Russell L. De Valois

The orientation and direction selectivity of cells in macaque visual cortex

Quantitative data are presented on the orientation and direction specificity of the responses of cells in macaque monkey striate cortex. There is a bimodal distribution of direction-specific and nondirection-specific cells, with similar orientation tuning in each class. Cells range in orientation bandwidth at half amplitude from 6 degrees to 360 degrees (i.e. no orientation tuning), with a median near 40 degrees. Foveal-parafoveal and simple-complex subsamples show similar ranges of orientation bandwidths as well as similar medians (the bandwidths being somewhat broader than those found in cat cortex). The foveal subsample and a high-spatial-frequency subsample have more horizontal and vertical optimal orientations than oblique ones. Most cells show inhibition to some orientations, as well as excitation to others. Minimum-response orientations are generally less than 90 degrees from the optimal orientation--indicating maximum inhibition adjacent to the excitatory orientations. Three simple receptive field models are shown to differ in their abilities to account for these results.

Classifying simple and complex cells on the basis of response modulation

Hubel and Wiesel (1962; Journal of Physiology, London, 160, 106-154) introduced the classification of cortical neurons as simple and complex on the basis of four tests of their receptive field structure. These tests are partly subjective and no one of them unequivocally places neurons into distinct classes. A simple, objective classification criterion based on the form of the response to drifting sinusoidal gratings has been used by several laboratories, although it has been criticized by others. We review published and unpublished evidence which indicates that this simple and objective criterion reliability divides neurons of the striate cortex in both cats and monkeys into two groups that correspond closely to the classically-described simple and complex classes.

A multi-stage color model.

The first stage of our model has three cone types, with L:M:S cones in ratios of 10:5:1. In the second stage, retinal connectivity leads to three pairs of cone-opponent, and one pair of cone-nonopponent systems. At a third (cortical) stage of color processing, the S-opponent cells are added to or subtracted from the L- and M-opponent units to split and rotate the one effective parvo geniculate response axis into separate RG and YB color axes, and separate luminance from color. We also discuss changes with eccentricity, and connectivity based on correlated neural activity.

Psychophysical studies of monkey Vision-III. Spatial luminance contrast sensitivity tests of macaque and human observers

Abstract The detectability of luminance modulated gratings of different spatial frequencies was determined at five different adaptation levels for three macaque monkeys and five normal human observers. The human and macaque observers gave results which were identical in form and similar in absolute values. Both species showed optimal contrast sensitivity in the middle spatial frequency range of about 3–5 c/deg with both low and high frequency attenuation, at high light levels. Contrast sensitivity to high frequencies dropped rapidly as adaptation levels were lowered, with a resulting shift in peak sensitivity to lower spatial frequencies. At the lowest adaptation level studied, neither macaque nor human observers showed any low frequency attenuation in the spatial luminance contrast sensitivity function.

Vernier acuity with stationary moving Gabors

We examined the ability of observers to determine the vertical alignment of three Gabor patches (cosine gratings tapered in X and Y by Gaussians) when the grating within the middle patch was moving right or left. The comparison patches were flickered in counterphase, as was the test patch in a control condition. In all conditions, the Gabor patch itself (the envelope) was stationary. Vernier acuity (i.e. sensitivity) was almost as good with the moving as with the flickering Gabors, but there was a very pronounced positional bias in the case of the patterns in which the internal gratings were moving. The (stationary) patches appeared to be displaced in the direction of the grating movement. Thus if the grating were drifting rightwards, the observer would see the patches as being aligned only when the test patch position in fact was shifted far over to the left. This movement-related bias increased rapidly with retinal eccentricity, reaching 15 min at 8 deg eccentricity. The bias was greatest at 4-8 Hz temporal frequency, and at low spatial frequencies. Whether the patterns were on the horizontal or the vertical meridian was largely irrelevant, but larger biases were found with patterns moving towards or away from the fovea than with those moving in a tangential direction.

Spatial mapping of monkey VI cells with pure color and luminance stimuli

We recorded the responses of single macaque striate cortical cells to color-varying and luminance-varying patterns. We show that (a) the vast majority of primate striate cells respond to pure color stimuli, in addition to responding to luminance-varying stimuli (b) in general, simple cells are color-selective whereas complex cells respond to multiple color regions, (c) most cortical cells show bandpass spatial frequency tuning to pure color-varying gratings, with various cells tuned to each of a wide range of spatial frequencies and (d) the peak spatial frequency and bandwidth of most striate cells is the same for color as for luminance-varying gratings; when they differ, cells tend to be more broadly tuned and peak at lower spatial frequencies for color (e) complex cells, on the average, respond to higher spatial frequencies than do simple cells.

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,.

Spatial and temporal receptive fields of geniculate and cortical cells and directional selectivity

The spatio-temporal receptive fields (RFs) of cells in the macaque monkey lateral geniculate nucleus (LGN) and striate cortex (V1) have been examined and two distinct sub-populations of non-directional V1 cells have been found: those with a slow largely monophasic temporal RF, and those with a fast very biphasic temporal response. These two sub-populations are in temporal quadrature, the fast biphasic cells crossing over from one response phase to the reverse just as the slow monophasic cells reach their peak response. The two sub-populations also differ in the spatial phases of their RFs. A principal components analysis of the spatio-temporal RFs of directional V1 cells shows that their RFs could be constructed by a linear combination of two components, one of which has the temporal and spatial characteristics of a fast biphasic cell, and the other the temporal and spatial characteristics of a slow monophasic cell. Magnocellular LGN cells are fast and biphasic and lead the fast-biphasic V1 subpopulation by 7 ms; parvocellular LGN cells are slow and largely monophasic and lead the slow monophasic V1 sub-population by 12 ms. We suggest that directional V1 cells get inputs in the approximate temporal and spatial quadrature required for motion detection by combining signals from the two non-directional cortical sub-populations which have been identified, and that these sub-populations have their origins in magno and parvo LGN cells, respectively.

Temporal properties of brightness and color induction.

With a matching procedure, we studied the temporal properties of direct brightness (or lightness) and chromatic changes (produced by modulation of the region being matched) and induced brightness and chromatic changes (produced by modulation of the surround of the region being matched). The amount of direct brightness and color change was found to vary only slightly with temporal frequency over the 0.5-8 Hz range studied, whereas induced changes were found to occur only at low temporal frequencies, below about 2.5 Hz. With high temporal-frequency modulation of the surround, the induced patterns appeared to flicker but not to change in brightness or color. Despite the fact that chrominance and luminance temporal contrast sensitivity functions are very different, the temporal induction curves for color and brightness were very similar. However, brightness induction was found to increase approximately linearly with increasing surround modulation up to very high levels, whereas the amount of color induction was much less dependent on the modulation depth of the surround.

Hue Scaling of Isoluminant and Cone-specific Lights

Using a hue scaling technique, we have examined the appearance of colored spots produced by shifts from white to isoluminant stimuli along various color vectors in order to examine color appearance without the complications of the combined luminance and chromatic stimulation involved in most previous hue scaling studies, which have used flashes of monochromatic light. We also used spots lying along cone-isolating vectors in order to determine what hues would be reported with a change in activation of only single cone types or of only single geniculate opponent-cell types, an issue of direct relevance to any model of color vision. We find that: 1. Unique hues do not correspond either to the change in activation of single cone types or of single geniculate opponent-cell types. This is well known to be the case for yellow and blue, but we find it to be true for red and green as well. 2. These conclusions are not limited to the particular white (Illuminant C) used as an adapting background in most of the experiments. Shifts along the same cone-contrast vectors relative to different backgrounds lead to much the same hue percepts, independent of the starting white used. 3. The shifts of the perceptual colors from the geniculate axes are in the directions, and close to the absolute amounts, predicted by our [De Valois & De Valois (1993). Vision Research, 33, 1053-1065] multi-stage color model in which we postulate that the S-opponent cells are added to or subtracted from the M- and L-opponent cells to form the four perceptual color systems. 4. There are distinct asymmetries with respect to the extent to which various hues within each perceptual opponent system deviate from the geniculate opponent-cell axes. Blue is shifted more from the S-LM axis than is yellow; green is shifted more from the L-M axis than is red. There are also asymmetries in the angular extent of opponent color regions. Blue is seen over a larger range of color vectors than is yellow, and red over a slightly larger range than green. 5. Such asymmetries are not accounted for by any model that treats red-green and yellow-blue each as unitary, mirror-image opponent-color systems. Although red and green are perceptually opponent, the red and green perceptual systems do not appear to be constructed in a mirror-image fashion with respect to input from different cone types or from different geniculate opponent-cell types. The same is true for yellow and blue.