Opponent Inputs Research Articles

Opponent processing in the retinal mosaic of nymphalid butterflies.

The eyes of nymphalid butterflies, investigated with incident illumination, show colourful facet reflection patterns—the eye shine—which is uniform or heterogeneous, dependent on the species. Facet colours suggest that the ommatidia contain different sets of photoreceptors and screening pigments, but how the colours and the cell characteristics are associated has not been clearly established. Here, we analyse the retinae of two nymphalids, Apatura ilia, which has a uniform eyeshine, and Charaxes jasius, a species with a heterogeneous eye shine, using single-cell recordings, spectroscopy and optical pupillometry. Apatura has UV-, blue- and green-sensitive photoreceptors, allocated into three ommatidial types. The UV- and blue-sensitive cells are long visual fibres (LVFs), receiving opponent input from the green-sensitive short visual fibres (SVFs). Charaxes has an expanded set of photoreceptors, allocated into three additional, red-reflecting ommatidial types. All red ommatidia contain green-sensitive LVFs, receiving opponent input from red receptors. In both species, the SVFs do not receive any opponent input. The simple retina of Apatura with three ommatidial types and two colour-opponent channels can support trichromatic vision. Charaxes has six ommatidial types and three colour-opponent channels. Its expanded receptor set can support tetrachromatic vision.This article is part of the theme issue ‘Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods’.

Task-dependent contrast gain in anomalous trichromats

Anomalous trichromacy is a form of color vision deficiency characterized by the presence of three cone types, but with shifted spectral sensitivities for L or M cones, causing a red-green color deficiency. However, long-term adaptation to this impoverished opponent input may allow for a more normal color experience at the suprathreshold level (“compensation”). Recent experimental evidence points to the presence of compensation in some tasks. The current study used threshold detection, suprathreshold contrast matching, and a reaction-time task to compare contrast coding in normal and anomalous observers along the cardinal cone-opponent axes. Compared to color normals, anomals required more L-M contrast, but not S contrast, to detect stimuli and to match an achromatic reference stimulus. Reaction times were measured for several contrast levels along the two cone-opponent axes. Anomals had higher overall reaction times, but their reaction-time versus contrast functions could be matched to those of controls simply by scaling contrast by the detection thresholds. Anomalous participants were impaired relative to controls for L-M stimuli in all three tasks. However, the contrast losses were three times greater for thresholds and reaction times than for suprathreshold matches. These data provide evidence for compensation in anomalous trichromats, but highlight the role that the experimental task plays in revealing it.

Color perception and compensation in color deficiencies assessed with hue scaling

Anomalous trichromats have three classes of cone receptors but with smaller separation in the spectral sensitivities of their longer-wave (L or M) cones compared to normal trichromats. As a result, the differences in the responses of the longer-wave cones are smaller, resulting in a weaker input to opponent mechanisms that compare the LvsM responses. Despite this, previous studies have found that their color percepts are more similar to normal trichromats than the smaller LvsM differences predict, suggesting that post-receptoral processes might amplify their responses to compensate for the weaker opponent inputs. We evaluated the degree and form of compensation using a hue-scaling task, in which the appearance of different hues is described by the perceived proportions of red-green or blue-yellow primary colors. The scaling functions were modeled to estimate the relative salience of the red-green to blue-yellow components. The red-green amplitudes of the 10 anomalous observers were 1.5 times weaker than for a group of 26 normal controls. However, their relative sensitivity at threshold for detecting LvsM chromatic contrast was on average 6 times higher, consistent with a 4-fold gain in the suprathreshold hue-scaling responses. Within-observer variability in the settings was similar for the two groups, suggesting that the suprathreshold gain did not similarly amplify the noise, at least for the dimension of hue. While the compensation was pronounced it was nevertheless partial, and anomalous observers differed systematically from the controls in the shapes of the hue-scaling functions and the corresponding loci of their color categories. Factor analyses further revealed different patterns of individual differences between the groups. We discuss the implications of these results for understanding both the processes of compensation for a color deficiency and the limits of these processes.

Position Review: Functional Selectivity in Mammalian Olfactory Receptors.

There is increasing appreciation that G-protein-coupled receptors (GPCRs) can initiate diverse cellular responses by activating multiple G proteins, arrestins, and other biochemical effectors. Structurally different ligands targeting the same receptor are thought to stabilize the receptor in multiple distinct active conformations such that specific subsets of signaling effectors are engaged at the exclusion of others, creating a bias toward a particular outcome, which has been referred to as ligand-induced selective signaling, biased agonism, ligand-directed signaling, and functional selectivity, among others. The potential involvement of functional selectivity in mammalian olfactory signal transduction has received little attention, notwithstanding the fact that mammalian olfactory receptors comprise the largest family of mammalian GPCRs. This position review considers the possibility that, although such complexity in G-protein function may have been lost in the specialization of olfactory receptors to serve as sensory receptors, the ability of olfactory receptor neurons (ORNs) to function as signal integrators and growing appreciation that this functionality is widespread in the receptor population suggest otherwise. We pose that functional selectivity driving 2 opponent inputs have the potential to generate an output that reflects the balance of ligand-dependent signaling, the direction of which could be either suppressive or synergistic and, as such, needs to be considered as a mechanistic basis for signal integration in mammalian ORNs.

Odorant-Specific Modes of Signaling in Mammalian Olfaction

Odors play an important role in our quality of life and well being, a role that is compromised by the effect of disease, drugs, aging, and environmental onslaught on the olfactory epithelium (OE). Olfactory receptor neurons (ORNs) in OE provide the primary input to the olfactory system, such that disruption of the cellular processes leading to the activation of the ORNs inevitably compromises olfactory function. The organization of the olfactory periphery in mammals is emerging to be more complex than originally thought. An often underappreciated aspect of that complexity is that odorants have 2 odorant-specific modes of signaling, that is, they inhibit as well as excite the ORNs. The ubiquity of this phenomenon across diverse animal species suggests that having opponent input into the olfactory system is fundamental to how olfaction works, yet in contrast to our canonical understanding of how odorants excite mammalian ORNs, our understanding of how odorants inhibit these cells is still unclear. Odorants potentially can inhibit ORNs through multiple not necessarily mutually exclusive mechanisms but compelling new data argue that phosphoinositide (PI) signaling at least in part mediates inhibitory odorant input to mammalian ORNs. The idea that inhibitory input is mediated through a distinct input pathway argues for the fundamental importance of inhibitory input to olfactory coding in mammals and identifies an additional possible cellular basis for olfactory dysfunction.

OMBO: An opponent modeling approach

In competitive domains, some knowledge about the opponent can give players a clear advantage. This idea led many people to propose approaches that automatically acquire models of opponents, based only on the observation of their input-output behavior. If opponent outputs could be accessed directly, a model can be constructed by feeding a machine learning method with traces of the behavior of the opponent. However, that is not the case in the RoboCup domain where an agent does not have direct access to the opponent inputs and outputs. Rather, the agent sees the opponent behavior from its own point of view and inputs and outputs (actions) have to be inferred from observation. In this paper, we present an approach to model low-level behavior of individual opponent agents. First, we build a classifier to infer and label opponent actions based on observation. Second, our agent observes an opponent and labels its actions using the previous classifier. From these observations, machine learning techniques generate a model that predicts the opponent actions. Finally, the agent uses the model to anticipate opponent actions. In order to test our ideas, we have created an architecture called OMBO (Opponent Modeling Based on Observation). Using OMBO, a striker agent can anticipate goalie actions. Results show that in this striker-goalie scenario, scores are significantly higher using the acquired opponent's model of actions.

Long-wavelength adaptation reveals slow, spectrally opponent inputs to the human luminance pathway

In addition to its expected fast, additive L- and M-cone inputs (L + M), the luminance pathway has slow, spectrally opponent inputs. We have previously shown that on long-wavelength fields, the dominant slow signals change from L-M at moderate intensity levels to M-L signals at high. Here, we focus on the transition between them, which we find is marked by substantial changes in temporal phase delay, and by large and unexpected shifts in flicker spectral sensitivity. At moderate temporal frequencies, counter to the selective adaptation caused by the field, spectral sensitivity changes from being M-cone-like to more L-cone-like. These changes can be accounted for by a change in the relative strengths of the slow spectrally opponent cone signals from L-M exceeding M-L below the transition to M-L exceeding L-M above it, and by the resulting changes in constructive and destructive interference between the dominant signal components. We speculate that the transition is caused by the deep-red field becoming equivalent, postreceptorally, to a green field at high bleaching levels. These results further challenge the dogma that there are separable psychophysical channels for the transmission and processing of color and luminance information. Although its output generates an achromatic percept, the luminance channel has spectrally opponent inputs.

Spectrally opponent inputs to the human luminance pathway: slow +M and −L cone inputs revealed by intense long‐wavelength adaptation

The nature of the inputs to achromatic luminance flicker perception was explored psychophysically by measuring middle- (M-) and long-wavelength-sensitive (L-) cone modulation sensitivities, M- and L-cone phase delays, and spectral sensitivities as a function of temporal frequency. Under intense long-wavelength adaptation, the existence of multiple luminance inputs was revealed by substantial frequency-dependent changes in all three types of measure. Fast (f) and slow (s) M-cone input signals of the same polarity (+sM and +fM) sum at low frequencies, but then destructively interfere near 16 Hz because of the delay between them. In contrast, fast and slow L-cone input signals of opposite polarity (-sL and +fL) cancel at low frequencies, but then constructively interfere near 16 Hz. Although these slow, spectrally opponent luminance inputs (+sM and -sL) would usually be characterized as chromatic, and the fast, non-opponent inputs (+fM and +fL) as achromatic, both contribute to flicker photometric nulls without producing visible colour variation. Although its output produces an achromatic percept, the luminance channel has slow, spectrally opponent inputs in addition to the expected non-opponent ones. Consequently, it is not possible in general to silence this channel with pairs of 'equiluminant' alternating stimuli, since stimuli equated for the non-opponent luminance mechanism (+fM and +fL) may still generate spectrally opponent signals (+sM and +sL).

Spectrally opponent inputs to the human luminance pathway: slow +L and −M cone inputs revealed by low to moderate long‐wavelength adaptation

The luminance pathway has slow (s), spectrally opponent cone inputs in addition to the expected fast (f), non-opponent inputs. The nature of these inputs to luminance flicker perception was further explored psychophysically by measuring middle- (M-) and long-wavelength-sensitive (L-) cone modulation sensitivities, M- and L-cone phase delays, and flicker spectral sensitivities under three conditions of low to moderate long-wavelength adaptation. Under these conditions we find that the luminance channel has fast M- and L-cone input signals (+fM and +fL), and slow, spectrally opponent cone input signals (+sL and -sM). The slow signals found under these conditions are therefore of the opposite polarity to those (+sM and -sL) found under more intense long-wavelength adaptation. At these less intense levels, fast and slow M-cone signals of opposite polarity (-sM and +fM) cancel at low frequencies, but then constructively interfere at intermediate frequencies (ca 12.5-22.5 Hz, depending on adapting level) because of the delay between them. In contrast, fast and slow L-cone signals of the same polarity (+sL and +fL) sum at low frequencies, but then destructively interfere at intermediate frequencies. Importantly, the spectrally opponent signals (+sL and -sM) contribute to flicker nulls without producing visible colour variation. Although its output generates an achromatic percept, the luminance channel has slow spectrally opponent as well as fast non-opponent inputs.

Spectral Sensitivity of Direction‐Selective Ganglion Cells in the Fish Retina

In color matching experiments with extracellular recordings from axon terminals of ganglion cells in the tectum opticum of immobilized goldfish, direction-selective ganglion cells were shown to be color-blind. Their spectral sensitivity is determined by a high positive input from the long wavelength-sensitive cones and weak opponent input from other cone types.

Color opponent retinal ganglion cells in the tammar wallaby retina.

In behavioral tests, tammar wallabies (Macropus eugenii) are dichromats. We investigated the neural basis for this color discrimination by making patch clamp recordings from retinal ganglion cells in an in vitro preparation. Pseudo-random noise stimuli were used to probe the spectral and temporal properties of the receptive fields. Color opponent ganglion cells were excited by medium wavelength-sensitive cones and inhibited by short wavelength-sensitive cones, and were classified as M-on/S-off cells. The S-off response was delayed by 15 ms relative to the M-on response, but, otherwise, the time course of the two responses was very similar. Second-order nonlinear response components, estimated by nonlinear systems analysis, served to accentuate the color opponency. Possible synaptic mechanisms underlying the cone opponent inputs are discussed.

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.

Temporal dynamics of chromatic tuning in macaque primary visual cortex.

The ability to distinguish colour from intensity variations is a difficult computational problem for the visual system because each of the three cone photoreceptor types absorb all wavelengths of light, although their peak sensitivities are at relatively short (S cones), medium (M cones), or long (L cones) wavelengths. The first stage in colour processing is the comparison of the outputs of different cone types by spectrally opponent neurons in the retina and upstream in the lateral geniculate nucleus. Some neurons receive opponent inputs from L and M cones, whereas others receive input from S cones opposed by combined signals from L and M cones. Here we report how the outputs of the L/M- and S-opponent geniculate cell types are combined in time at the next stage of colour processing, in the macaque primary visual cortex (V1). Some V1 neurons respond to a single chromatic region, with either a short (68-95 ms) or a longer (96-135 ms) latency, whereas others respond to two chromatic regions with a difference in latency of 20-30 ms. Across all types, short latency responses are mostly evoked by L/M-opponent inputs whereas longer latency responses are evoked mostly by S-opponent inputs. Furthermore, neurons with late S-cone inputs exhibit dynamic changes in the sharpness of their chromatic tuning over time. We propose that the sparse, S-opponent signal in the lateral geniculate nucleus is amplified in area V1, possibly through recurrent excitatory networks. This results in a delayed, sluggish cortical S-cone signal which is then integrated with L/M-opponent signals to rotate the lateral geniculate nucleus chromatic axes.

Dendritic Computation of Direction Selectivity and Gain Control in Visual Interneurons

The extraction of motion information from time varying retinal images is a fundamental task of visual systems. Accordingly, neurons that selectively respond to visual motion are found in almost all species investigated so far. Despite its general importance, the cellular mechanisms underlying direction selectivity are not yet understood in most systems. Blocking inhibitory input to fly visual interneurons by picrotoxinin (PTX), we demonstrate that their direction selectivity arises largely from interactions between postsynaptic signals elicited by excitatory and inhibitory input elements, which are themselves only weakly tuned to opposite directions of motion. Their joint activation by preferred as well as null direction motion leads to a mixed reversal potential at which the postsynaptic response settles for large field stimuli. Assuming the activation ratio of these opponent inputs to be a function of pattern velocity can explain how the postsynaptic membrane potential saturates with increasing pattern size at different levels for different pattern velocities ("gain control"). Accordingly, we find that after blocking the inhibitory input by PTX, gain control is abolished.

Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights.

1. We measured the response of macaque ganglion cells to sinusoidally modulated red and green lights as the relative phase, theta, of the lights was varied. 2. At low frequencies, red-green ganglion cells of the parvocellular (PC-) pathway with opponent inputs from middle-wavelength sensitive (M-) and long-wavelength sensitive (L-) cones were minimally sensitive to luminance modulation (theta = 0 deg) and maximally sensitive to chromatic modulation (theta = 180 deg). With increasing frequency, the phase, theta, of minimal amplitude gradually changed, in opposite directions for cells with M- and L-cone centres. 3. At high frequencies (at and above 20 Hz), phasic cells of the magnocellular (MC-) pathway were maximally responsive when theta approximately 0 deg and minimally responsive when theta approximately 180 deg, as expected from an achromatic mechanism. At lower frequencies, the phase of minimal response shifted, for both on- and off-centre cells, to values of theta intermediate between 0 and 180 deg. This phase asymmetry was absent if the centre alone was stimulated with a small field. 4. For PC-pathway cells, it was possible to provide an account of response phase as a function of theta, using a model involving three parameters; phases of the L- and M-cone mechanisms and a L/M cone weighting term. For red-green cells, the phase parameters were monotonically related to temporal frequency and revealed a centre-surround phase difference. The phase difference was linear with a slope of 1-3 deg Hz-1. If this represents a latency difference, it would be 3-8 ms. Otherwise, temporal properties of the M- and L-cones appeared similar if not identical. By addition of a scaling term, the model could be extended to give an adequate account of the amplitude of responses. 5. We were able to activate selectively the surrounds of cells with short-wavelength (S-) cone input to their centres, and so were able to assess L/M cone weighting to the surround. M- and L-cone inputs added linearly for most cells. On average, the weighting corresponded to the Judd modification of the luminosity function although there was considerable inter-cell variability. 6. To account for results from MC-pathway cells, it was necessary to postulate a cone-opponent, chromatic input to their surrounds. We developed a receptive field model with linear summation of M- and L-cones to centre and surround, and with an additional M,L-cone opponent input to the surround.(ABSTRACT TRUNCATED AT 400 WORDS)

The effect of adaptation on the differential sensitivity of the S-cone color system

This paper presents a psychophysical dissection of the S-cone color system. Experiments were guided by a skeletal model that assumed a first stage consisting of S-, M- and L-cones, and a second stage of the opponent combination of the 5 and L + M signals. The response of the S-cone system was isolated by measuring difference thresholds between lights that were equiluminant tritanopic confusion pairs and thus differed only in S-cone excitation. Two types of mechanisms that control sensitivity in the S-cone system were identified: (i) static mechanisms that have a restricted range and thus limit discrimination to a small range of inputs; and (ii) adaptive mechanisms that change the state of the system in response to changes in steady illumination, so that the system is sensitive to small changes from the adapting light. These mechanisms were localized by lights that stimulated the S-cone system while keeping the signal constant at either the S, the L + M, or the post-opponent stage. The response function of the static mechanism was estimated by measuring difference thresholds at judgment points other than the steady adapting light. This procedure was repeated at a number of adaptation lights to examine the properties of adaptive mechanisms. The data were consistent with an elaborated model that included identical multiplicative gain control mechanisms in the S and L + M pre-opponent branches, and a post-opponent static sigmoidal nonlinearity with different amounts of compression for positive and negative opponent inputs.

Responses of primate retinal ganglion cells to moving spectral contrast

A moving border formed by color contrast across which brightness contrast can be independently controlled was used to examine responses of ganglion cells in monkey retina. We used two forms of color contrasts, white/yellow and red/green. Three classes of ganglion cells were examined: blue/yellow opponent, red/green opponent and non-color opponent on-center phasic cells. Blue/yellow opponent cells respond strongly to white/yellow contrast at all brightness gradients, responding better to a white/yellow border at minimum brightness contrast than to a white/black border at maximum brightness contrast. These cells respond before and reach their maximum response long after the border has crossed the receptive field center. Red/green opponent and phasic non-opponent cells do not detect white/yellow borders at minimum brightness contrast; at sufficient brightness contrast phasic and some red/green opponent cells detect this border responding maximally as the border crosses their receptive field center. Red/green opponent and non-opponent phasic on-center cells respond to red/green contrast at both maximum and minimum brightness contrast. The former are excited by only one side, the latter by either side of the red/green contrast entering their receptive field. Phasic on-center cells have a maintained excitatory rod signal which is suppressed when a detectable border enters their field. The results suggest that the blue/yellow opponent system plays a major role in distinguishing white/yellow borders and has a poorer spatial resolution than the red/green one, that phasic ganglion cells receive a rod and a red/green but not a blue/yellow opponent input, and that this blue/yellow system has a retinal pathway which does not obviously influence rods or other cones.

Excerpts from a letter by C. Tsokos to D. Perkel

Anomalous trichromats have three classes of cone receptors but with smaller separation in the spectral sensitivities of their longer-wave (L or M) cones compared to normal trichromats. As a result, the differences in the responses of the longer-wave cones are smaller, resulting in a weaker input to opponent mechanisms that compare the LvsM responses. Despite this, previous studies have found that their color percepts are more similar to normal trichromats than the smaller LvsM differences predict, suggesting that post-receptoral processes might amplify their responses to compensate for the weaker opponent inputs. We evaluated the degree and form of compensation using a hue-scaling task, in which the appearance of different hues is described by the perceived proportions of red-green or blue-yellow primary colors. The scaling functions were modeled to estimate the relative salience of the red-green to blue-yellow components. The red-green amplitudes of the 10 anomalous observers were 1.5 times weaker than for a group of 26 normal controls. However, their relative sensitivity at threshold for detecting LvsM chromatic contrast was on average 6 times higher, consistent with a 4-fold gain in the suprathreshold hue-scaling responses. Within-observer variability in the settings was similar for the two groups, suggesting that the suprathreshold gain did not similarly amplify the noise, at least for the dimension of hue. While the compensation was pronounced it was nevertheless partial, and anomalous observers differed systematically from the controls in the shapes of the hue-scaling functions and the corresponding loci of their color categories. Factor analyses further revealed different patterns of individual differences between the groups. We discuss the implications of these results for understanding both the processes of compensation for a color deficiency and the limits of these processes.