Detection and discrimination of achromatic contrast: A ganglion cell perspective.

The magnocellular (MC) pathway in the primate has much higher achromatic contrast sensitivity than the parvocellular (PC) pathway, and is implicated in luminance contrast detection. But MC pathway responses tend to saturate at lower achromatic contrast than do PC pathway responses. It has been proposed that the PC pathway plays a major role in discriminating suprathreshold achromatic contrast, because the MC pathway is in saturation. This has been termed the pulsed-pedestal protocol. To test this hypothesis, responses of MC and PC pathway ganglion cells have been examined under suprathreshold conditions with stimulus configurations similar to those in psychophysical tests. For MC cells, response saturation was much less for flashed or moving edges than for sinusoidal modulation, and MC cell thresholds predicted for these stimuli were similar to psychophysical discrimination (and detection) data. Results suggest the protocol is not effective in segregating MC and PC function.

A quantitative description of macaque ganglion cell responses to natural scenes: the interplay of time and space.

KEY POINTS: Responses to natural scenes are the business of the retina. We find primate ganglion cell responses to such scenes consistent with those to simpler stimuli. A biophysical model confirmed this and predicted ganglion cell responses with close to retinal reliability. Primate ganglion cell responses to natural scenes were driven by temporal variations in colour and luminance over the receptive field centre caused by eye movements, and little influenced by interaction of centre and surround with structure in the scene. We discuss implications in the context of efficient coding of the visual environment. Much information in a higher spatiotemporal frequency band is concentrated in the magnocellular pathway. ABSTRACT: Responses of visual neurons to natural scenes provide a link between classical descriptions of receptive field structure and visual perception of the natural environment. A natural scene video with a movement pattern resembling that of primate eye movements was used to evoke responses from macaque ganglion cells. Cell responses were well described through known properties of cell receptive fields. Different analyses converge to show that responses primarily derive from the temporal pattern of stimulation derived from eye movements, rather than spatial receptive field structure beyond centre size and position. This was confirmed using a model that predicted ganglion cell responses close to retinal reliability, with only a small contribution of the surround relative to the centre. We also found that the spatiotemporal spectrum of the stimulus is modified in ganglion cell responses, and this can reduce redundancy in the retinal signal. This is more pronounced in the magnocellular pathway, which is much better suited to transmit the detailed structure of natural scenes than the parvocellular pathway. Whitening is less important for chromatic channels. Taken together, this shows how a complex interplay across space, time and spectral content sculpts ganglion cell responses.

Macaque retinal ganglion cell responses to visual patterns: harmonic composition, noise, and psychophysical detectability.

The goal of these experiments was to test how well cell responses to visual patterns can be predicted from the sinewave tuning curve. Magnocellular (MC) and parvocellular (PC) ganglion cell responses to different spatial waveforms (sinewave, squarewave, and ramp waveforms) were measured across a range of spatial frequencies. Sinewave spatial tuning curves were fit with standard Gaussian models. From these fits, waveforms and spatial tuning of a cell's responses to the other waveforms were predicted for different harmonics by scaling in amplitude for the power in the waveform's Fourier expansion series over spatial frequency. Since higher spatial harmonics move at a higher temporal frequency, an additional scaling for each harmonic by the MC (bandpass) or PC (lowpass) temporal response was included, together with response phase. Finally, the model included a rectifying nonlinearity. This provided a largely satisfactory estimation of MC and PC cell responses to complex waveforms. As a consequence of their transient responses, MC responses to complex waveforms were found to have significantly more energy in higher spatial harmonic components than PC responses. Response variance (noise) was also quantified as a function of harmonic component. Noise increased to some degree for the higher harmonics. The data are relevant for psychophysical detection or discrimination of visual patterns, and we discuss the results in this context.

Mixing of Chromatic and Luminance Retinal Signals in Primate Area V1.

Vision emerges from activation of chromatic and achromatic retinal channels whose interaction in visual cortex is still poorly understood. To investigate this interaction, we recorded neuronal activity from retinal ganglion cells and V1 cortical cells in macaques and measured their visual responses to grating stimuli that had either luminance contrast (luminance grating), chromatic contrast (chromatic grating), or a combination of the two (compound grating). As with parvocellular or koniocellular retinal ganglion cells, some V1 cells responded mostly to the chromatic contrast of the compound grating. As with magnocellular retinal ganglion cells, other V1 cells responded mostly to the luminance contrast and generated a frequency-doubled response to equiluminant chromatic gratings. Unlike magnocellular and parvocellular retinal ganglion cells, V1 cells formed a unimodal distribution for luminance/color preference with a 2- to 4-fold bias toward luminance. V1 cells associated with positive local field potentials in deep layers showed the strongest combined responses to color and luminance and, as a population, V1 cells encoded a diverse combination of luminance/color edges that matched edge distributions of natural scenes. Taken together, these results suggest that the primary visual cortex combines magnocellular and parvocellular retinal inputs to increase cortical receptive field diversity and to optimize visual processing of our natural environment.

Dependence of chromatic responses in V1 on visual field eccentricity and spatial frequency: an fMRI study.

Psychophysical sensitivity to red-green chromatic modulation decreases with visual eccentricity, compared to sensitivity to luminance modulation, even after appropriate stimulus scaling. This is likely to occur at a central, rather than a retinal, site. Blood-oxygenation-level-dependent (BOLD) functional magnetic resonance imaging (fMRI) responses to stimuli designed to separately stimulate different afferent channels' [red-green, luminance, and short-wavelength (S)-cone] circular gratings were recorded as a function of visual eccentricity (±10 deg) and spatial frequency (SF) in human primary visual cortex (V1) and further visual areas (V2v, V3v). In V1, the SF tuning of BOLD fMRI responses became coarser with eccentricity. For red-green and luminance gratings, similar SF tuning curves were found at all eccentricities. The pattern for S-cone modulation differed, with SF tuning changing more slowly with eccentricity than for the other two modalities. This may be due to the different retinal distribution with eccentricity of this receptor type. A similar pattern held in V2v and V3v. This would suggest that transformation or spatial filtering of the chromatic (red-green) signal occurs beyond these areas.

Color vision: introduction by the feature editors.

This feature issue of the Journal of the Optical Society of America A (JOSA A) reflects the basic and applied research interests of members of the color vision community. Most of the articles stem from presentations at the 23rd Biennial Symposium of the International Colour Vision Society (ICVS).

Eye movements and the neural basis of context effects on visual sensitivity.

The effects of context on visual sensitivity are well established (e.g., sensitivity to luminance flicker is substantially higher on mean-gray surrounds than on white or black surrounds). The neural mechanisms generating context effects, however, remain unresolved. In the absence of direct tests, some theories invoke enhancement of edges by lateral inhibition, whereas others rely on transients caused by miniature eye movements that maintain fixation. We first replicated the luminance results on human observers and found unexpectedly that sensitivity to red-green flicker is also affected by surround color, being substantially higher on mean-gray surrounds than on red or green surrounds. To identify the neural bases of both context effects, we used in vivo electrophysiological recordings of primate magnocellular and parvocellular ganglion cell responses to luminance and red-green modulations, respectively. To test neuronal sensitivity to stationary edge contrast, neuronal responses were measured at various distances from the modulation edge against various surrounds. We found no evidence of enhanced responses to stationary edges on any surrounds, ruling out lateral inhibition-type explanations. To simulate the effects of eye movements, target patches were abruptly displaced while measuring responses. Abruptly displaced edges evoked vigorous transient responses that were selective for modulation-phase on mean-gray surrounds, but were phase-invariant on other surrounds. Eye movements could thus enhance detection of flicker on mean-gray surrounds, and neurometric analyses supported a primary role for eye movements in enhancing sensitivity. In addition, the transformation of spatial edges to transient neuronal responses by eye movements provides the signals for detecting luminance and color edges in natural scenes.

Distribution and specificity of S-cone ("blue cone") signals in subcortical visual pathways.

We review here the distribution of S-cone signals and properties of S-cone recipient receptive fields in subcortical pathways. Nearly everything we know about S-cone signals in the subcortical visual system comes from the study of visual systems in cats and primates (monkeys); in this review, we concentrate on results from macaque and marmoset monkeys. We discuss segregation of S-cone recipient (blue-on and blue-off) receptive fields in the dorsal lateral geniculate nucleus and describe their receptive field properties. We treat in some detail the question of detecting weak S-cone signals as an introduction for newcomers to the field. Finally, we briefly consider the question on how S-cone signals are distributed among nongeniculate targets.

Color coding in the primate visual pathway: a historical view.

The physiology and anatomy of the primate visual pathway are reviewed from a historical perspective, especially in relation to color vision. From the work of the last decades, certain issues have been selected which remain unresolved and still pose a challenge for neurobiologists and psychophysicists. It is suggested that the structure of the primate visual pathway has been colored by the evolution of trichromacy and that many features of the parvocellular pathway represent adaptations to this end.

Independence and interaction of luminance and chromatic contributions to spatial hyperacuity performance.

Here we test interactions of luminance and chromatic input to spatial hyperacuity mechanisms. First, we tested alignment of luminance and chromatic gratings matched or mismatched in contrast polarity or grating type. Thresholds with matched gratings were low while all mismatched pairs were elevated. Second, we determined alignment acuity as a function of luminance or chromatic contrast alone or in the presence of constant contrast components of the other type. For in-phase components, performance followed the envelope of the more sensitive mechanism. However, polarity reversals revealed an asymmetric effect for luminance and chromatic conditions, which suggested that luminance can override chromatic mechanisms in hyperacuity; we interpret these findings in the context of spatial mechanisms.

Color vision: Introduction by the feature editors.

This feature issue of the Journal of the Optical Society of America A (JOSA A) stems from the 22nd Biennial Symposium of the International Colour Vision Society (ICVS) and reflects the basic and applied research interests of members of the color vision community. A profile is included of the 2013 Verriest Medal recipient.

Simultaneous chromatic and luminance human electroretinogram responses.

The parallel processing of information forms an important organisational principle of the primate visual system. Here we describe experiments which use a novel chromatic­achromatic temporal compound stimulus to simultaneously identify colour and luminance specific signals in the human electroretinogram (ERG). Luminance and chromatic components are separated in the stimulus; the luminance modulation has twice the temporal frequency of the chromatic modulation. ERGs were recorded from four trichromatic and two dichromatic subjects (1 deuteranope and 1 protanope). At isoluminance, the fundamental (first harmonic) response was elicited by the chromatic component in the stimulus. The trichromatic ERGs possessed low-pass temporal tuning characteristics, reflecting the activity of parvocellular post-receptoral mechanisms. There was very little first harmonic response in the dichromats' ERGs. The second harmonic response was elicited by the luminance modulation in the compound stimulus and showed, in all subjects, band-pass temporal tuning characteristic of magnocellular activity. Thus it is possible to concurrently elicit ERG responses from the human retina which reflect processing in both chromatic and luminance pathways. As well as providing a clear demonstration of the parallel nature of chromatic and luminance processing in the human retina, the differences that exist between ERGs from trichromatic and dichromatic subjects point to the existence of interactions between afferent post-receptoral pathways that are in operation from the earliest stages of visual processing.

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.

Psychophysical and physiological responses to gratings with luminance and chromatic components of different spatial frequencies.

Gratings that contain luminance and chromatic components of different spatial frequencies were used to study the segregation of signals in luminance and chromatic pathways. Psychophysical detection and discrimination thresholds to these compound gratings, with luminance and chromatic components of the one either half or double the spatial frequency of the other, were measured in human observers. Spatial frequency tuning curves for detection of compound gratings followed the envelope of those for luminance and chromatic gratings. Different grating types were discriminable at detection threshold. Fourier analysis of physiological responses of macaque retinal ganglion cells to compound waveforms showed chromatic information to be restricted to the parvocellular pathway and luminance information to the magnocellular pathway. Taken together, the human psychophysical and macaque physiological data support the strict segregation of luminance and chromatic information in independent channels, with the magnocellular and parvocellular pathways, respectively, serving as likely the physiological substrates.

Spatial distributions of cone inputs to cells of the parvocellular pathway investigated with cone-isolating gratings.

Receptive fields of midget ganglion cells and parvocellular lateral geniculate nucleus (LGN) neurons show color-opponent responses because they receive antagonistic input from the middle- and long-wavelength sensitive cones. It has been controversial as to whether this opponency can derive from random connectivity; if receptive field centers of cells near the fovea are cone-specific due to midget morphology, this would confer some degree of color opponency even with random cone input to the surround. A simple test of this mixed surround hypothesis is to compare spatial frequency tuning curves for luminance gratings and gratings isolating cone input to the receptive field center. If tuning curves for luminance gratings were bandpass, then with the mixed surround hypothesis tuning curves for gratings isolating the receptive field center cone class should also be bandpass, but to a lesser extent than for luminance. Tuning curves for luminance, chromatic, and cone-isolating gratings were measured in macaque retinal ganglion cells and LGN cells. We defined and measured a bandpass index to compare luminance and center cone-isolating tuning curves. Midget retinal ganglion cells and parvocellular LGN cells had bandpass indices between 0.1 and 1 with luminance gratings, but the index was usually near 1 (meaning low-pass tuning) when the receptive field center cone class alone was modulated. This is strong evidence for a considerable degree of cone-specific input to the surround. A fraction of midget and parvocellular cells showed evidence of incomplete specificity. Fitting the data with receptive field models revealed considerable intercell variability, with indications in some cells of a more complex receptive structure than a simple difference of Gaussians model.

Visual pathways and psychophysical channels in the primate.

The main cell systems of the retina that provide input to the striate cortex are now well described, although certain aspects of their anatomy and physiology remain contentious. Under simple stimulus conditions and in a threshold context psychophysical performance can often be assigned to one or other of these systems, and an identification of psychophysical channels with afferent pathways is justifiable. However, results from psychophysical studies using more complex stimulus conditions are more difficult to relate to 'front end' channels, and it is more difficult to separate the physiological contributions of afferent pathways from those of cortical mechanisms, in particular the separation of dorsal and ventral streams.

Segregation of chromatic and luminance signals using a novel grating stimulus.

Segregation of chromatic and luminance signals in afferent pathways are investigated with a grating stimulus containing luminance and chromatic components of different spatial frequencies. Ganglion cell recordings were obtained from the retinae of macaques (Macaca fascicularis). Cell responses to the 'compound' gratings were compared to responses to standard chromatic and luminance gratings. Parvocellular (PC) pathway cell responses to compound and chromatic gratings were very similar, as were magnocellular (MC) cell responses to compound and luminance gratings. This was the case over a broad range of spatial and temporal frequencies and contrasts. In psychophysical experiments with human observers, discrimination between grating types was possible close to detection threshold. These results are consistent with chromatic and luminance structure in complex patterns being strictly localized in different afferent pathways. This novel stimulus may prove useful in identifying afferent inputs to cortical neurons.

Temporal frequency and chromatic processing in humans: an fMRI study of the cortical visual areas.

Psychophysical sensitivity to isoluminant chromatic modulation declines at temporal frequencies beyond 4 Hz, whereas chromatically opponent cells of the afferent visual pathway (long- to middle-wavelength (L-M) cone-opponent or short-wavelength (S) cone cells) show responses at much higher temporal frequencies, indicating a central limitation in temporal processing capacity. Here, we sought to localize this limit in cortical retinotopic visual areas. We used fMRI to investigate responses of lateral geniculate nucleus and cortical visual areas in humans to isoluminant chromatic modulation as a function of temporal frequency (2-12 Hz). Our results suggest that L-M cone-opponent and S-cone signals are processed in LGN up to 12 Hz. In all visual areas except MT (middle temporal) and V3a, S-cone responses declined steeply with temporal frequency, implying that psychophysical sensitivity loss to blue-yellow modulation might occur early within these areas. While V1 showed robust L-M responses up to 12 Hz, there was a progressive falloff of responses with temporal frequency as information is transferred from V1 to higher areas (V2, V3, and V4), suggesting that, in humans, temporal limitation in perception of red-green chromatic modulation likely results from limited processing capacity of higher ventral extrastriate areas.

Combination of rod and cone inputs in parasol ganglion cells of the magnocellular pathway.

This study investigates how rod and cone inputs are combined in the magnocellular (MC) pathway in the mesopic luminance range, when both rods and cones are active. Responses of parafoveal MC ganglion cells from macaque retina were measured as a function of temporal frequency (0.62-20 Hz) or contrast (0.05-0.55) at mesopic light levels (0.2, 2, 20, and 200 td). Stimuli were of three modulation types: (1) isolated rod stimuli (only rod signals were modulated), (2) isolated cone stimuli (only cone luminance signals from long- and middle-wavelength sensitive cones were modulated), and (3) combined rod and cone stimuli (both rod and cone luminance signals were modulated in phase, as with conventional stimuli). The results showed that under mesopic conditions, the relative rod and cone inputs to the MC cells varied with light level and they are combined linearly prior to saturation. Further, rod contrast gain is relatively stable over the mesopic range while cone contrast gain increased with light level. Finally, the measured rod and cone inputs are consistent with the measured human temporal contrast sensitivity functions under comparable stimulation conditions.

Macaque ganglion cell responses to probe stimuli on modulated backgrounds.

In the natural environment, visual targets have to be detected and identified on changing backgrounds. Here, responses of parasol (magnocellular) ganglion cells to probes on modulated backgrounds are described. At low frequency, the adaptation level of the background influences the probe response, but with increasing frequency there is a strong interaction with the response to the background per se, so that on- and off-center cell responses are modulated in different phases. Interactions with the background response include both thresholding effects (when the cell's firing is suppressed and no pulse response occurs) and saturation effects (when the background response is vigorous the pulse generates few additional spikes). At 30 Hz, the effect of the pulse is largely a suppression or phase shift of the background response. The data are relevant to the probed-sinewave paradigm, in which pulse detection thresholds are modulated with pulse phase relative to a sinusoidal background. The physiological substrates of the psychophysical results with the probed-sinewave paradigm appear complex, with on- and off-center cells likely to contribute to detection at different pulse phases.