Studies in the greater galago have not provided a comprehensive description of the organization of eye-specific retino-geniculate-cortical projections to the recipient layers in V1. Here we demonstrate the overall patterns of ocular dominance domains in layers III, IV, and VI revealed following a monocular injection of the transneuronal tracer wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP). We also correlate these patterns with the array of cytochrome oxidase (CO) blobs in tangential sections through the unfolded and flattened cortex. In layer IV, we observed for the first time that eye-specific domains form an interconnected pattern of bands 200–250 μm wide arranged such that they do not show orientation bias and do not meet the V1 border at right angles, as is the case in macaques. We also observed distinct WGA-HRP labeled patches in layers III and VI. The patches in layer III, likely corresponding to patches of K lateral geniculate nucleus (LGN) input, align with layer IV ocular dominance columns (ODCs) of the same eye dominance and overlap partially with virtually all CO blobs in both hemispheres, implying that CO blobs receive K LGN input from both eyes. We further found that CO blobs straddle the border between layer IV ODCs, such that the distribution of CO staining is approximately equal over ipsilateral and contralateral ODCs. These results, together with studies showing that a high percentage of cells in CO blobs are monocular, suggest that CO blobs consist of ipsilateral and contralateral subregions that are in register with underlying layer IV ODCs of the same eye dominance. In macaques and humans, CO blobs are centered on ODCs in layer IV. Our finding that CO blobs in galago straddle the border of neighboring layer IV ODCs suggests that this novel feature may represent an alternative way by which visual information is processed by eye-specific modular architecture in mammalian V1.

Color vision in mammals is based on the expression of at least two cone opsins that are sensitive to different wavelengths of light. Furthermore, retinal pathways conveying color-opponent signals are required for color discrimination. Most of the primates are trichromats, and “color-coded channels” of their retinas are unveiled to a large extent. In contrast, knowledge of cone-selective pathways in nonprimate dichromats is only slowly emerging, although retinas of dichromats like mice or rats are extensively studied as model systems for retinal information processing. Here, we review recent progress of research on color-coded pathways in nonprimate dichromats to identify differences or similarities between di- and trichromatic mammals. In addition, we applied immunohistochemical methods and confocal microscopy to retinas of different species and present data on their neuronal properties, which are expected to contribute to color vision. Basic neuronal features such as the “blue cone bipolar cell” exist in every species investigated so far. Moreover, there is increasing evidence for chromatic OFF channels in dichromats and retinal ganglion cells that relay color-opponent signals to the brain. In conclusion, di- and trichromats share similar retinal pathways for color transmission and processing.

The functions of the primate color-opponent and broad-band channels were assessed by examining the visual capacities of rhesus monkeys following selective lesions of parvocellular and magnocellular lateral geniculate nucleus, which respectively relay these two channels to the cortex. Parvocellular lesions impaired color vision, high spatial-frequency form vision, and fine stereopsis. Magnocellular lesions impaired high temporal- frequency flicker and motion perception but produced no deficits in stereopsis. Low spatial-frequency form vision, stereopsis, and brightness perception were unaffected by either lesion. Much as the rods and cones of the retina can be thought of as extending the range of vision in the intensity domain, we propose that the color-opponent channel extends visual capacities in the wavelength and spatial-frequency domains whereas the broad-band channel extends them in the temporal domain.

The lateral geniculate nucleus (LGN) of every primate examined contains a set of small relay cells in addition to separate sets of magnocellular and parvocellular relay cells. These small cells receive a direct retinal projection, and an indirect retinal projection via the superior colliculus (SC). Receptive-field analyses of the small LGN cells in the bush baby, a lorisiform primate, indicate that this cell class is composed of subclasses, similar in physiology to cat W cells. In an effort to identify some of these subclasses, we have examined the morphological features of retinal and collicular axonal arbors that end on small W-like cells in the LGN of the bush baby, Galago crassicaudatus. Small cells in this species are found in a prominent pair of koniocellular (K) layers as well as the interlaminar zones (ILZs).

Retinal arbors were examined by bulk iontophoretic injection of horseradish peroxidase into the optic tract. Collicular arbors were filled via iontophoretic injection of biocytin into the superficial layers of the SC. Forty-eight axon arbors were completely reconstructed and quantitatively evaluated. Our findings show that retinal and collicular axon terminals differ in morphology on the basis of a number of criteria. Our analyses also suggest that retinal axons may have a stronger influence on K cells and collicular axons have a stronger influence on ILZ cells. The ramifications of these findings are provocative since these small LGN cells are known to project directly to the cytochrome-oxidase (CO) blobs within striate cortex. This relationship suggests that CO blob cells receive complex visual input not only from magnocellular and parvocellular LGN cells, but also from small cell pathways that are differentially influenced by retinal and collicular cells.

Visually evoked field potentials in human subjects and single-cell responses from retinal ganglion cells in the macaque monkey were compared in closely similar stimulus situations. The classical heterochromatic flicker photometry (HFP) technique was used to measure spectral sensitivity in man, both psychophysically and by recording the 40-Hz response, and to measure the spectral sensitivity of magnocellular (MC-) pathway cells of the macaque. The three measures gave closely similar spectral-sensitivity curves. Close agreement between the three measures was also found when the variable-modulation HFP technique was used to measure spectral sensitivity. When the relative phase between red and green lights was varied, the point of minimum subjective flicker for human observers was close to a sharp minimum found in the amplitude of the 40-Hz response in human and was also close to a minimum in the response of MC-pathway neurons in the monkey. The human 40-Hz response saturated at between 10 and 30% modulation depth, and so did the response of MC-pathway cells in the monkey.

The 16-Hz response in human showed none of the above correlations with MC-pathway properties. On the other hand, parvocellular (PC-) pathway cells responded vigorously to constant-luminance, chromatic modulation, at frequencies higher than can be detected by human observers. The human 16-Hz response also was strong in that stimulus situation. In addition, the response of PC-pathway cells on increasing modulation depth showed little saturation, and this behaviour was paralleled by the human 16-Hz response.

We conclude that the properties of MC-pathway neurons in macaque are closely similar to the properties of the human 40-Hz response in the respects just described. We suggest that the 40-Hz response may offer a means of objectively isolating and investigating the contribution of the magnocellular stream to cortical activity in human. In contrast, the properties of PC-pathway neurons in macaque are quite different from the properties of the human 40-Hz response, and in several respects resemble the properties of the human 16-Hz response.

An important issue in understanding the function of primary visual cortex in the macaque monkey is how the several efferent neuron groups projecting to extrastriate cortex acquire their different response properties. To assist our understanding of this issue, we have compared the anatomical distribution of VI intrinsic relays that carry information derived from magno- (M) and parvocellular (P) divisions of the dorsal lateral geniculate nucleus between thalamic recipient neurons and interareal efferent neuron groups within area VI. We used small, iontophoretic injections of biocytin placed in individual cortical laminae of area VI to trace orthograde and retrograde inter- and intralaminar projections. In either the same or adjacent sections, the tissue was reacted for cytochrome oxidase (CO), which provides important landmarks for different efferent neuron populations located in CO rich blobs and CO poor interblobs in laminae ⅔, as well as defining clear boundaries for the populations of efferent neurons in laminae 4A and 4B. This study shows that the interblobs, but not the blobs, receive direct input from thalamic recipient 4C neurons; the interblobs receive relays from mid 4C neurons (believed to receive convergent M and P inputs), while blobs receive indirect inputs from either M or P (or both) pathways through layers 4B (which receives M relays from layer 4Cα) and 4A (which receives P relays directly from the thalamus as well as from layer 4Cβ). The property of orientation selectivity, most prominent in the interblob regions and in layer 4B, may have a common origin from oriented lateral projections made by mid 4C spiny stellate neurons. While layer 4B efferents may emphasize M characteristics and layer 4A efferents emphasize P characteristics, the dendrites of their constituent pyramidal neurons may provide anatomical access to the other channel since both blob and interblob regions in layers ⅔ have anatomical access to M and P driven relays, despite functional differences in the way these properties may be expressed in the two compartments.

Four indices of visual performance were measured in control macaques and in macaques that had been exposed to monomeric acrylamide, a neurotoxicant that preferentially damages P retinal ganglion cells. Morphological examination of the retina and visual pathways of these monkeys showed virtually complete loss of P ganglion cells over a region extending to at least 40 deg from the fovea, and relative sparing of M ganglion cells. The four tests examined visual functions for which the visual pathway from P ganglion cells might be of great importance: visual acuity, contrast discrimination, hyperacuity, and shape discrimination.

In the acrylamide-dosed monkeys, visual acuity was reduced slightly more than fourfold, a somewhat larger reduction than that seen previously after ibotenic-acid lesions of the P pathway in the geniculate. The residual acuity was in good agreement with the Nyquist frequency calculated from the density of ON or OFF M ganglion cells. Contrast increment thresholds were elevated for the dosed monkeys only in one of the two conditions tested. The elevation was found only under those spatiotemporal conditions for which we have previously shown that contrast thresholds are increased by acrylamide exposure, and was most marked at low background contrasts. Vernier acuity was elevated in one dosed monkey, but not affected in a second monkey that also had severe loss of P ganglion cells. Finally, we found no effect of acrylamide exposure on the number of training trials required to learn simple or complex shape discriminations. These results support previous findings in showing that the P pathway mediates visual acuity, and they show that several other important aspects of visual perception are not exclusively dependent on the P pathway.

The effects of V4, MT, and combined V4+MT lesions were assessed on a broad range of visual capacities that included measures of contrast sensitivity, wavelength and brightness discrimination, form vision, pattern vision, motion and flicker perception, stereopsis, and the selection of stimuli that were less prominent than those with which they appeared in stimulus arrays. The major deficit observed was a loss in the ability, after V4 lesions, to select such less prominent stimuli; this was the case irrespective of the manner in which the stimulus arrays were made visible, using either luminance, chrominance, motion, or stereoscopic depth as surface media. In addition, V4 lesions yielded mild deficits in color, brightness, and form vision whereas MT lesions yielded mild to moderate deficits in motion and flicker perception. Both lesions produced mild deficits in contrast sensitivity, shape-from-motion perception, and yielded increased reaction times on many of the tasks. The impairment resulting from combined V4 and MT lesions was not greater than the sum of the deficits of either lesion. None of the lesions produced significant deficits in stereopsis. The findings suggest that (1) area V4 is part of a neural system that is involved in extracting stimuli from the visual scene that elicit less neural activity early in the visual system than do other stimuli with which they appear and (2) several other extrastriate regions and more than just two major cortical processing streams contribute to the processing of basic visual functions in the extrastriate cortex.

The main objective of the present study was to describe the postnatal development of magnocellular and parvocellular LGN axons within the primate striate cortex. For this purpose, we bulk labeled axons in neonatal prosimians (galagos) in vivo or in vitro at regular intervals from birth (PO) to 12 weeks after birth by injecting horseradish peroxidase (HRP) into white matter anterior to the striate cortex. Filled axons within layer IV were reconstructed, quantitatively analyzed, and compared to a population of adult axons described previously (Florence & Casagrande, 1987).

Our results show that although axons are morphologically immature at birth, they are restricted to the upper (IVα) and lower (IVβ) tiers of layer IV of the striate cortex as in adults. In adults, we referred to the presumed magnocellular LGN axons terminating in IVα as type I and the presumed parvocellular axons terminating in IVβ as type II. We used the same convention for developing axons.

From birth to 3 weeks postnatal, type I and II axon classes are more variable in appearance than adult counterparts, and are not morphologically class distinct. As axons mature, parent axon shafts increase in caliber, arbors become smaller and more radial, and other immature features (e.g. spikes, protrusions, growth cones) are less evident. Both arbor classes mature slowly and some still exhibit immature features (e.g. growth cones) as late as 12 weeks postnatally. Although arbors do not show class-distinctive features until late in development, each class does show some unique maturational trends. Type I arbors are only slightly larger than adult counterparts at birth, whereas type II arbors are dramatically larger. Type I arbors increase in branch complexity with age, whereas type II arbors simply show a shift in complexity toward the center of the arbor with decreasing size over time. These growth trends suggest that magnocellular and parvocellular pathways to cortex could be differentially vulnerable to the manipulation of postnatal visual experience.

As in other primates, the lateral geniculate nucleus (LGN) of the prosimian primate, bush baby (Galago crassicaudatus), contains three morphologically and physiologically distinct cell classes [magnocellular (M), parvocellular (P), and koniocellular (K)] (Norton & Casagrande, 1982; Casagrande & Norton, 1991). The present study examined quantitatively the center/surround relationships of cells in all three classes. Estimates of receptive-field center size (Rc) and sensitivity (Kc) and of surround size (Rs) and sensitivity (Ks) were obtained from 47 LGN relay cells by fitting a difference of Gaussians function to contrast-sensitivity data. For M and P cells, center size (Rc) increases with eccentricity but is about two times larger for M than for P cells at a given eccentricity. Surround size (Rs) increases with eccentricity for P but not for M or K cells. The center sensitivity (Kc) is inversely related to center size (Rc) and surround sensitivity (Ks) is inversely related to surround size (Rs) for cells in all classes, a result consistent with the sensitivity regulation that is produced by light adaptation. High spatial-frequency cutoff (acuity) is inversely related to center size (Rc). However, the peak contrast sensitivity is relatively independent of Rc. The ratio of the integrated strength (volume) of the surround to the volume of the center remains relatively constant (median, 0.87) across all three cell classes. This ratio is an excellent predictor of a cell’s rolloff in contrast sensitivity at low spatial frequencies: cells with a low surround/center ratio have less low-frequency rolloff. Although M, P, and K cells generally display similar center/surround relationships, differences in center size and the other parameters between the classes distinguish most M, P, and K cells. These findings demonstrate that both similarities and differences in the visual-response properties of primate LGN cells in these three parallel afferent pathways can be explained by basic center/surround relationships.

We examined the laminar distribution of corticogeniculate neurons in the macaque striate cortex labeled by axonal transport following injections of retrograde tracers into the lateral geniculate nucleus (LGN). Large injections of retrograde tracers involving all layers of the LGN resulted in a distinctive bilaminar distribution of labeled cells in cortical layer 6. One tier of labeled neurons was located along the layer 5–6 border and a second was located near the bottom of the layer, leaving the middle of layer 6 largely free of labeled neurons. Following injections of tracers that were restricted to the magnocellular layers of the LGN, almost all of the labeled neurons were located in the lower tier. In contrast, following injections of retrograde tracers confined to the parvocellular layers of the LGN, labeled cells were found in both tiers, with the greatest number in the upper tier. Thus, layer 6 of macaque striate cortex consists of three distinct sublayers only two of which are the source of descending projections to the LGN: an upper tier that projects exclusively to the parvocellular layers and a lower tier that projects to both magnocellular and parvocellular layers.

Behavioral and electrophysiological studies of insects demonstrate both spectrally independent and chromatically dependent behaviors and interneurons. This account describes the neuroanatomical identification of two parallel retinotopic subsystems, one supplying descending channels to spectrally independent neck and flight motor circuits, the other supplying polychromatic channels to neuropils associated with leg motor circuits in the thoracic ganglia. In the compound eye, two classes of photoreceptors contribute to each of several thousand sampling units. High-sensitivity, chromatically uniform short-axon photoreceptors (R1-R6) supply the lamina's external plexiform layer and are presynaptic to L1, L2 efferents. These project in parallel with a second system of trichromatic long-axon receptors and the L3 efferent. Both pathways supply columns of the medulla, equal in number to ommatidia. Golgi and cobalt-silver impregnation demonstrates that neurons from the medulla diverge to two deeper regions, the lobula plate and lobula, the former a thin tectum of neuropil dorsal to the more substantial lobula. Layer relationships between medulla neurons and their afferent supply suggest that the lobula plate and lobula are each supplied by one or the other, but not both, of the two parallel subsystems. Independence of the two parallel pathways is suggested by ablation of the photoreceptor layer leading to selective degeneration of the motion-sensitive lobula plate neuropil. In addition, octets of small-field neurons associated with the R1-R6/L1, L2 pathway give rise to synaptic complexes with motion-sensitive neurons of the lobula plate. A variety of behavioral and electrophysiological studies provide supporting evidence that certain insects possess parallel visual pathways comparable to the magnocellular and parvocellular subsystems of primates.

This study examined the consequences of visual system lesions on visual aftereffects produced by achromatic stimuli of various luminance contrasts and chromatic stimuli of various wavelength compositions. The effects of repeated exposure to such adapting stimuli were assessed using probes whose luminance contrast and wavelength composition were systematically varied using both detection and discrimination paradigms. Interocular tests revealed that both peripheral and central mechanisms contribute to the visual aftereffects produced by the adapting stimulus arrays used in this study. Contrary to the hypothesis according to which the midget system of the retina is the conveyor of visual afterimages, we found that blocking this system with lesions of parvocellular lateral geniculate nucleus, through which the midget cells make their way to the striate cortex in primates, did not eliminate the visual aftereffects. It appears therefore that the parasol system of the retina, which courses through the magnocellular layers of the lateral geniculate nucleus to cortex, can convey the necessary signals for the generation of visual aftereffects. Lesions of areas V4 and MT did not have significant effects on the visual aftereffects studied suggesting that the central factors that contribute to the visual aftereffects occur either already in area VI or are conveyed to higher centers through regions other than areas V4 and MT.

Previous studies report that background luminance flicker, which is asynchronous with signal averaging, reduces the amplitude and increases the latency of the pattern-onset visual evoked potential (VEP). This effect has been attributed to saturation of the magnocellular (m-) pathway by the flicker stimulus. In the current study, we evaluate this hypothesis and further characterize this effect. We found that flicker had similar effects on the pattern-onset and pattern-reversal VEP, suggesting that the reversal and onset responses have similar generators. Chromatic flicker decreased latency of the chromatic VEP whereas luminance flicker increased peak latency to luminance targets. This result indicates that luminance flicker saturates a rapidly conducting m-pathway whereas chromatic flicker saturates a more slowly conducting parvocellular (p-) pathway. Finally, evoked potentials to chromatic and luminance stimuli were recorded from 34 electrodes over the scalp in the presence of static and asynchronously modulated backgrounds. An equivalent dipole model was used to assess occipital, parietal, and temporal lobe components of the surface response topography. Results showed that chromatic flicker reduced activity to a greater extent in the ventral visual pathway whereas luminance flicker reduced activity to a greater extent in the dorsal visual pathway to parietal lobe. We conclude that the VEP to isoluminant color and luminance stimuli contains both m- and p-pathway components. Asynchronous flicker can be used to selectively reduce the contribution of these pathways to the surface recorded VEP. Our results provide evidence of parallel pathways in the human visual system, with a dorsal luminance channel projecting predominantly to the posterior parietal lobe and a ventral color channel projecting predominantly to inferior temporal lobe.

Psychophysical studies have documented that many observers show lower thresholds for rapid-off than for rapid-on sawtooth luminance modulation. This finding, together with physiological findings from chromatically opponent ganglion cells of the macaque monkey, prompted a search for a similar bias in psychophysical detection of chromatic increments and decrements of light. Using a luminance pedestal in conjunction with a luminance background to favor detection by chromatic mechanisms, we measured spectral sensitivity for rapid-on and rapid-off sawtooth stimuli presented spatially coextensive with the pedestal. There were two different pedestal chromaticities: one broadband, and the second composed only of long-wavelength light to enhance short-wavelength-sensitive, cone-mediated detection. Spectral-sensitivity measurements for different wavelength stimuli revealed no systematic differences across the visible spectrum as a function of sawtooth waveform polarity or pedestal chromaticity. Similarly, temporal contrast-sensitivity functions for hetero-chromatically modulated red-green sawtooth stimuli did not reveal an asymmetry in sensitivity for rapid-red and rapid-green chromatic change. Some of the observers showed a higher sensitivity for luminance modulated rapid-off sawtooth stimuli, as also noted in previous studies. This asymmetry was not found when a white luminance pedestal and background was used. These results suggest that the cone inputs to chromatically opponent ON- and OFF-center cells are sufficiently balanced to provide equivalent psychophysical thresholds for chromatic increments and decrements of light.

The lateral geniculate nucleus (LGN) of primates contains three classes of relay cells, the magnocellular (M), parvocellular (P), and koniocellular (K) cells. At present, very little is known about either the structure or function of the K relay cells in New or Old World monkeys (simian primates). In monkeys, K cells are located between the main LGN layers and adjacent to the optic tract. For convenience, these intercalated cell layers are numbered K1-K4 starting closest to the optic tract with K1. The objective of this study was to examine the details of K axon morphology in the primary visual cortex (V1) of owl monkeys and to determine if different K layers give rise to distinct axon types. For this purpose, injections of WGA-HRP or PHA-L were made into specific K LGN layers and the distribution and morphology of the resulting labeled axons were analyzed. Injections of fluorescent tracers also were made within the superficial layers of V1 to further document connections via analysis of the patterns of retrogradely labeled cells in the LGN. Our main finding is that K axons in owl monkeys terminate as delicate focused arbors within single cytochrome oxidase (CO) blob columns in cortical layer III and within cortical layer I. Overall, the morphology of the K axons in these monkeys is quite similar to what we described previously for K geniculocortical axons in the distantly related bush baby (prosimian primate), suggesting that the basic features of this pathway are common to all primates. Our results also provide evidence that the axon arbors from different K layers are morphologically distinct; axons from LGN layer K1 project mainly to cortical layer I, while axons from LGN layer K3 chiefly terminate in cortical layer III. Taken together, these results imply that the basic features of axons within the K pathway are conserved across primates, and that the K axons from different K layers are likely to differ in function based upon their different morphologies.

Ibotenic-acid lesions of the magnocelluar portion of the macaque lateral geniculate nucleus were used to examine the role of the M-cell pathway in spatio-temporal contrast sensitivity. A lesion was place in layer 1 of the lateral geniculate of each of two monkeys. Physiological mapping in one animal demonstrated that the visual-field locus of the lesion was on the horizontal meridian, approximately 6 deg in the temporal field. Visual thresholds were tested monocularly in the contralateral eye, and fixation locus was monitored with a scleral search coil to control the retinal location of the test target.

Three threshold measures were clearly disrupted by the magnocellular lesions. Contrast sensitivity for a 1 cycle/deg grating that drifted at 10 Hz was reduced from about twofold greater than, to about the same as, that for 10-Hz counterphase modulated gratings. Sensitivity for a very low spatial frequency (Gaussian blob), 10-Hz flickering stimulus was reduced so severely that no threshold could be measured. In addition, flicker resolution was greatly reduced at lower modulation depths (0.22), but not at higher depths (1.0). Two of the measured thresholds were unaffected by the lesions. Contrast sensitivity for 2 cycle/deg stationary gratings remained intact, and little or no effect on sensitivity was found for 1 cycle/deg, 10-Hz counterphase modulated gratings.

Together, these results suggest that the magnocellular pathway makes little contribution to visual sensitivity at low to moderate temporal frequencies. On the other hand, some contribution to detection sensitivity is evident at lower spatial and high temporal frequencies, especially for drifting stimuli. It appears that a major role of the magnocellular pathway may be to provide input to cortical mechanisms sensitive to rapid visual motion.

While much attention has been given to the correlation between cytochrome-oxidase (CO) compartments and patterns of cortico-cortical projections originating from supragranular layers in the striate cortex, little is known in this regard about patterns of cortico-subcortical projections originating from infragranular cortex. We studied the tangential distribution of the striate cortex neurons projecting to the superior colliculus and used two approaches to analyze the relationship of this distribution to the arrangement of CO “blobs.” First, chi-square analysis indicated that significantly fewer labeled neurons were found within the CO blob compartment than the number expected for a random distribution. Second, spatial cross-correlation analysis – which circumvents the inherent subjectivity of delineating blob boundaries – revealed an area around blob centers in which there was a decreased probability of encountering labeled cells. The size of this area compared well with that of our outlines of CO blobs. We conclude that corticotectal projection neurons in the striate cortex are distributed preferentially within the interblob compartment of the infragranular striate cortex. These results demonstrate that the spatial distribution of cortico-subcortical projection neurons within infragranular cortex can correlate with the CO architecture of the primary visual cortex.