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The magnocellular (MC) pathway in the primate has much higher achromatic contrast sensitivity than the parvocellular (PC) pathway, and is implicated in luminance contrast detection. But MC pathway responses tend to saturate at lower achromatic contrast than do PC pathway responses. It has been proposed that the PC pathway plays a major role in discriminating suprathreshold achromatic contrast, because the MC pathway is in saturation. This has been termed the pulsed-pedestal protocol. To test this hypothesis, responses of MC and PC pathway ganglion cells have been examined under suprathreshold conditions with stimulus configurations similar to those in psychophysical tests. For MC cells, response saturation was much less for flashed or moving edges than for sinusoidal modulation, and MC cell thresholds predicted for these stimuli were similar to psychophysical discrimination (and detection) data. Results suggest the protocol is not effective in segregating MC and PC function.

The physiology and anatomy of the primate visual pathway are reviewed from a historical perspective, especially in relation to color vision. From the work of the last decades, certain issues have been selected which remain unresolved and still pose a challenge for neurobiologists and psychophysicists. It is suggested that the structure of the primate visual pathway has been colored by the evolution of trichromacy and that many features of the parvocellular pathway represent adaptations to this end.

We review here the distribution of S-cone signals and properties of S-cone recipient receptive fields in subcortical pathways. Nearly everything we know about S-cone signals in the subcortical visual system comes from the study of visual systems in cats and primates (monkeys); in this review, we concentrate on results from macaque and marmoset monkeys. We discuss segregation of S-cone recipient (blue-on and blue-off) receptive fields in the dorsal lateral geniculate nucleus and describe their receptive field properties. We treat in some detail the question of detecting weak S-cone signals as an introduction for newcomers to the field. Finally, we briefly consider the question on how S-cone signals are distributed among nongeniculate targets.

Comparisons of S- or prepotential activity, thought to derive from a retinal ganglion cell afferent, with the activity of relay cells of the lateral geniculate nucleus (LGN) have sometimes implied a loss, or leak, of visual information. The idea of the "leaky" relay cell is reconsidered in the present analysis of prepotential firing and LGN responses of color-opponent cells of the macaque LGN to stimuli varying in size, relative luminance, and spectral distribution. Above a threshold prepotential spike frequency, called the signal transfer threshold (STT), there is a range of more than 2 log units of test field luminance that has a 1:1 relationship between prepotential- and LGN-cell firing rates. Consequently, above this threshold, the LGN cell response can be viewed as an extension of prepotential firing (a "nonleaky relay cell"). The STT level decreased when the size of the stimulus increased beyond the classical receptive field center, indicating that the LGN cell is influenced by factors other than the prepotential input. For opponent ON cells, both the excitatory and the inhibitory response decreased similarly when the test field size increased beyond the center of the receptive field. These findings have consequences for the modeling of LGN cell responses and transmission of visual information, particularly for small fields. For instance, for LGN ON cells, information in the prepotential intensity-response curve for firing rates below the STT is left to be discriminated by OFF cells. Consequently, for a given light adaptation, the STT improves the separation of the response range of retinal ganglion cells into "complementary" ON and OFF pathways.

The main cell systems of the retina that provide input to the striate cortex are now well described, although certain aspects of their anatomy and physiology remain contentious. Under simple stimulus conditions and in a threshold context psychophysical performance can often be assigned to one or other of these systems, and an identification of psychophysical channels with afferent pathways is justifiable. However, results from psychophysical studies using more complex stimulus conditions are more difficult to relate to 'front end' channels, and it is more difficult to separate the physiological contributions of afferent pathways from those of cortical mechanisms, in particular the separation of dorsal and ventral streams.

Segregation of chromatic and luminance signals in afferent pathways are investigated with a grating stimulus containing luminance and chromatic components of different spatial frequencies. Ganglion cell recordings were obtained from the retinae of macaques (Macaca fascicularis). Cell responses to the 'compound' gratings were compared to responses to standard chromatic and luminance gratings. Parvocellular (PC) pathway cell responses to compound and chromatic gratings were very similar, as were magnocellular (MC) cell responses to compound and luminance gratings. This was the case over a broad range of spatial and temporal frequencies and contrasts. In psychophysical experiments with human observers, discrimination between grating types was possible close to detection threshold. These results are consistent with chromatic and luminance structure in complex patterns being strictly localized in different afferent pathways. This novel stimulus may prove useful in identifying afferent inputs to cortical neurons.

Parasol ganglion cells of the magnocellular (MC) pathway form the physiological substrate of a luminance channel underlying photometric tasks, but they also respond weakly to red-green chromatic modulation. This may take the form of a first-harmonic (1F) response to chromatic modulation at low temporal frequencies, and/or a second-harmonic (2F) response that is more marked at higher frequencies. It is shown here that both these responses originate from a receptive field component that is intermediate in size between center and surround, i.e., a discrete, chromatic receptive field is superimposed upon an achromatic center-surround structure. Its size is similar to the receptive field (center plus surround) of midget, parvocellular cells from the same retinal eccentricity. A 2F MC cell chromatic response component is shown to be present under cone silent substitution conditions, when only the middle- (M) or long-wavelength (L) cone is modulated. This and other features suggest it is a rectified response to a chromatic signal rather than a consequence of non-linear summation of M- and L-cone signals. A scheme is presented which could give rise to such responses. It is suggested that this chromatic input to MC cells can enhance motion signals to red-green borders close to equiluminance.

This analysis assesses sensitivity of primate ganglion cells to sinusoidal modulation as a function of temporal frequency, based on the structure of their impulse trains; sensitivity to luminance and chromatic modulation was compared to human psychophysical sensitivity to similar stimuli. Each stimulus cycle was Fourier analyzed, and response amplitudes subjected to neurometric analysis; this assumes a detector with duration inversely proportional to frequency, that is, the stimulus epoch analyzed is a single cycle rather than a fixed duration, and provides an upper bound for a detection by an observer who bases judgments on a single cell. Signal-to-noise ratio for a given Fourier amplitude rapidly decreased with temporal frequency. This is a consequence of the statistics of impulse trains making up the response; at higher temporal frequencies, there are fewer impulses per cycle. Performance of this "single-cell" observer was then compared with that of modeled central detection mechanisms of fixed duration. For chromatic modulation, a filter/detector with a time constant of approximately 40 ms operating upon the parvocellular (PC) pathway provided a match to psychophysical results, whereas for luminance modulation, a filter/detection mechanism operating upon the magnocellular (MC) pathway with a time constant of approximately 5-10 ms provided a suitable match. The effects of summation and nonlinear interactions between cell inputs to detection are also considered in terms of enhanced sensitivity and "sharpness" of thresholds, that is, the steepness of the neurometric function. For both luminance (MC cells) and chromatic modulation (PC cells), restricted convergence (<20 cells) appears adequate to provide sharp thresholds and sensitivity comparable to psychophysical performance.

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

We recently developed a new technique to measure cone inputs to visual neurons and used this technique to seek short-wavelength-sensitive (S) cone inputs to parasol, magnocellular (MC) and midget, parvocellular (PC) ganglion cells. Here, we compare our physiological measurements of S-cone weights to those predicted by a random wiring model that assumes cells' receptive fields receive input from mixed cone types. The random wiring model predicts the average weights of S-cone input to be similar to the total percentage of S-cones but with considerable scatter, and the S-cone input polarity to be consistent with that of PC cells' surround and of MC cells' center. This is not consistent with our physiological measurements. We suggest that the ganglion cells' receptive fields may have a mechanism to avoid S-cone inputs, as is the case in the H1 horizontal cells. Previous reports of S-cone inputs, in particular substantial input to MC cells, are likely to reflect variation in prereceptoral filtering and/or the failure to correct for variation in macular pigment.

The specificity of cone inputs to ganglion cells has implications for the development of retinal connections and the nature of information transmitted to higher areas of the brain. We introduce a rapid and precise method for measuring signs and magnitudes of cone inputs to visual neurons. Colors of stimuli are modulated around circumferences of three color planes in clockwise and counterclockwise directions. For each neuron, the projection of the preferred vector in each plane was estimated by averaging the response phases to clockwise and counterclockwise modulation. The signs and weights of cone inputs were derived directly from the preferred vectors. The efficiency of the method enables us to measure cone inputs at different temporal frequencies and short-wavelength-sensitive (S) cone adaptation levels. The results show that S-cone inputs to the parvocellular and magnocellular ganglion cells are negligible, which implies underlying connectional specificity in the retinal circuitry.

Retinal adaptation mechanisms are considered relative to the Westheimer paradigm. Responses to a probe presented upon pedestals were obtained from macaque ganglion cells. On-center magnocellular (MC) cell responses decreased to a plateau as pedestal diameter increased, consistent with operation of a local adaptation pool. Off-center cells also demonstrated a vigorous response with small pedestals, but as pedestal size increased, responsivity decreased and then partially recovered as pedestals encroached upon the surround. The response trough was due to a profound suppression of maintained activity. Comparison with psychophysical data suggests a multiple physiological substrate for the Westheimer paradigm, involving an interaction between adaptation pools, changes in maintained firing due to center-surround mechanisms and a cortical component.

The description of colour pathways in the primate retina has become clearer within the past decade. This review summarises current views on the pathways subserving colour vision in the primate retina, beginning in the receptors and outer retina and leading to the mechanisms in the inner retina that add and subtract the receptor signals. Although the main features of colour pathways are now well-defined, there remains uncertainty about some of the wiring details. In particular, the question of how much connectional specificity is present is unresolved. Finally, means of isolating these pathways by psychophysical tests are considered; some current tests are likely to be less specific than hoped.

Two parallel visual systems, the magnocellular (M) and parvocellular (P) pathways, originate from different types of retinal ganglion cells, and are known to be segregated in different portions of the pregeniculate visual pathways. Their relative contribution to two main cortical streams, dorsal and ventral, is still under discussion, but it is reasonable to suppose that selective damage to the M or P subcortical system might interfere with specific aspects of processing within one or the other cortical system. Using two different apparent-motion tasks, we compared the performance of patients affected by compression of the ventral part of the pregeniculate visual pathways with that of normal controls. In the first task, observers detected small displacements of a low-contrast vertical bar, while in the second task they estimated the visible persistence of moving dots. In the first task, patients were impaired with parafoveal displays, especially in the temporal portion of the visual field. In the second task, patients showed reduced suppression of visible persistence at long, but not at short, exposure durations. Three considerations support the hypothesis that these results represent a selective impairment of the M system. First, M axons are more likely to suffer from compression, particularly in the case of a mass growing from below since they are known to occupy a ventral subpial position in the optic chiasm and tract. Second, the performance of patients with a ventral compression is consistent with the characteristics of the response properties of P ganglion cells, which have previously been shown to exhibit elevated and unmodulated thresholds for displacement detection in the macaque monkey. Third, such patients are less sensitive to the inhibitory signals that suppress visible persistence, which probably originate in the M system.

We have studied the morphology and physiology of retinal ganglion cells of a short-wavelength-sensitive cone (SWS-cone) pathway in dichromatic and trichromatic New World anthropoids, the capuchin monkey (Cebus apella) and tufted-ear marmoset (Callithrix jacchus). In Old World anthropoids, in which males and females are both trichromats, blue-ON/yellow-OFF retinal ganglion cells have excitatory SWS-cone and inhibitory middle- and long-wavelength-sensitive (MWS- and LWS-) cone inputs, and have been anatomically identified as small-field bistratified ganglion cells (SB-cells) (Dacey & Lee, 1994). Among retinal ganglion cells of New World monkeys, we find SB-cells which have very similar morphology to such cells in macaque and human; for example, the inner dendritic tree is larger and denser than the outer dendritic tree. We also find blue-on retinal ganglion cells of the capuchin to have physiological responses strongly resembling such cells of the macaque monkey retina; for example, responses were more sustained, with a gentler low frequency roll-off than MC-cells, and no evidence of contrast gain control. There was no difference between dichromatic and trichromatic individuals. The results support the view that SWS-cone pathways are similarly organized in New and Old World primates, consistent with the hypothesis that these pathways form a phylogenetically ancient color system.

Old-world simians are all trichromats, but in most new-world primates there is a polymorphism; males are dichromats but most females are trichromats. In the old world simian, luminance and red-green chromatic channels defined by psychophysical experiments have as a basis parasol ganglion cells of the magnocellular (MC) pathway and midget ganglion cells of the parvocellular (PC) pathway respectively. Small bistratified ganglion cells provide a basis for a blue-yellow chromatic channel, which should probably be considered a separate entity. In both dichromatic and trichromatic new-world animals, the MC pathway and the small bistratified, blue-yellow system seem anatomically and physiologically similar to those in their old-world relatives. The midget ganglion cells of the parvocellular pathway in trichromats are anatomically and physiologically similar to the old-world pattern. In dichromatic animals, they are anatomically similar and physiologically resemble those of trichromatic animals, except for the lack of chromatic opponency. We conclude that these three systems may from a basic pattern for the visual pathway of primates. However, the results from dichromats indicate that the evolution of trichromacy may be found to be more complex than presently supposed.

Magnetic resonance imaging sensitized to activity-related changes in cerebral blood oxygenation was performed to map responses to selective stimulation of the parvo- and magnocellular visual pathways in calcarine and adjacent ventral occipital cortex of human subjects. In a repetitive stimulation protocol isoluminant chromatic or isochromatic luminance modulation was alternated with steady light of the same mean chromaticity and luminance as a reference condition. While no significant effects were observed for diffuse luminance modulation, two consistent cortical foci responded to isoluminant chromatic stimulation. A strong response was obtained in calcarine cortex at both 2 and 10 Hz, and even for selective S-cone stimulation. A second weaker color-sensitive response was seen bilaterally in the collateral sulcus. Thus, the data not only confirm color-sensitive activation in the collateral sulcus elicited in previous studies by selective cognitive tasks, but additionally demonstrate color-sensitive activation in primary visual cortex. With stimuli defined according to electrophysiological response properties of early visual processing stages, this study complements phenomenological or cognitive approaches in functional mapping of the human visual system.

Using permanently implanted electrodes in squirrel monkeys and macaques, transmission through the lateral geniculate nucleus (LGN) was assayed from the amplitude of potentials evoked in optic radiation by and electrical pulse applied to optic tract. Averaging of either individually or machine selected potentials, elicited at 0.3, 1.0, 20 or 50 HZ, in all cases showed a decrease in transmission ranging from 5-60% in the period after saccadic eye movements made ad libitum. The suppression was greater in a patterned visual environment than in diffuse illumination, which in turn was greater than that occurring following saccades in the dark. Demonstration of the effect in darkness always required data averaging and never exceeded 20%. The effect was consistently greater in the magnocellular than parvocellular component. Suppresion was often abruptly terminated and replaced by a facilitation of 5-15% about 100 msec after saccade detection. Comparable effects were observed for excitability of striate cortex tested by a stimulus pulse applied to optic radiation. In addition, sharply demarcated potentials inherently arising in LGN and striate cortex were found in association with saccades made even in total darkness. Neglecting a possible but dubious contribution from eye muscle proprioceptors, the experiments establish the existence of a centrally originating modulation of visual processing at both LGN and striate cortex in ralation to saccadic eye movement in primates. This modulation may partially underlie the phenomenon of "saccadic suppression" and hasten the acquistion of a meaningful visualsample immediately following an ocular saccade. It remains uncertain as to how it may relate to similar or greater effects accompanying changes in alertness, or to fluctuations of unknown origin occurring sometimes semirhythmically at 0.05-0.03 HZ (Fig 7).

The activity of retinal ganglion cells and cortical cells with overlapping receptive fields was simultaneously recorded. The responses to moving stimuli of individual simple cortical cells could be accounted for on the basis of the cell receiving either on-centre or off-centre afferents; instances in which it was necessary to postulate a mixed on- and off-centre input were not found. In six instances cross correlograms of ganglion cell and cortical cell activity showed that the ganglion cell was afferent, via a relay cell in the LGN, to the cortical neurone. The receptive fields of such pairs were almost completely overlapping and concentric. In three cases a sustained ganglion cell projected to a simple cortical cell. In one case a transient ganglion cell projected to a simple cell, and in one case a sustained and a transient ganglion cell projected to the same simple cell.

We have recorded from 661 single neurons in the foveal and parafoveal region of area 17 of the awake trained macaque monkey. The functional properties of 538 cells were investigated in detail, with flashed and moving stimuli of varying form and colour. Irrespective of their functional properties such determined, each neuron was also tested with a 2 X 2 degrees square of various luminance and colour. This was done in order to get an idea how such a simple stimulus is represented by the activities of neurons in area 17. Most of the neurons showed response preference for certain aspects of visual stimuli. We have distinguished the following functional groups: 1. Sustained spectrally selective neurons (21%). These cells respond with tonic discharges to light of their optimal wavelength, and their spectral selectivity corresponded to that of opponent parvocellular cells of the lateral geniculate body. 44% of these cells were excited selectively by long, 23% by middle and 33% by short wavelength light. When slowly moving the 2 X 2 degrees square of their preferred wavelength across the receptive field, discharge rate remained elevated, as long as the stimulus covered the RF and with little contour enhancement. The majority of the sustained spectrally sensitive cells responded equally well or better to large than to small (1.0 degree) stimuli, 17.5% were less activated and few of them completely suppressed by larger stimuli. Such cells were poorly orientation sensitive. Only three cells with weak double opponency could be identified (2.7% of this group). 2. Broadband contour (18%) and 3. Panchromatic contour cells (41%). Most neurons of these two groups were strongly activated by spots (1 degree) centered on their RF. They showed a short phasic response to contrast borders and most of them responded to luminance contrasts, including contrast reversal and colour contrasts equated for luminance. The broadband contour cells showed a slight wavelength preference with only weak or without any opponent suppression, the panchromatic contour neurons did not show any wavelength selectivity. Most showed orientation or direction sensitivity, but very sharp orientation selectivity was less common in spectrally biassed than in panchromatic contour cells (see Fig. 11). They responded tonically to gratings of optimal orientation and therefore may play a role also for cortical representation of textures. 22% of a restricted sample of panchromatic contour cells (or 9% of all cells) were hypercomplex.(ABSTRACT TRUNCATED AT 400 WORDS)