Chromatic and achromatic vision of macaques: role of the P pathway

Chromatic and achromatic contrast sensitivity were measured in a human observer, 2 normal macaque monkeys, and 3 monkeys with severe toxicant-induced damage to the parvocellular projecting retinogeniculate pathway (P cell-deficient monkeys). Damage to the P pathway was produced by the oral administration of acrylamide monomer (Eskin and Merigan, 1986). Contrast sensitivity was measured in all subjects with isochromatic luminance gratings, as well as isoluminant chromatic gratings, modulated along several directions of a color space that represents color-opponent and luminance contrast (Krauskopf et al., 1986). The chromatic and achromatic sensitivity of the control monkeys was virtually identical to that of the human observer. Chromatic sensitivity of the P cell-deficient monkeys, measured at a low spatial frequency (0.3 c/deg), along a constant-blue color axis, was 0.9-1.5 log units lower than that of controls. Similar losses were seen along a tritanopic confusion axis and along 2 intermediate axes of color direction. Chromatic thresholds measured at higher spatial frequency (2.0 c/deg) were similarly reduced. Counterphase-modulated chromatic gratings were used to test color sensitivity over a range of temporal frequencies up to 15 Hz, and the loss of color vision was substantial over the entire range of frequencies. The luminance contrast sensitivity of the P cell-deficient monkeys for stationary gratings decreased after exposure by 0.5-0.8 log units. These results indicate that the chromatic and achromatic spatial vision of macaques is very similar to that of humans. They also suggest that the P pathway plays an important role in macaque chromatic sensitivity at all spatial frequencies, as well as achromatic sensitivity at high spatial and lower temporal frequencies.     

A case study of cortical colour "blindness" with relatively intact achromatic discrimination.

A patient is described whose most striking visual disorder was a grossly impaired ability to discriminate between different colours (hues) that were matched for brightness. In contrast his ability to discriminate between different neutral greys presented in the same fashion was much less abnormal, even though the greys were perceptually difficult. Although visual acuity was reduced and visual fields were constricted, and the patient's memory was moderately impaired, these associated symptoms could not themselves be the cause of his unusual colour vision. The patient had the symptoms of cerebral achromatopsia, and the relative preservation of his form vision (when his reduced acuity is taken into account) and his achromatic vision supports the view that the many different visual cortical areas recently demonstrated in the brains of monkeys, and presumed to exist in man, have a perceptual specialisation that matches their physiological differences.     

Visual function of a patient with advanced adrenoleukodystrophy: comparison of luminance and color contrast sensitivities

We assessed achromatic luminance and isoluminant chromatic contrast sensitivity functions of a 20-year-old male. He showed severe motor and intellectual disabilities after advanced adrenoleukodystrophy, which started at the age of 7. Optokinetic nystagmus (OKN) to drifting gratings was used to assess his contrast sensitivities. Although the achromatic luminance contrast sensitivities were lower over the entire range of spatial frequencies tested than those of the healthy adults, they were preserved to the level comparable to healthy 7-year-old children, except for the frequency of 1 and 4 cycles/degree. In contrast, both of the red-green and blue chromatic contrast sensitivities were remarkably lower in all frequency range compare to healthy children and adults. These results indicate that it is possible for even an advanced case of ALD to show residual visual capacity that was preserved to a remarkable extent.     

Cerebral Achromatopsia in Monkeys

In human cerebral achromatopsia, extrastriate cortical damage produces a severe or complete loss of colour vision, with relative sparing of non-chromatic vision. The critical lesion appears to be in a medial occipito-temporal area, occupying the lingual and caudal fusiform gyri; positron emission tomography has shown that this cortical region is one of several activated in normal human observers during colour vision tasks. Attempts to find an analogous 'colour centre' in the cortex of monkeys have not been successful. In particular, ablation of cortical area V4, sometimes thought on physiological grounds to be more involved in wavelength and colour coding than any other visual cortical area, produces only mild impairments in colour discrimination. In the present study we tested the colour vision of monkeys after cortical ablations that mainly or entirely spared area V4. One group of monkeys (group AT) received ablations in the temporal lobe anterior to area V4, and a second group (group MOT) received ablations in a medial occipito-temporal area roughly corresponding in cranial location to the lesion that produces human cerebral achromatopsia. The animals in group MOT showed no impairment of their colour vision. Group AT, in contrast, had a severe impairment in chromatic vision, with a relative sparing of non-chromatic vision. Their behaviour was indistinguishable from that of a human patient with total cerebral achromatopsia who had been tested on the same tasks. These results show that area V4 in macaque monkeys is not analogous, and probably not homologous, to the human colour centre. Instead, they suggest that the area of the monkey's brain corresponding to the colour area in the human brain is in the temporal cortex, anterior to area V4.     

Selectivity of human retinotopic visual cortex to S-cone-opponent, L/M-cone-opponent and achromatic stimulation

Our aim was to make a quantitative comparison of the response of the different visual cortical areas to selective stimulation of the two different cone-opponent pathways [long- and medium-wavelength (L/M)- and short-wavelength (S)-cone-opponent] and the achromatic pathway under equivalent conditions. The appropriate stimulus-contrast metric for the comparison of colour and achromatic sensitivity is unknown, however, and so a secondary aim was to investigate whether equivalent fMRI responses of each cortical area are predicted by stimulus contrast matched in multiples of detection threshold that approximately equates for visibility, or direct (cone) contrast matches in which psychophysical sensitivity is uncorrected. We found that the fMRI response across the two colour and achromatic pathways is not well predicted by threshold-scaled stimuli (perceptual visibility) but is better predicted by cone contrast, particularly for area V1. Our results show that the early visual areas (V1, V2, V3, VP and hV4) all have robust responses to colour. No area showed an overall colour preference, however, until anterior to V4 where we found a ventral occipital region that has a significant preference for chromatic stimuli, indicating a functional distinction from earlier areas. We found that all of these areas have a surprisingly strong response to S-cone stimuli, at least as great as the L/M response, suggesting a relative enhancement of the S-cone cortical signal. We also identified two areas (V3A and hMT+) with a significant preference for achromatic over chromatic stimuli, indicating a functional grouping into a dorsal pathway with a strong magnocellular input.     

Parvocellular pathway impairment in autism spectrum disorder: Evidence from visual evoked potentials

In humans, visual information is processed via parallel channels: the parvocellular (P) pathway analyzes color and form information, whereas the magnocellular (M) stream plays an important role in motion analysis. Individuals with autism spectrum disorder (ASD) often show superior performance in processing fine detail, but impaired performance in processing global structure and motion information. To date, no visual evoked potential (VEP) studies have examined the neural basis of atypical visual performance in ASD. VEPs were recorded using 128-channel high density EEG to investigate whether the P and M pathways are functionally altered in ASD. The functioning of the P and M pathways within primary visual cortex (V1) were evaluated using chromatic (equiluminant red–green sinusoidal gratings) and achromatic (low contrast black–white sinusoidal gratings) stimuli, respectively. Unexpectedly, the N1 component of VEPs to chromatic gratings was significantly prolonged in ASD patients compared to controls. However, VEP responses to achromatic gratings did not differ significantly between the two groups. Because chromatic stimuli preferentially stimulate the P-color but not the P-form pathway, our findings suggest that ASD is associated with impaired P-color pathway activity. Our study provides the first electrophysiological evidence for P-color pathway impairments with preserved M function at the V1 level in ASD.     

Direct and transcallosal contribution to the cortical visual evoked response in rats

The averaged visually evoked cortical potential (VECP) in response to contrast reversal of a grating was measured on striate cortex over a range of spatial frequencies and contrasts. The response to binocular or monocular stimulation was almost abolished by unilateral section of the optic tract on the side of the recording, indicating that the transcallosal pathway makes little contribution to the VECP. Additional section of the corpus callosum, and application of spreading depression to the normal hemisphere shows that the small response following tract section was transcallosal. It was confined to stimuli of low spatial frequencies and high contrast.     

Task related EEG alpha asymmetries and abnormalities of hemispheric specialisation in schizophrenia

Spatial contrast sensitivity was behaviorally determined for two monocularly lid-sutured cats. The spatial contrast sensitivity function for the non-deprived eyes matched previously reported functions obtained from normally reared cats. In comparison, sensitivity was significantly lower at all spatial frequencies for the deprived eye of both cats. In one cat, subsequent removal of the non-deprived eye resulted in a two to threefold increase in sensitivity at all spatial frequencies. However, no improvement in sensitivity was observed for the second animal. Single-unit electrophysiological recording in the striate cortex of these two animals revealed a postenucleation difference in the percent of visually influenced cells. In the cat for which no behavioral improvement occurred, only 13% of striate cortex cells could be driven by visual stimulation of the previously deprived eye. In contrast 38% of striate cortex cells were similarly influenced in the cat for which visual improvement was observed. These data suggest a correlation between the physiological effectiveness of the postcritical period enucleation procedure and the visual capacity of monocularly lid-sutured cats.     

The effect of spatial frequency on chromatic and achromatic steady-state visual evoked potentials.

OBJECTIVE: Little is known about the physiological properties of the major components of steady-state visual evoked potentials (VEPs). Based on the hypothesis that isoluminant color and high contrast pattern differentially activate the parvo- and magnocellular pathways, we studied difference in spatial frequency function between chromatic and achromatic VEPs to sinusoidal gratings. METHODS: Steady-state VEPs to isoluminant chromatic (red-green) and high contrast (90%) achromatic (black-white) sinusoidal gratings with nine spatial frequencies (0.5 to 8.0 cycles/degrees (cpd)) at 4 Hz (8 reversals/s) were recorded in 13 normal subjects. VEPs were Fourier analyzed to obtain phase and amplitude of the second (2F) and fourth (4F) harmonic responses. RESULTS: The 2F amplitude of chromatic VEPs decreased above 4.0 cpd in a low-pass function while that of achromatic VEPs showed a band-pass function with a peak at 4.0 cpd. The 4F amplitude of chromatic VEPs was not affected significantly by spatial frequency whereas that of achromatic VEPs exhibited a high-pass function. The phases of 2F and 4F showed a non-monotonic function of spatial frequency in both chromatic and achromatic stimuli with peaks at middle spatial frequencies. CONCLUSION: Chromatic and achromatic visual stimuli differently affected 2F and 4F components, which thus suggests that 2F and 4F components are generated from different neuronal subgroups largely in the parvocellular pathway.     

Attentional capture by colour and motion in cerebral achromatopsia

Cerebral achromatopsia is a rare condition in which damage to the ventromedial occipital area of the cortex results in the loss of colour experience. Nevertheless, cortically colour-blind patients can still use wavelength variation to perceive form and motion. In a series of six experiments we examined whether colour could also direct exogenous attention in an achromatopsic observer. We employed the colour singleton paradigm, the phi motion effect, and the correspondence process to assess attentional modulation. Although colour singletons failed to capture attention, a motion signal, based solely on chromatic information, was able to direct attention in the patient. We then show that the effect is abolished when the chromatic contours of stimuli are masked with simultaneous luminance contrast. We argue that the motion effect is dependent on chromatic contrast mediated via intact colour-opponent mechanisms. The results are taken as further evidence for the processing of wavelength variation in achromatopsia despite the absence of colour experience.     

Distinct contrast response functions in striate and extra-striate regions of visual cortex revealed with magnetoencephalography (MEG).

OBJECTIVE: To spatially and temporally characterise the cortical contrast response function to pattern onset stimuli in humans. METHODS: Magnetoencephalography (MEG) was used to investigate the human cortical contrast response function to pattern onset stimuli with high temporal and spatial resolution. A beamformer source reconstruction approach was used to spatially localise and identify the time courses of activity at various visual cortical loci. RESULTS: Consistent with the findings of previous studies, MEG beamformer analysis revealed two simultaneous generators of the pattern onset evoked response. These generators arose from anatomically discrete locations in striate and extra-striate visual cortex. Furthermore, these loci demonstrated notably distinct contrast response functions, with striate cortex increasing approximately linearly with contrast, whilst extra-striate visual cortex followed a saturating function. CONCLUSIONS: The generators that underlie the pattern onset visual evoked response arise from two distinct regions in striate and extra-striate visual cortex. SIGNIFICANCE: The spatially, temporally and functionally distinct mechanisms of contrast processing within the visual cortex may account for the disparate results observed across earlier studies and assist in elucidating causal mechanisms of aberrant contrast processing in neurological disorders.     

Anosognosia for cerebral achromatopsia—A longitudinal case study

Cerebral achromatopsia is a rare disorder of colour vision caused by bilateral damage to the occipito-temporal cortex. Patients with cerebral achromatopsia are commonly said to suffer due to their disturbed colour sense. Here, we report the case of a patient with cerebral achromatopsia who was initially unaware of his deficit, although three experiments with eye movement recordings demonstrated his severe inability to use colour information in everyday tasks. During two months, the evolution of his colour vision deficit was followed with repeated standardized colour vision tests and eye movement recordings. While his performance continuously improved, he became more and more aware of the deficit. Only after colour vision had almost normalized, his subjective colour sensation was inconspicuous again. The simultaneous occurrence of achromatopsia and the corresponding anosognosia and their parallel recovery suggest that both deficits were due to dysfunction of the same brain region. Consequently, the subjective experience of colour loss in achromatopsia may depend on the residual function of the damaged colour centre.     

The processing of edge information in visual areas of the cortex as evidenced by evoked potentials

Using averaged visually evoked potentials (VEPs), recorded from bipolar cortical electrodes, as indicators of sensory information processing, the sensitivity to stimulus differences of parafoveal and foveal striate, foveal prestriate, and inferotemporal cortex was measured in 3 rhesus monkeys. The stimuli used were a blank field and a series of 5 checkerboard patterns in which check size was varied from 2°24′ to 9′ of retinal arc subtended per check. All stimuli had equal luminance (5.0 ft.-Lamberts) and duration (9 μsec).The results of this study indicate that: (1) VEPs obtained in all of the cortical regions were sensitive to stimulus differences simultaneously at several points along the temporal continuum following the stimulus; (2) the earliest signs of sensitivity to stimulus differences in the VEPs generally appeared initially in the parafoveal striate cortex at about 70 msec post stimulus and tended to be followed in succession by foveal striate, foveal prestriate, and inferotemporal cortex; (3) sensitivity was found for at least 190 msec and as long as 400 msec after stimulus presentation for all of the cortical regions examined and was generally maintained in foveal and parafoveal striate cortex for longer periods than in foveal prestriate and inferotemporal cortex; (4) the most significant signs of sensitivity were found in the parafoveal striate cortex and a simple transformation of edge information into VEP amplitude was shown to occur there; and (5) none of the cortical regions demonstrated long-term habituation of sensitivity to stimulus differences.These data give evidence for both serial and parallel processing of edge information between and within the different regions of the primary visual and visual association cortex with an apparent focus of edge information processing in parafoveal striate cortex.     

Cerebral color blindness: an acquired defect in hue discrimination.

In contrast to the traditional view that striate visual cortex (area 17) is surrounded by two homogeneous cortical areas (areas 18 and 19), recent studies have shown that mammalian extrastriate visual cortex contains several anatomically and functionally distinct subregions. One such region, the V-4 complex of the rhesus monkey, is highly specialized for the analysis of color information, suggesting that a lesion in a homologous region might produce a defect in color vision while sparing other visual functions. We have studied a patient whose clinical syndrome supports this suggestion: a 44-year-old man with normal color vision suffered two cerebral infarctions that produced first a right and then a left superior homonymous quadrantanopia and also caused prosopagnosia, topographical disorientation, and severely impaired color vision. Computed tomography demonstrated extensive lesions in both inferior occipital lobes in the territories of the lateral branches of the posterior cerebral arteries, involving the lingual and medial occipitotemporal gyri bilaterally; these gyri contain the inferior portion of striate cortex and segments of extrastriate visual cortex. The patient had no difficulty in giving the correct color names associated with common objects presented either verbally or in outline drawings. Standardized testing with the Farnsworth-Munsell 100-hue test, the Nagel anomaloscope, and a method that tests for just-noticeable differences between monochromatic stimuli all showed that the patient's ability to distinguish one color from another was markedly imparied but not totally absent. In contrast, visual acuity, reading, visually guided eye movements, and stereopsis were normal. Cells in the V-4 complex of monkey extrastriate cortex are highly specialized for distinguishing one color from another; the hue discrimination deficit that was demonstrated in this patient with cerebral color blindness indicates that a region or regions with similar function has been damaged.     

Functional anatomy of macaque striate cortex. IV. Contrast and magno-parvo streams

Macaque monkeys were shown achromatic gratings of various contrasts during 14C-2-deoxy-d-glucose (DG) infusion in order to measure the contrast sensitivity of different subdivisions of primary visual cortex. DG uptake is essentially saturated at stimulus contrasts of 50% and above, although the saturation contrast varies with layer and with different criteria. Following visual stimulation with gratings of 8% contrast, stimulus-driven uptake was relatively high in striate layer 4Ca (which receives primary input from the magnocellular LGN layers), but was absent in layer 4Cb (which receives primary input from the parvocellular layers). In this same (magnocellular-specific) stimulation condition, striate layers 4B, 4Ca, and 6 showed strong stimulus-induced DG uptake, and layers 2, 3, 4A, and 5 showed only light or negligible uptake. By comparison to other cases that were shown stimuli of systematically higher contrast, and to a wide variety of DG cases shown very different stimuli, it is evident that information derived from the magnocellular and parvocellular layers in the LGN remains partially, or largely, segregated in its passage through striate cortex, and projects in a still somewhat segregated fashion to different extrastriate areas. The sum of all available evidence suggests that the magnocellular information projects strongly through striate layers 4Ca, 4B, and 6, with moderate input into the blobs in layers 2 + 3, and to blob-aligned portions of layer 4A. Parvocellular-dominated regions of striate cortex include both the blob and interblob portions of layers 2 + 3, 4A, 4Cb, and 5. Because the major striate input to V2 arrives from striate layers 2 + 3, and because the major striate input to MT originates in layer 4B and 6, it appears that area V2 receives information derived largely from the parvocellular LGN layers, and that area MT receives information derived mainly from the magnocellular layers.     

Visual evoked potentials and positron emission tomographic mapping of regional cerebral blood flow and cerebral metabolism: can the neuronal potential generators be visualized?

Visual evoked potentials (VEPs) and visual evoked spectrum array (VESA) to flashes and pattern-reversal were correlated with regional cerebral blood flow (rCBF) or local cerebral glucose metabolism in 4 hemianopsic patients and one subject with cortical blindness. Normal VEPs, topographical distribution and occipital rCBF were noted in hemianopsic patients with macular sparing. A dissociation of topographical distribution of VEPs to flashes and pattern-reversal was demonstrated in one patient with hemianopsia and macular splitting. In this case, rCBF showed unilateral activation of visual areas 17, 18 and 19 of the cortex. The distribution of surface-recorded potentials reflected the complex interaction of electrical field potentials within at least 3 cortical areas rather than volume transmission of striate dipoles alone. VEPs were preserved in a cortically blind patient. rCBF and local cerebral glucose metabolism revealed a functioning island of occipital cortex that most likely represented the generator of the VEP. The combination of VEP and PET permits the correlation of electrophysiological events with the visualization of cortical areas presumably activated by the same visual stimulus.     

Spatial and temporal sensitivity degradation of primary visual cortical cells in senescent rhesus monkeys

Human visual function declines with age. Much of this decline is mediated by changes in the central visual pathways. In this study we compared the spatial and temporal sensitivities of striate cortical cells in young and old paralysed macaque monkeys. Extracellular single-unit recordings were employed. Our results show that cortical neurons in old monkeys exhibit lower optimal spatial and temporal frequencies, lower spatial resolution and lower high temporal frequency cut-offs than do cells in young adult monkeys. These changes in old monkeys are accompanied by increased visually evoked responses, increased spontaneous activities and decreased signal-to-noise ratios. The increased excitability of cells in old animals is consistent with an age-related degeneration of intracortical inhibition. The degradation of spatial and temporal function in old striate cortex should contribute to the decline in visual function that accompanies normal aging.     

Convergence of parvocellular and magnocellular information channels in the primary visual cortex of the macaque

We investigated whether responses of single cells in the striate cortex of anaesthetized macaque monkeys exhibit signatures of both parvocellular (P) and magnocellular (M) inputs from the dorsal lateral geniculate nucleus (dLGN). We used a palette of 128 isoluminant hues at four different saturation levels to test responses to chromatic stimuli against a white background. Spectral selectivity with these isoluminant stimuli was taken as an indication of P inputs. The presence of magnocellular inputs to a given cortical cell was deduced from its responses to a battery of tests, including assessment of achromatic contrast sensitivity, relative strengths of chromatic and luminance borders in driving the cell at different velocities and conduction velocity of their retino-geniculo-cortical afferents. At least a quarter of the cells in our cortical sample appear to receive convergent P and M inputs. We cannot however, exclude the possibility that some of these cells could be receiving a convergent input from the third parallel channel from the dLGN, namely the koniocellular (K) rather than the P channel. The neurons with convergent P and M inputs were recorded not only from supragranular and infragranular layers but also from the principal geniculate input recipient layer 4. Thus, our results challenge classical ideas of strict parallelism between different information streams at the level of the primate striate cortex.     

Chromatic mechanisms in striate cortex of macaque

We measured the responses of 305 neurons in striate cortex to moving sinusoidal gratings modulated in chromaticity and luminance about a fixed white point. Stimuli were represented in a 3-dimensional color space defined by 2 chromatic axes and a third along which luminance varied. With rare exceptions the chromatic properties of cortical neurons were well described by a linear model in which the response of a cell is proportional to the sum (for complex cells, the rectified sum) of the signals from the 3 classes of cones. For each cell there is a vector passing through the white point along which modulation gives rise to a maximal response. The elevation (theta m) and azimuth (phi m) of this vector fully describe the chromatic properties of the cell. The linear model also describes neurons in l.g.n. (Derrington et al., 1984), so most neurons in striate cortex have the same chromatic selectivity as do neurons in l.g.n. However, the distributions of preferred vectors differed in cortex and l.g.n.: Most cortical neurons preferred modulation along vectors lying close to the achromatic axis and those showing overt chromatic opponency did not fall into the clearly defined chromatic groups seen in l.g.n. The neurons most responsive to chromatic modulation (found mainly in layers IVA, IVC beta, and VI) had poor orientation selectivity, and responded to chromatic modulation of a spatially uniform field at least as well as they did to any grating. We encountered neurons with band-pass spatial selectivity for chromatically modulated stimuli in layers II/III and VI. Most had complex receptive fields. Neurons in layer II/III did not fall into distinct groups according to their chromatic sensitivities, and the chromatic properties of neurons known to lie within regions rich in cytochrome oxidase appeared no different from those of neurons in the interstices. Six neurons, all of which resembled simple cells, showed unusually sharp chromatic selectivity.     

Visual command hallucinations in a patient with pure alexia

Around 25% of patients with visual hallucinations secondary to eye disease report hallucinations of text. The hallucinated text conveys little if any meaning, typically consisting of individual letters, words, or nonsense letter strings (orthographic hallucinations). A patient is described with textual visual hallucinations of a very different linguistic content following bilateral occipito-temporal infarcts. The hallucinations consisted of grammatically correct, meaningful written sentences or phrases, often in the second person and with a threatening and command-like nature (syntacto-semantic visual hallucinations). A detailed phenomenological interview and visual psychophysical testing were undertaken. The patient showed a classical ventral occipito-temporal syndrome with achromatopsia, prosopagnosia, and associative visual agnosia. Of particular significance was the presence of pure alexia. Illusions of colour induced by monochromatic gratings and a novel motion-direction illusion were also observed, both consistent with the residual capacities of the patient's spared visual cortex. The content of orthographic visual hallucinations matches the known specialisations of an area in the left posterior fusiform gyrus--the visual word form area (VWFA)--suggesting the two are related. The VWFA is unlikely to be responsible for the syntacto-semantic hallucinations described here as the patient had a pure alexic syndrome, a known consequence of VWFA lesions. Syntacto-semantic visual hallucinations may represent a separate category of textual hallucinations related to the cortical network implicated in the auditory hallucinations of schizophrenia.