses preceding loss of red responses. NMDA initially removed responses to both red and green light. The most striking effect of NMDA was seen during early washout where the responses to red were reversed (hyperpolarizing). These responses eventually recovered their normal polarity. These results suggest that the depolarizing response of C-type H cells to red light is mediated by L-type H cells, but not via inhibition of the excitatory input from green cones to C-type H cells.

Parallel pathways in the visual system: Their role in perception at isoluminance

It has been proposed that the functions of the two major parallel channels of the primate visual system, the color-opponent and the broad-band, can be determined in psychophysical experiments by eliminating luminance but maintaining chrominance information (isoluminance), since under such conditions the broad-band channel is believed to be silenced. To test this proposition we examined the visual functions of monkeys after blocking either of these channels and we also assessed the responses of neurons to isoluminant stimuli in the lateral geniculate nucleus. We show that color, texture, stereopsis and pattern perception in the absence of the color-opponent channel, and flicker and motion perception in the absence of the broad-band channel are compromised. Yet isoluminance functions for stereopsis and texture in the absence of the broad-band channel and for motion in the absence of the color-opponent channel are indistinguishable from normal. Our recordings show that the neuronal responses of the broad-band cells for isoluminant exchange of red and green lights are reduced but not eliminated and that the color-opponent cells also become similarly less responsive under these conditions. We conclude that perceptual losses at isoluminance are not specific for either channel.