Samuel G. Solomon

The machinery of colour vision

Some fundamental principles of colour vision, deduced from perceptual studies, have been understood for a long time. Physiological studies have confirmed the existence of three classes of cone photoreceptors, and of colour-opponent neurons that compare the signals from cones, but modern work has drawn attention to unexpected complexities of early organization: the proportions of cones of different types vary widely among individuals, without great effect on colour vision; the arrangement of different types of cones in the mosaic seems to be random, making it hard to optimize the connections to colour-opponent mechanisms; and new forms of colour-opponent mechanisms have recently been discovered. At a higher level, in the primary visual cortex, recent studies have revealed a simpler organization than had earlier been supposed, and in some respects have made it easier to reconcile physiological and perceptual findings.

Early and Late Mechanisms of Surround Suppression in Striate Cortex of Macaque

The response of a neuron in striate cortex to an optimally configured visual stimulus is generally reduced when the stimulus is enlarged to encroach on a suppressive region that surrounds its classical receptive field (CRF). To characterize the mechanism that gives rise to this suppression, we measured its spatiotemporal tuning, its susceptibility to contrast adaptation, and its capacity for interocular transfer. Responses to an optimally configured grating confined to the CRF were strongly suppressed by annular surrounding gratings drifting at a wide range of temporal and spatial frequencies (including spatially uniform fields) that extended from well below to well above the range that drives most cortical neurons. Suppression from gratings capable of driving cortical CRFs was profoundly reduced by contrast adaptation and showed substantial interocular transfer. Suppression from stimuli that lay outside the spatiotemporal passband of most cortical CRFs was relatively stronger when the stimulus on the CRF was of low contrast, was generally insusceptible to contrast adaptation, and showed little interocular transfer. Our findings point to the existence of two mechanisms of surround suppression: one that is prominent when high-contrast stimuli drive the CRF, is orientation selective, has relatively sharp spatiotemporal tuning, is binocularly driven, and can be substantially desensitized by adaptation; the other is relatively more prominent when low-contrast stimuli drive the CRF, has very broad spatiotemporal tuning, is monocularly driven, and is insusceptible to adaptation. Its character suggests an origin in the input layers of primary visual cortex, or earlier.

Contrast sensitivity in natural scenes depends on edge as well as spatial frequency structure.

The contrast sensitivity function is routinely measured in the laboratory with sine-wave gratings presented on homogenous gray backgrounds; natural images are instead composed of a broad range of spatial and temporal structures. In order to extend channel-based models of visual processing to more natural conditions, we examined how contrast sensitivity varies with the context in which it is measured. We report that contrast sensitivity is quite different under laboratory than natural viewing conditions: adaptation or masking with natural scenes attenuates contrast sensitivity at low spatial and temporal frequencies. Expressed another way, viewing stimuli presented on homogenous screens overcomes chronic adaptation to the natural environment and causes a sharp, unnatural increase in sensitivity to low spatial and temporal frequencies. Consequently, the standard contrast sensitivity function is a poor indicator of sensitivity to structure in natural scenes. The magnitude of masking by natural scenes is relatively independent of local contrast but depends strongly on the density of edges even though neither greatly affects the local amplitude spectrum. These results suggest that sensitivity to spatial structure in natural scenes depends on the distribution of local edges as well as the local amplitude spectrum.

Spike sorting for large, dense electrode arrays

Developments in microfabrication technology have enabled the production of neural electrode arrays with hundreds of closely spaced recording sites, and electrodes with thousands of sites are under development. These probes in principle allow the simultaneous recording of very large numbers of neurons. However, use of this technology requires the development of techniques for decoding the spike times of the recorded neurons from the raw data captured from the probes. Here we present a set of tools to solve this problem, implemented in a suite of practical, user-friendly, open-source software. We validate these methods on data from the cortex, hippocampus and thalamus of rat, mouse, macaque and marmoset, demonstrating error rates as low as 5%.

Asymmetric localization of flotillins/reggies in preassembled platforms confers inherent polarity to hematopoietic cells

Hematopoietic cells have long been defined as round, nonpolar cells that show uniform distribution of cell surface-associated molecules. However, recent analyses of the immunological synapse and the importance of lipid microdomains in signaling have shed new light on the aspect of lymphocyte polarization during the activation processes, but none of the molecules implicated so far in either the activation process or the microdomain residency are known to have a preferential localization in nonactivated cells. Chemical crosslinking and fluorescence resonance energy transfer methods have allowed the visualization of certain glycosylphosphatidylinositol-anchored proteins in lipid rafts but so far no microdomain resident protein has been shown to exist as visible stable platforms in the membrane. We report here that two lipid microdomain resident proteins, flotillins/reggies, form preassembled platforms in hematopoietic cells. These platforms recruit signaling molecules upon activation through lipid rafts. The preassembled platforms significantly differ from the canonical cholesterol-dependent “lipid rafts,” as they are resistant to cholesterol-disrupting agents. Most evidence for the functional relevance of microdomains in living cells remains indirect. Using laser scanning confocal microscopy, we show that these proteins exist as stable, microscopically patent domains localizing asymmetrically to one pole of the cell. We present evidence that the asymmetric concentration of these microdomain resident proteins is built up during cytokinesis.

Chromatic sensitivity of ganglion cells in the peripheral primate retina.

Visual abilities change over the visual field. For example, our ability to detect movement is better in peripheral vision than in foveal vision, but colour discrimination is markedly worse. The deterioration of colour vision has been attributed to reduced colour specificity in cells of the midget, parvocellular (PC) visual pathway in the peripheral retina. We have measured the colour specificity (red–green chromatic modulation sensitivity) of PC cells at eccentricities between 20 and 50 degrees in the macaque retina. Here we show that most peripheral PC cells have red–green modulation sensitivity close to that of foveal PC cells. This result is incompatible with the view that PC pathway cells in peripheral retina make indiscriminate connections (‘random wiring’) with retinal circuits devoted to different spectral types of cone photoreceptors. We show that selective cone connections can be maintained by dendritic field anisotropy, consistent with the morphology of PC cell dendritic fields in peripheral retina. Our results also imply that postretinal mechanisms contribute to the psychophysically demonstrated deterioration of colour discrimination in the peripheral visual field.

Functional asymmetries in visual pathways carrying S-cone signals in macaque

In the lateral geniculate nucleus of macaque, we recorded from neurons with substantial input from S-cones and found that, on several important dimensions, the properties of neurons that receive inhibitory input from S-cones (“S−”) are quite unlike those of neurons that receive excitatory input from S-cones (“S+”). First, the organization of chromatic inputs differs substantially: in S+ cells, S-cone signals were usually opposed by those of L- and M-cones; in S− cells, signals from L-cones were usually opposed to those of S- and M-cones. Second, to pure S-cone modulation, S+ cells are twice as sensitive as S− cells, but S− cells were much more susceptible to contrast adaptation. Third, in S− cells but not S+ cells, the spatial frequency resolution for achromatic modulation was often greater, the tuning curve and more bandpass, than that for S-cone modulation. Along the dimensions on which we measured, the properties of the S+ cells were relatively tightly clustered, suggesting a homogenous class. Although the chromatic properties of S− cells are heterogeneous, the distribution of their tuning along other stimulus dimensions does not suggest multiple subtypes.

The Impact of Suppressive Surrounds on Chromatic Properties of Cortical Neurons

Stimulation of the suppressive surround of a cortical neuron affects the responsivity and tuning of the classical receptive field (CRF) on several stimulus dimensions. In V1 and V2 of macaques prepared for acute electrophysiological experiments, we explored the chromatic sensitivity of the surround and its influence on the chromatic tuning of the CRF. We studied receptive fields of single neurons with patches of drifting grating of optimal spatial frequency and orientation and variable size, modulated along achromatic or isoluminant color directions. The responses of most neurons declined as the patch was enlarged beyond the optimal size (surround suppression). In V1 the suppression evoked by isoluminant gratings was less than one-half that evoked by achromatic gratings. Consequently, many cells were most sensitive to achromatic modulation when patches just covered the CRF but were most sensitive to isoluminant modulation when patches were enlarged to cover the suppressive surround. Non-oriented neurons that were strongly chromatically opponent generally lacked suppressive surrounds. In V2 most neurons showed equal surround suppression from isoluminant gratings and achromatic gratings. This makes the relative sensitivity of V2 neurons to achromatic and isoluminant gratings mainly independent of the size of the grating. We also measured the chromatic properties of the CRF in the presence of differently colored surrounds. In neither V1 nor V2 did the surround alter the chromatic tuning of the CRF. Cortical mechanisms sensitive to chromatic contrast seem to provide little input to the suppressive surrounds of V1 neurons but substantial input to those of V2 neurons.

Spatial properties of koniocellular cells in the lateral geniculate nucleus of the marmoset Callithrix jacchus.

The receptive field dimensions, contrast sensitivity and linearity of spatial summation of koniocellular (KC), parvocellular (PC) and magnocellular (MC) cells in the lateral geniculate nucleus (LGN) of 11 adult marmosets were measured using achromatic sinusoidal gratings. The receptive field centre diameter of cells in each (PC, KC and MC) class increases with distance from the fovea. There is substantial overlap in centre size between the three cell classes at any eccentricity, but the PC cells have, on average, the smallest centres and the KC cells have the largest. Some PC and KC cells did not respond at all to the grating stimulus. The contrast sensitivity of the receptive field centre mechanism in KC cells decreases in proportion to the centre area. A similar trend was seen for the surround mechanism. These characteristics are common to PC and MC cells, suggesting that they originate at an early stage of visual processing in the retina. The KC cells showed, in general, lower peak evoked discharge rates than PC or MC cells. The spontaneous discharge rate of KC cells was lower than that of PC cells and similar to that of MC cells. The majority of cells in all divisions of the LGN show linear spatial summation. A few cells did show non‐linear spatial summation; these cells were predominantly located in the MC and ventral KC layers. The ventral KC layers below and between the MC layers contain cells with larger and more transiently responding receptive fields than cells in the more dorsal KC layers. We conclude that many of the contrast‐dependent spatial properties of cells in the marmoset LGN are common to PC, MC and KC cells. The main difference between KC cells and the other two classes is that there is more variability in their response properties, and they are less responsive to high spatial frequencies.

Suppressive Surrounds and Contrast Gain in Magnocellular-Pathway Retinal Ganglion Cells of Macaque

The modulation sensitivity of visual neurons can be influenced by remote stimuli which, when presented alone, cause no change in the ongoing discharge rate of the neuron. We show here that the extraclassical surrounds that underlie these effects are present in magnocellular-pathway (MC) but not in parvocellular-pathway (PC) retinal ganglion cells of the macaque. The response of MC cells to drifting gratings and flashing spots was halved by drifting or contrast-reversing gratings surrounding their receptive fields, but PC cell responses were unaffected. The suppression cannot have arisen from the classical receptive field, or been caused by scattered light, because it could be evoked by annuli that themselves caused little or no response from the cell, and is consistent with the action of a divisive suppressive mechanism. Suppression in MC cells was broadly tuned for spatial and temporal frequency and greater at high contrast. If perceptual phenomena with similar stimulus contexts, such as the “shift effect” and saccadic suppression, have a retinal component, then they reflect the activity of the MC pathway.