Distribution of corticotectal cells in macaque.

We compared the cortical inputs to the superficial and deep compartments of the superior colliculus, asking if the corticotectal system, like the colliculus itself, consists of two functional divisions: visual and visuomotor. We made injections of retrograde tracer extending into both superficial and deep layers in three colliculi: the injection site involved mainly the upper quadrant representation in one case, the lower quadrant representation in a second case, and both quadrants in a third. In a fourth colliculus, the tracer injection was restricted to the lower quadrant representation of the superficial layers. After injections involving both superficial and deep layers, labeled cells were seen over V1, many prestriate visual areas, and in prefrontal and posterior parietal cortex. Both the density of labeled cells and the degree of visuotopic order as inferred from the distribution of labeled cells in cortex varied among areas. In visual areas comprising the lower levels of the cortical hierarchy, visuotopy was preserved, whereas in "higher" areas the distribution of labeled cells did not strongly reflect the visuotopic location of the injection. Despite the widespread distribution of labeled cells, there were several areas with few or no labeled cells: MSTd, 7a, VIP, MIP, and TE. In the case with an injection restricted to superficial layers, labeled cells were seen only in V1 and in striate-recipient areas V2, V3, and MT. The results are consistent with the idea that the corticotectal system consists of two largely nonoverlapping components: a visual component consisting of striate cortex and striate-recipient areas, which projects only to the superficial layers, and a visuomotor component consisting of many other prestriate visual areas as well as frontal and parietal visuomotor areas, which projects to the deep compartment of the colliculus.

Vertical meridian representation on the prelunate gyrus in area V4 of macaque.

The representation of the lower quadrant in area V4 is presently thought to extend along the prelunate gyrus from a foveal representation laterally all the way to the dorsal end of the superior temporal sulcus. However, several studies suggest the possibility of a more complex organization. To see if the visuotopic organization on the crown of the gyrus was relatively homogeneous or instead contained inhomogeneities indicative of more complex organization, we recorded from a grid of points over the prelunate gyrus. Receptive-field size and scatter in the region are large, making it difficult to infer topography from simple inspection of receptive-field sequences. We developed an averaging procedure using data from all recording sites to detect an inhomogeneity in topography with respect to the vertical meridian. With this procedure, we found a vertical meridian representation just medial to the medial end of the lateral sulcus. We also found a significant difference in the incidence of orientation sensitivity on either side of the meridian representation. The results show that the crown of the prelunate gyrus cannot be described as a single homogeneous region, but instead contains at least two different sub-regions adjoining along a shared representation of the vertical meridian.

Effect of attentive fixation in macaque thalamus and cortex.

Attentional modulation of neuronal responsiveness is common in many areas of visual cortex. We examined whether attentional modulation in the visual thalamus was quantitatively similar to that in cortex. Identical procedures and apparatus were used to compare attentional modulation of single neurons in seven different areas of the visual system: the lateral geniculate, three visual subdivisions of the pulvinar [inferior, lateral, dorsomedial part of lateral pulvinar (Pdm)], and three areas of extrastriate cortex representing early, intermediate, and late stages of cortical processing (V2, V4/PM, area 7a). A simple fixation task controlled transitions among three attentive states. The animal waited for a fixation point to appear (ready state), fixated the point until it dimmed (fixation state), and then waited idly to begin the next trial (idle state). Attentional modulation was estimated by flashing an identical, irrelevant stimulus in a neuron's receptive field during each of the three states; the three responses defined a "response vector" whose deviation from the line of equal response in all three states (the main diagonal) indicated the character and magnitude of attentional modulation. Attentional modulation was present in all visual areas except the lateral geniculate, indicating that modulation was of central origin. Prevalence of modulation was modest (26%) in pulvinar, and increased from 21% in V2 to 43% in 7a. Modulation had a push-pull character (as many cells facilitated as suppressed) with respect to the fixation state in all areas except Pdm where all cells were suppressed during fixation. The absolute magnitude of attentional modulation, measured by the angle between response vector and main diagonal expressed as a percent of the maximum possible angle, differed among brain areas. Magnitude of modulation was modest in the pulvinar (19-26%), and increased from 22% in V2 to 41% in 7a. However, average trial-to-trial variability of response, measured by the coefficient of variation, also increased across brain areas so that its difference among areas accounted for more than 90% of the difference in modulation magnitude among areas. We also measured attentional modulation by the ratio of cell discharge due to attention divided by discharge variability. The resulting signal-to-noise ratio of attention was small and constant, 1.3 +/- 10%, across all areas of pulvinar and cortex. We conclude that the pulvinar, but not the lateral geniculate, is as strongly affected by attentional state as any area of visual cortex we studied and that attentional modulation amplitude is closely tied to intrinsic variability of response.

Loss of relative-motion sensitivity in the monkey superior colliculus after lesions of cortical area MT.

Many cells in the superficial layers of the monkey superior colliculus are sensitive to relative motion. The response to a small stimulus moving through a cell's receptive field is strongly modulated by the relative motion between the stimulus and a textured pattern moving through the surrounding visual field; modulation is independent of absolute direction and speed of the stimulus. To determine whether cortical visual area MT is essential for this type of relative-motion sensitivity, colliculus cells were studied in the anesthetized, immobilized preparation after ablation of area MT. Unilateral MT lesions were made by either aspiration, kainic acid injection, or a combination of both methods. Data from the lesioned animals were compared with those from intact animals. Ipsilateral to the lesions, colliculus cells showed an almost total loss of sensitivity to relative motion. This loss was related neither to inadvertent injury of cortical areas neighboring MT nor to incidental optic radiation damage. Two other forms of motion-dependent, center-surround interactions were still present in the colliculus after the cortical lesions. These were a rudimentary sensitivity to differential motion between stimulus and background, which occurs for only one direction of stimulus movement, and a nonselective center-surround suppression, which is induced by movement of a background stimulus in any direction. Visual responsiveness, ocular dominance, and flash-evoked responses were also unaffected by the cortical lesions. We conclude that input from area MT is crucial for relative-motion sensitivity, but not for other response properties, in the superficial layers of the monkey colliculus.

Effect of corticotectal tract lesions on relative motion selectivity in the monkey superior colliculus.

Many cells in the superficial layers of the monkey superior colliculus are sensitive to the relative motion between a small target moving through the classic receptive field and a textured, moving background pattern that fills the visual field beyond the classic receptive field. The cells respond well when motion of the target differs from that of the background, but their responses are suppressed when the target moves in phase with the background. To determine whether this relative motion sensitivity depends on input to the colliculus from visual cortex, we studied colliculus cells in immobilized, anesthetized monkeys after unilateral thermocoagulation, or anesthetic blockade, of the corticotectal tract at the level of the pulvinar. In the colliculus ipsilateral to the corticotectal tract lesions, relative motion sensitivity was significantly reduced when compared either with the colliculus in intact animals or with the colliculus contralateral to the lesion. However, a moving-background stimulus still had a modest suppressive effect compared with a stationary background ("background motion sensitivity"), as is the case for intact animals. Anesthetic blockade of the corticotectal tract had similar effects; relative motion sensitivity, but not background motion sensitivity, was lost following injection of mepivacaine or bupivacaine. Pulvinar cell loss alone, induced by kainic acid injection, had no effect on relative motion sensitivity in the colliculus. The corticotectal tract lesions, but not the anesthetic injections, also had minor effects on flash-evoked responses and spontaneous discharge rates; these effects may reflect a retrograde response of some tectopulvinar cells to injury of their axons by the corticotectal tract lesions. In the colliculus opposite the corticotectal tract lesion, relative motion sensitivity was similar to that in normal animals. However, responses in the presence of a moving background were enhanced, suggesting that removal of cortical input to one colliculus may disinhibit the contralateral colliculus, a phenomenon reminiscent of the Sprague effect in the cat. We conclude that while cortical input to the colliculus may contribute little to the classic receptive field properties of superficial-layer cells, it clearly does contribute to relative motion sensitivity.

Selectivity for relative motion in the monkey superior colliculus.

1. Cells in the superficial layers of the colliculus were studied in immobilized monkeys anesthetized with nitrous oxide. We examined sensitivity to the relative motion between two stimuli: a small target in a cell's receptive field and a large random-dot background pattern that filled most of the visual field outside the receptive field. 2. Most cells were nonselective for either target direction or speed when the background pattern was stationary but were selective for both direction and speed relative to a moving background. Selectivity for relative motion was independent of the absolute direction and speed of both target and background. When both moved at the same speed in the same direction, the response evoked by the target was strongly suppressed. Changing the background direction relative to the target reduced the suppression; suppression was minimal when the two moved in opposite directions. Selectivity for relative direction was broad: the average tuning width at half-amplitude was 136 degrees. When target and background moved in the same direction, increasing or decreasing background speed relative to the target likewise reduced suppression. Average tuning width for relative speed was 1.4 log units. 3. Selectivity for relative motion was a global phenomenon. Suppression was present even when the background pattern was excluded from a region 10 times the receptive-field diameter. However, suppression gradually diminished with increasing distance between the receptive field and the background pattern. 4. Relative motion selectivity was most common in the deeper part of the superficial layers. Ninety percent of the cells below the middle of the stratum griseum superficiale were selective for relative direction, whereas above this level only 45% of the cells were. 5. Cells in the magnocellular and parvocellular layers of the lateral geniculate nucleus did not show selectivity for relative direction. 6. We suggest that the lower one-half of the superficial grey layer and the stratum opticum together constitute a subdivision of the superior colliculus that is specialized to detect strong discontinuities in relative motion. Descending input by way of the corticotectal tract is probably essential for the detection process. the projections from this tectal motion zone to the pulvinar, and from there to prestriate cortex, may provide a feedback pathway through which motion discontinuities such as occur at dynamic occlusion boundaries can influence local feature detection by cortical neurons.

Bilateral projections from the parabigeminal nucleus to the superior colliculus in monkey.

We examined the distribution of labeled neurons in the parabigeminal nucleus of the monkey following injections of retrograde fluorescent tracers into the superior colliculus. The extent of the visual field representation included in the injection site was assessed from the location of labeled cells in striate cortex. The results suggest a rough topographic organization of the parabigeminal nucleus, with the lower quadrant represented anteriorly and the upper quadrant posteriorly. We also found bilateral projections from the parabigeminal nucleus to both superior colliculi, but the crossed projection appeared to terminate only in that part of the colliculus where the vertical meridian is represented. Parabigeminal cells with a crossed projection were larger than those projecting to the ipsilateral colliculus. The results suggest that the organization of the monkey's parabigemino-tectal system is fundamentally similar to that of many other vertebrates.

Saccadic eye movements following kainic acid lesions of the pulvinar in monkeys.

Behavioral and anatomical experiments have suggested that the pulvinar might play a role in the generation of saccadic eye movements to visual targets. To test this idea, we trained monkeys to make visually-guided saccades by requiring them to detect the dimming of a small target. We used three different saccade paradigms. On single-step trials, saccades were made from a central fixation point (FP) to a target at 12, 24 or 36 degrees to the left or right. On overlap trials, the FP remained lit during presentation of a target at 12 or 24 degrees. On double-step trials, the target stepped first to 24 degrees, and then back to 12 degrees on the same side. Animals were trained to criterion, received kainic acid lesions of the pulvinar, and were retested on all three tasks. The lesions were very large, destroying almost all of the visually responsive pulvinar. They also encroached on the lateral geniculate nucleus, thereby producing small foveal scotomas, and this resulted in some behavioral changes, including difficulty in maintaining fixation on the target and in detecting its dimming. Results on the saccade tests suggest that the pulvinar is not crucial for initiation of saccadic eye movements. Saccade latency and amplitude were unimpaired on both single-step and overlap trials. Saccadic performance was also normal on double-step trials. In a second experiment, we measured the average length of fixations during spontaneous viewing of a complex visual scene. Fixation lengths did not differ from those of unoperated control monkeys. We suggest that the neglect, increased saccadic latencies, and prolonged fixations attributed to pulvinar damage in previous studies were probably the result instead of inadvertent damage to tectal afferents. The present results, together with single unit data, point to a role for the pulvinar not in the generation of saccades, but rather in the integration of saccadic eye movements with visual processing.

Comparison of saccadic eye movements in humans and macaques to single-step and double-step target movements.

Human and monkey saccade amplitude and latency, in response to 12-36 degrees target steps, differed substantially despite nearly identical experimental conditions. On single-step trials, monkeys did not undershoot targets, and latencies were insensitive to stimulus and contextual factors. Human saccades did undershoot, their latency was longer, and both undershoot and latency were affected by stimulus variables and experimental context. On double-step trials, the second target step altered primary saccade amplitude when the step occurred as little as 40 msec prior to saccade onset for both humans and monkeys. However, humans and monkeys showed somewhat different amplitude transition functions, and monkeys showed little evidence of parallel programming.

Comparison of the effects of superior colliculus and pulvinar lesions on visual search and tachistoscopic pattern discrimination in monkeys.

In order to investigate whether pulvinar lesions produce behavioral impairments similar to those that follow superior colliculus lesions, monkeys were tested on a visual search task before and after receiving radiofrequency lesions of either the superior colliculus or pulvinar. The animals searched for a small target pattern within an array of varying numbers of irrelevant patterns. After receiving colliculus lesions, the animals showed marked post-operative increases in either search time, percent errors, or both. By contrast, pulvinar lesions had little or no effect on visual search performance. Similarly, in learning to search for a target they had not previously seen, animals with colliculus lesions were impaired relative to unoperated controls, whereas pulvinar-lesioned animals did not differ from controls. In an attempt to confirm the finding that pulvinar lesions impair tachistoscopic pattern discrimination, we determined exposure-duration thresholds of pulvinar- and colliculus-lesioned monkeys for performance of a pattern discrimination. The thresholds of the colliculus-lesioned monkeys were elevated 20-fold relative to controls. By contrast, thresholds of the pulvinar-lesioned monkeys were normal. We conclude that the pulvinar is not critical for the attentional processes in which the superior colliculus participates.

Global visual processing in the monkey superior colliculus.

Neurons were recorded in the superficial layers of the superior colliculus in anesthetized monkeys. As classically described, cells were non-selective for target direction and speed when the target moved through an empty visual field. However, these same cells were sensitive to target direction and speed relative to a textured moving background. The target's response was suppressed when its direction and speed were similar to that of the background, irrespective of the absolute direction of background movement.

Anterograde degeneration in the superior colliculus following kainic acid and radiofrequency lesions of the macaque pulvinar.

Several studies have reported behavioral deficits following thermocoagulation of the primate pulvinar. However, these deficits may have resulted from damage to corticotectal fibers as they pass through the pulvinar. To evaluate this possibility and to determine whether kainic acid can be used to destroy pulvinar cells without damaging corticotectal fibers, we compared anterograde degeneration in the superior colliculus following kainic acid and radiofrequency lesions of the pulvinar. Kainic acid injections into the pulvinar produced total loss of neuronal perikarya within the inferior and lateral pulvinar. Four to 7 days following the kainic acid lesions, terminal and fiber degeneration within the superior colliculus was no greater than that produced by control injections of saline. By contrast, thermocoagulation lesions of the inferior and lateral pulvinar produced dense fiber and terminal degeneration throughout the superficial and intermediate layers of the superior colliculus. We conclude that whereas thermocoagulation of the pulvinar severely damages the corticotectal tract, kainic acid lesions spare these fibers of passage. Thus kainic acid lesions should provide an effective tool for studying the functional significance of the pulvinar.

Effects of kainic acid and radiofrequency lesions of the pulvinar on visual discrimination in the monkey.

Monkeys with thermocoagulation or kainic acid lesions of the pulvinar and unoperated control monkeys were tested in two tasks: pattern discrimination retention and color discrimination learning in which the stimuli were located at the response sites or were separated spatially from them (S-R separation). The monkeys with kainic acid pulvinar lesions were mildly impaired in retention of the pattern discrimination, but were unimpaired in the color discrimination tasks with or without the S-R separation. The monkeys with thermocoagulation lesions, like monkeys with superior colliculus lesions in a prior study, were severely impaired in performing one of the color discrimination tasks with S-R separation. These findings suggest that: (a) the inferior pulvinar, unlike the superior colliculus, does not contribute to the performance of discriminations involving S-R separation; and (b) corticotectal projections traversing the pulvinar and destroyed by the thermocoagulation lesions are crucial to the performance of discriminations involving S-R separation. The results of an earlier experiment also suggested that interruption of corticotectal fibers passing through the pulvinar impairs performance in another task sensitive to superior colliculus lesions--spatial localization of light flashes. Thus, corticotectal projections may be crucial for the contribution of the colliculus to performance in a variety of visual tasks.

Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus.

Superior colliculus lesions had little effect on the visual response of neurons in the monkey inferior pulvinar. By contrast, striate cortex lesions eliminated the visual response of all inferior pulvinar neurons for a period of 3 weeks after the lesion. At longer survival times, a few pulvinar neurons responded to small light spots, but sensitivity to orientation and direction of movement never returned. Thus striate cortex, rather than the colliculus, appears to be responsible for the visual properties of pulvinar cells.

Localization and detection of visual stimuli in monkeys with pulvinar lesions.

Since the pulvinar receives a major ascending projection of the superior colliculus, pulvinar lesions might produce behavioral impairments resembling those that follow colliculus lesions. To test this possibility, we examined the effect of pulvinar lesions in monkeys on the localization and detection of brief light flashes, a task in which monkeys with colliculus lesions are severely impaired. Some of the pulvinar-lesioned monkeys showed localization impairments similar to those in monkeys with colliculus lesions. However, histological analyses of the lesions suggested that these deficits were related not to the pulvinar damage per se, but rather to interruption of corticotectal fibers that pass through the pulvinar. We conclude that the pulvinar is not critical for the ability to locate and detect brief visual stimuli.

Localization and detection of visual stimuli following superior colliculus lesions in rhesus monkeys.

Rhesus monkeys were trained to fixate a central stimulus and to detect and localize a 50 msec light flash presented 6-80 degrees on either side of the central stimulus. Following large lesions of the superior colliculus, they showed persistent deficits in localizing flashes presented 43-80 degrees from the fixation stimulus. However, they were not consistently impaired when the flashes were presented more centrally, and their performance with peripheral stimuli improved when the stimulus duration was 1 sec. Thus, the superior colliculus appears to be necessary for the localization of brief visual stimuli in the far periphery.