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.     

Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey

We tested color and contrast sensitivity in the magnocellular and parvocellular subdivisions of the lateral geniculate body and in layers 2, 3, 4B, and 4C alpha of visual area 1 to obtain physiological data on the degree of segregation of the 2 pathways and on the fate of the color and contrast information as it is transmitted from the geniculate to the cortex. On average, magnocellular geniculate cells were much less responsive than parvocellular cells to shifts between 2 equiluminant colors. Nevertheless, many magnocellular cells (though not all) continued to give some response at equiluminance. As expected from previous studies, luminance contrast sensitivity differed markedly between magnocellular and parvocellular layers. In V-1, the properties of cells in the magnorecipient layers 4C alpha and 4B faithfully reflected the properties of magnocellular geniculate cells, showing no evidence of any parvocellular input. Like magnocellular geniculate cells, they showed high contrast sensitivity, and with color contrast stimuli they showed large response decrements at equiluminance. In the interblob regions of cortical layers 2 and 3, which anatomically appear to receive most of their inputs from parvorecipient layer 4C beta, contrast sensitivities of some of the cells were compatible with a predominantly parvocellular input. Other interblob cells had sensitivities intermediate between magno- and parvocellular geniculate cells, suggesting a possible contribution from the magnocellular system. Many cells in cortical layers 2 and 3 responded to color-contrast borders equally well at all relative brightnesses of the 2 colors, including equiluminance. We recorded from many direction- and disparity-selective cells in V-1: most of the direction-selective and all of the clearly stereo-selective cells were located in layer 4B.     

Dysfunction of early-stage visual processing in schizophrenia.

OBJECTIVE: Schizophrenia is associated with deficits in higher-order processing of visual information. This study evaluated the integrity of early visual processing in order to evaluate the overall pattern of visual dysfunction in schizophrenia. METHOD: Steady-state visual-evoked potential responses were recorded over the occipital cortex in patients with schizophrenia and in age- and sex-matched comparison volunteers. Visual-evoked potentials were obtained for stimuli composed of isolated squares that were modulated sinusoidally in luminance contrast, number of squares, or chromatic contrast in order to emphasize magnocellular or parvocellular visual pathway activity. RESULTS: Responses of patients to magnocellular-biased stimuli were significantly lower than those of comparison volunteers. These lower response levels were observed in conditions using both low luminance contrast and large squares that biased processing toward the magnocellular pathway. In contrast, responses to stimuli that biased processing toward the parvocellular pathway were not significantly different between schizophrenia patients and comparison volunteers. A significant interaction of group and stimulus type was observed in the condition using low luminance contrast. CONCLUSIONS: These findings suggest a dysfunction of lower-level visual pathways, which was more prominent for magnocellular than parvocellular biased stimuli. The magnocellular pathway helps in orienting toward salient stimuli. A magnocellular pathway deficit could contribute to higher-level visual cognitive deficits in schizophrenia.     

Visual acuity in hooded rats: effects of superior collicular or posterior neocortical lesions

The visual resolution acuity of hooded rats was measured with an avoidance technique, using large, high contrast square-wave gratings of high mean luminance. Measurements were taken before and after ablation of either posterior cortex or the superior colliculus. The cortical lesions included both striate and temporal cortex, and caused retrograde degeneration throughout the dorsal lateral geniculate nucleus. Neither group showed signs of detecting even coarse square-wave gratings when first tested after operation. The animals with collicular lesions quickly relearnt, and their acuity was unaltered. After extensive training 3 out of 4 cortical animals relearnt to detect gratings, and their acuity was reduced to about one-third of its preoperative value. It seems likely that in rats the geniculocortical pathway carries sufficient information for the normal detection of high spatial frequencies. Whether a pathway from superior colliculus to neocortex via a thalamic relay also carries this information is uncertain.     

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.     

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.     

Luminance and chromatic contrast sensitivity in dyslexia: the magnocellular deficit hypothesis revisited

The hypothesis of a magnocellular channel deficit in dyslexia was tested. Subjects were 10-year-old dyslexics and normal readers. Psychophysical thresholds for luminance and chromatic contrasts were estimated using black and white and red and green sinusoidal gratings of various spatial frequencies, presented in static and dynamic conditions (drift and reversal). Significant group differences were found for luminance contrast, with a higher sensitivity in dyslexics. No group differences were obtained for chromatic contrast. High luminance contrast sensitivity correlated with low reading and writing skills. The typical finding of an increase contrast sensitivity to low spatial frequency gratings, due to their dynamic presentations, was absent in dyslexics. The results provide support for the magnocellular deficit hypothesis. The pattern of this deficit, however, is much more complex than that emerging from previous research.     

Projections of three subcortical visual centers to marmoset lateral geniculate nucleus

The dorsal lateral geniculate nucleus receives projections from visuotopically organized subcortical nuclei, in addition to inputs from the retina, visual cortices, and the thalamic reticular nucleus. Here, we study subcortical projections to the geniculate from the superior colliculus (SC) and parabigeminal nucleus (PBG) in the midbrain, and the nucleus of the optic tract (NOT) in the pretectum of marmosets. Marmosets are New World diurnal foveate monkeys, and are an increasingly popular model for studying the primate visual system. Furthermore, the koniocellular geniculate layers in marmosets, unlike those in the geniculate of commonly studied diurnal Old World monkeys, are well differentiated from the parvocellular and magnocellular layers. Thus, in the present study, we have made small iontophoretic injections of the retrograde tracer microruby, targeted to the koniocellular layers in the geniculates of four marmosets. We found direct projections from the ipsilateral SC, PBG, and NOT to the koniocellular geniculate layers. The distribution of retrogradely labeled cells in the superficial, visual layers of SC is consistent with the idea that projections from the SC to the koniocellular layers are visuotopically organized. A little over 20 years ago, Vivien Casagrande ( 1994 ) introduced the idea that koniocellular geniculate layers (rather than the parvocellular and magnocellular layers) are principal targets of visuotopically organized subcortical nuclei. Our results add to subsequent evidence assembled by Casagrande and others in favor of this hypothesis.     

Does primate motion perception depend on the magnocellular pathway?

This study examined the importance of the primate magnocellular retinocortical pathway in the perception of moving stimuli. A portion of the magnocellular pathway was permanently and selectively interrupted by ibotenic acid injections in the LGN of macaque monkeys. We then tested contrast sensitivity for detecting moving stimuli, as well as two indices of motion perception, contrast sensitivity for opposite direction discrimination and speed difference thresholds, in the affected portion of the visual field. Magnocellular lesions greatly reduced detection contrast sensitivity at high temporal and low spatial frequencies and had a similar effect on contrast sensitivity for opposite direction discrimination under these same stimulus conditions. Consequently, opposite direction discriminations could be made at contrast threshold, suggesting that magnocellular lesions reduced the visibility of stimuli used to test direction perception, but did not act directly on direction perception. Magnocellular lesions also elevated speed difference thresholds under some stimulus conditions. However, this deficit was reduced or eliminated by raising the contrast of the test stimulus. Together, these findings suggest that magnocellular lesions reduce the visibility of stimuli used to test motion perception but that they do not appear to alter motion perception otherwise.     

Organization of individual afferent axons in layer IV of striate cortex in a primate

Evidence from a number of anatomical and physiological studies shows that information is transmitted from the retina to visual cortex via physiologically and anatomically distinct populations of neurons in the lateral geniculate nucleus (LGN). In order to gain a better understanding of the functional roles of these parallel channels from the LGN to cortex in primates, individual afferent axons to layer IV of striate cortex of galagos were filled with HRP by bulk injection into the white matter underlying striate cortex. A total of 55 axons and their terminal arbors, from zones representing both the central and peripheral visual fields, were completely reconstructed through serial sections. Based upon the sublaminar distribution and the morphology of these axons, they have been categorized into 2 groups, designated type I and II axons. Evidence from both past work and the present study suggests that type I axons represent the projections from physiologically defined Y-like cells in the magnocellular layers of the LGN, while type II axons represent the projections from X-like cells in the parvocellular LGN layers. Our results show that type I (presumed Y-like) arbors occupy relatively more cortical space within their main terminal sublayer (IV alpha) than is the case for the type II (presumed X-like) arbors which ramify primarily in layer IV beta. In addition, type I arbors have larger parent axons, fewer boutons along a restricted length of axon, and a greater tendency to branch in layer VI than type II arbors. Finally, both axon types are larger in the area of cortex representing central vision than in the area representing peripheral vision. These morphological characteristics suggest that the physiological differences between magnocellular and parvocellular geniculate cells may be amplified in cortex by differences in the organization of their terminal arbors. Further, within each afferent population, the terminal organization of axons reflects their visuotopic relationships in striate cortex. Comparison of these findings with data from cats and monkeys supports the idea that the relationship between the size of the terminal arbors of LGN X-like or parvocellular cells and the size of the cortical spatial subunit varies with differences in visual acuity across species; for LGN Y-like (or magnocellular) cells this relationship remains constant.     

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.     

Differential inhibition of chromatic and achromatic perception by transcranial magnetic stimulation of the human visual cortex.

The magnocellular visual pathway is devoted to low-contrast achromatic and motion perception whereas the parvocellular pathway deals with chromatic and high resolution spatial vision. To specifically separate perception mediated by these pathways we have used low-contrast Gaussian filtered black-white or coloured visual stimuli. By use of transcranial magnetic stimulation (TMS) over the visual cortex inhibition of magnocellular stimuli was achieved distinctly earlier by about 40 ms compared with parvocellular information. A nonspecific inhibition of all stimuli could be seen peaking at 75-90 ms, significantly higher for magnocellular stimuli. The particular vulnerability of magnocellular stimuli to TMS is correlated with distinct physiological properties of this pathway such as faster conduction velocity and non-linear stimulus encoding.     

The role of the magnocellular pathway in serial deployment of visual attention

Normal human visual function often demands detection of a target among a number of other objects cluttering the scene, such as when searching for a known face in a crowd. In these and similar tasks, the search performed is a serial one, with an attentional spotlight scanning the objects of the scene. We have investigated whether one of the afferent channels in vision, the colour-blind magnocellular pathway, is essential in such serial searches. We did this by using items that were isoluminant with the background but of a different colour, for which the magnocellular cells would be blind. The search in these conditions required much longer reaction times than when even a very small luminance contrast (2%) was added to the items. Because such luminance contrasts can be detected only by magnocellular cells and not by neurons of the other channels (parvocellular and koniocellular), the magnocellular pathway appears vitally important for serial search. In contrast, in a feature search task, which does not require allocation of attentional resources, the search was as efficient with isoluminance as when luminance contrast was added to the items.     

Behavioural and electrophysiological chromatic and achromatic contrast sensitivity in an achromatopsic patient.

OBJECTIVES--In cases of incomplete achromatopsia it is unclear whether residual visual function is mediated by intact striate cortex or results from incomplete lesions to extrastriate cortical visual areas. A patient with complete cerebral achromatopsia was tested to establish the nature of his residual vision and to determine the integrity of striate cortex function. METHODS--Behavioural contrast sensitivity, using the method of adjustment, and averaged visually evoked cortical potentials were measured to sinusoidally modulated chromatic and achromatic gratings in an achromatopsic patient and a normal observer. Eye movements were measured in the patient using a Skalar infrared monitoring system. RESULTS--The patient's chromatic contrast sensitivity was normal, indicating that despite his dense colour blindness his occipital cortex still processed information about spatial variations in hue. His sensitivity to achromatic gratings was depressed particularly at high spatial frequencies, possibly because of his jerk nystagmus. These behavioural results were reinforced by the nature of visually evoked responses to chromatic and achromatic gratings, in which total colour blindness coexisted with an almost normal cortical potential to isoluminant chromatic gratings. CONCLUSIONS--The results show that information about chromatic contrast is present in some cortical areas, and coded in a colour-opponent fashion, in the absence of any perceptual experience of colour.     

The contribution of color to motion processing in Macaque middle temporal area.

The chromatic properties of an image yield strong cues for object boundaries and thus hold the potential to facilitate the detection of object motion. The extent to which cortical motion detectors exploit chromatic information, however, remains a matter of debate. To address this further, we quantified the strength of chromatic input to directionally selective neurons in the middle temporal area (MT) of macaque cerebral cortex using an equivalent luminance contrast (EqLC) paradigm. This paradigm, in which two sinusoidal gratings, one heterochromatic and the other achromatic, are superimposed and moved in opposite directions, allows the sensitivity of motion detectors to heterochromatic stimuli to be quantified and expressed relative to the benchmark of sensitivity for a luminance-defined stimulus. The results of these experiments demonstrate that the chromatic contrast in a moving red-green heterochromatic grating strongly influences directional responses in MT when the luminance contrast in that same grating is relatively low; for such stimuli, EqLC is at least 5%. When luminance contrast is added to the heterochromatic grating, however, EqLC wanes sharply and becomes negative (-4%) when luminance contrast is sufficiently high (>17-23%). Thus, the chromatic properties of an object appear to confer little or no benefit to motion processing by MT neurons when sufficient luminance contrast concurrently exists. These data support a simple model in which chromatic motion processing in MT is almost exclusively determined by magnocellular input. Additionally, a comparison of neuronal and psychophysical data suggests that MT may not be the sole contributor to the perceptual experience elicited by motion of heterochromatic patterns, or that only a subset of MT neurons serve this function.     

Lesions of the Superior Temporal Cortical Motion Areas Impair Speed Discrimination in the Macaque Monkey

The effects of circumscribed lesions of the superior temporal cortical motion areas on speed discrimination were tested in three macaque monkeys using both moving random-textured patterns and moving bars. The lesions, which included the middle temporal visual area, the adjacent medial superior temporal visual area and the fundus superior temporal visual area, produced a severe and lasting deficit in speed discrimination when tested with the random patterns. In contrast, deficits were smaller when tested with moving bars. Control lesions of the inferior temporal cortex in two monkeys had little effect on speed discrimination. There was no clear deficit following inferior temporal or superior temporal sulcus lesions on a vernier acuity task. These experiments indicate that the middle temporal and adjacent areas play a crucial role in speed discrimination and that lesion effects depend on the cues available to the animals.     

Analysis of the lateral geniculate nucleus in dichromatic and trichromatic marmosets

Marmosets are diurnal New World monkeys that show sex‐linked cone photopigment polymorphism, whereby all males and some females are dichromats ("red‐green colorblind"), but most females show trichromatic color vision. Here we asked whether trichromats express chromatic‐specific circuitry in the lateral geniculate nucleus (LGN). The volume of parvocellular (P), magnocellular (M), and koniocellular (K) layers was calculated in Nissl‐stained sections from the LGN of adult marmosets (Callithrix jacchus; 10 trichromatic females; 2 dichromatic females; and 13 dichromatic males). Retinal ganglion cell axon terminals within the P and K layers were reconstructed and measured following anterograde tracer (dextran) injections. We show that there is little difference in LGN layer volume with respect to age, weight, or sex of the animals, or between dichromatic and trichromatic phenotypes. The morphology of retinal ganglion cell terminals was largely indistinguishable on comparing dichromats and trichromats, and likewise on comparing terminals representing peripheral or foveal retina. We conclude that the LGN circuits we studied are largely independent of red‐green color vision phenotype and visual field location. J. Comp. Neurol. 523:1948–1966, 2015 © 2015 Wiley Periodicals, Inc.     

Immunohistochemical investigations of neurofilament M' and alphabeta-crystallin in the magnocellular layers of the primate lateral geniculate nucleus

The magnocellular and parvocellular pathways are two major processing streams in the primate visual system. Using high-density grid arrayed cDNA clones to hybridize to cDNA probes from cortical regions of each pathway, a list of candidate differentially expressed genes was produced [Mol. Brain Res. 82 (2000) 11-24]. Magnocellular pathway candidates include neurofilament M' and alphabeta-crystallin. Using antibodies generated against these proteins, immunohistochemical analysis revealed preferential staining of the magnocellular layers in the primate lateral geniculate nucleus, providing verification of two candidate magnocellular-enriched genes.     

Segregation of short-wavelength-sensitive (S) cone signals in the macaque dorsal lateral geniculate nucleus

An important problem in the study of the mammalian visual system is whether functionally different retinal ganglion cell types are anatomically segregated further up along the central visual pathway. It was previously demonstrated that, in a New World diurnal monkey (marmoset), the neurones carrying signals from the short-wavelength-sensitive (S) cones [blue–yellow (B/Y)-opponent cells] are predominantly located in the koniocellular layers of the dorsal lateral geniculate nucleus (LGN), whereas the red–green (R/G)-opponent cells carrying signals from the medium- and long-wavelength-sensitive cones are segregated in the parvocellular layers. Here, we used extracellular single-unit recordings followed by histological reconstruction to investigate the distribution of color-selective cells in the LGN of the macaque, an Old World diurnal monkey. Cells were classified using cone-isolating stimuli to identify their cone inputs. Our results indicate that the majority of cells carrying signals from S-cones are located either in the koniocellular layers or in the 'koniocellular bridges' that fully or partially span the parvocellular layers. By contrast, the R/G-opponent cells are located in the parvocellular layers. We conclude that anatomical segregation of B/Y- and R/G-opponent afferent signals for color vision is common to the LGNs of New World and Old World diurnal monkeys.     

Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey

Many lines of evidence suggest that the visual signals relayed through the magnocellular and parvocellular subdivisions of the primate dorsal LGN remain largely segregated through several levels of cortical processing. It has been suggested that this segregation persists through to the highest stages of the visual cortex, and that the pronounced differences between the neuronal response properties in the parietal cortex and inferotemporal cortex may be attributed to differential contributions from magnocellular and parvocellular signals. We have examined this hypothesis directly by recording the responses of cortical neurons while selectively blocking responses in the magnocellular or parvocellular layers of the LGN. Responses were recorded from single units or multiunit clusters in the middle temporal visual area (MT), which is part of the pathway leading to parietal cortex and thought to receive primarily magnocellular inputs. Responses in the MT were consistently reduced when the magnocellular subdivision of the LGN was inactivated. The reduction was almost always pronounced and often complete. In contrast, parvocellular block rarely produced striking changes in MT responses and typically had very little effect. Nevertheless, unequivocal parvocellular contributions could be demonstrated for a minority of MT responses. At a few MT sites, responses were recorded while magnocellular and parvocellular blocks were made simultaneously. Responses were essentially eliminated for all these paired blocks. These results provide direct evidence for segregation of magnocellular and parvocellular contributions in the extrastriate visual cortex and support the suggestion that these signals remain largely segregated through the highest levels of cortical processing.