Target selection for saccadic eye movements: direction-selective visual responses in the superior colliculus.

We investigated the role of the superior colliculus (SC) in saccade target selection in rhesus monkeys who were trained to perform a direction-discrimination task. In this task, the monkey discriminated between opposed directions of visual motion and indicated its judgment by making a saccadic eye movement to one of two visual targets that were spatially aligned with the two possible directions of motion in the display. Thus the neural circuits that implement target selection in this task are likely to receive directionally selective visual inputs and be closely linked to the saccadic system. We therefore studied prelude neurons in the intermediate and deep layers of the SC that can discharge up to several seconds before an impending saccade, indicating a relatively high-level role in saccade planning. We used the direction-discrimination task to identify neurons whose prelude activity "predicted" the impending perceptual report several seconds before the animal actually executed the operant eye movement; these "choice predicting" cells comprised approximately 30% of the neurons we encountered in the intermediate and deep layers of the SC. Surprisingly, about half of these prelude cells yielded direction-selective responses to our motion stimulus during a passive fixation task. In general, these neurons responded to motion stimuli in many locations around the visual field including the center of gaze where the visual discriminanda were positioned during the direction-discrimination task. Preferred directions generally pointed toward the location of the movement field of the SC neuron in accordance with the sensorimotor demands of the discrimination task. Control experiments indicate that the directional responses do not simply reflect covertly planned saccades. Our results indicate that a small population of SC prelude neurons exhibits properties appropriate for linking stimulus cues to saccade target selection in the context of a visual discrimination task.     

Direction-selective visual responses in macaque superior colliculus induced by behavioral training

In a previous report, we described a heretofore undetected population of neurons in the intermediate and deep layers of the monkey superior colliculus (SC) that yielded directionally selective visual responses to stimuli presented within the central 4 degrees of the visual field. We observed these neurons in three monkeys that had been extensively trained to perform a visual direction discrimination task in this region of the visual field. The task required the monkeys to report the perceived direction of motion by making a saccadic eye movement to one of two targets aligned with the two possible directions of motion. We hypothesized that these neurons reflect a learned association between visual motion direction and saccade direction formed through extensive training on the direction discrimination task. We tested this hypothesis by searching for direction-selective visual responses in two monkeys that had been trained to perform a similar motion discrimination task in which the direction of stimulus motion was dissociated from the direction of the operant saccade. Strongly directional visual responses were absent in these monkeys, consistent with the notion that extensive training can induce highly specific visual responses in a subpopulation of SC neurons.     

Progression in neuronal processing for saccadic eye movements from parietal cortex area lip to superior colliculus

Neurons in both the lateral intraparietal area (LIP) of the monkey parietal cortex and the intermediate layers of the superior colliculus (SC) are activated well in advance of the initiation of saccadic eye movements. To determine whether there is a progression in the covert processing for saccades from area LIP to SC, we systematically compared the discharge properties of LIP output neurons identified by antidromic activation with those of SC neurons collected from the same monkeys. First, we compared activity patterns during a delayed saccade task and found that LIP and SC neurons showed an extensive overlap in their responses to visual stimuli and in their sustained activity during the delay period. The saccade activity of LIP neurons was, however, remarkably weaker than that of SC neurons and never occurred without any preceding delay activity. Second, we assessed the dependence of LIP and SC activity on the presence of a visual stimulus by contrasting their activity in delayed saccade trials in which the presentation of the visual stimulus was either sustained (visual trials) or brief (memory trials). Both the delay and the presaccadic activity levels of the LIP neuronal sample significantly depended on the sustained presence of the visual stimulus, whereas those of the SC neuronal sample did not. Third, we examined how the LIP and SC delay activity relates to the future production of a saccade using a delayed GO/NOGO saccade task, in which a change in color of the fixation stimulus instructed the monkey either to make a saccade to a peripheral visual stimulus or to withhold its response and maintain fixation. The average delay activity of both LIP and SC neuronal samples significantly increased by the advance instruction to make a saccade, but LIP neurons were significantly less dependent on the response instruction than SC neurons, and only a minority of LIP neurons was significantly modulated. Thus despite some overlap in their discharge properties, the neurons in the SC intermediate layers showed a greater independence from sustained visual stimulation and a tighter relationship to the production of an impending saccade than the LIP neurons supplying inputs to the SC. Rather than representing the transmission of one processing stage in parietal cortex area LIP to a subsequent processing stage in SC, the differences in neuronal activity that we observed suggest instead a progressive evolution in the neuronal processing for saccades.     

Participation of prefrontal neurons in the preparation of visually guided eye movements in the rhesus monkey

1. We recorded from 257 neurons in the banks of the posterior third of the principal sulcus of two rhesus monkeys trained to look at a fixation point and make saccades to stimuli in the visual periphery. Sixty-six percent (220/257) discharged or were suppressed in association with one or more aspects of the tasks we used. 2. Fifty-eight percent (151/257) of the neurons responded to the appearance of a spot of light in some part of the contralateral visual field. Cells did not seem to have absolute requirements for stimulus shape, size, or direction of motion. 3. Thirty-six percent (29/79) of visually responsive neurons tested quantitatively gave an enhanced response to the stimulus in the receptive field when the monkey had to make a saccade to the stimulus when its appearance was synchronous with the disappearance of the fixation point (synchron task). Twenty-nine percent (19/57) of the neurons gave an enhanced response to the stimulus when the monkey had to make a saccade to the stimulus some time after it appeared (delayed-saccade task). In general, enhancement in the synchron task correlated well with enhancement in the delayed-saccade task. 4. Enhancement was spatially specific. It did not occur when the monkey made a saccade to a stimulus outside the receptive field even though there was a stimulus within the receptive field. 5. Twenty-three percent (27/117) of neurons studied in the delayed-saccade task gave two bursts, one at the appearance of the stimulus and a second one around the saccade. This second burst generally did not occur when the monkey made the same saccade to a remembered target, but instead required the presence of the visual stimulus, and so we describe it as a reactivation of the visual response. Reactivation was also spatially specific. 6. The latency from reactivation to the beginning of the saccade ranged from 160 ms before the saccade to the beginning of the saccade. Reactivation usually continued for several hundred milliseconds after the saccade, sometimes for the duration of the trial. 7. Reactivation and enhancement are not the same mechanism. Although some cells showed both phenomena there was no correlation between enhancement and reactivation. 8. Cells that showed reactivation in the saccade task also showed reactivation at a weaker level in a suppressed-saccade task. In this task the monkeys had to hold fixation despite the disappearance of the fixation point and the continued presence of the peripheral stimulus.(ABSTRACT TRUNCATED AT 400 WORDS)     

Target selection for saccadic eye movements: prelude activity in the superior colliculus during a direction-discrimination task.

We investigated the role of the superior colliculus (SC) in saccade target selection while macaque monkeys performed a direction-discrimination task. The monkeys selected one of two possible saccade targets based on the direction of motion in a stochastic random-dot display; the difficulty of the task was varied by adjusting the strength of the motion signal in the display. One of the two saccade targets was positioned within the movement field of the SC neuron under study while the other target was positioned well outside the movement field. Approximately 30% of the neurons in the intermediate and deep layers of the SC discharged target-specific preludes of activity that "predicted" target choices well before execution of the saccadic eye movement. Across the population of neurons, the strength of the motion signal in the display influenced the intensity of this "predictive" prelude activity: SC activity signaled the impending saccade more reliably when the motion signal was strong than when it was weak. The dependence of neural activity on motion strength could not be explained by small variations in the metrics of the saccadic eye movements. Predictive activity was particularly strong in a subpopulation of neurons with directional visual responses that we have described previously. For a subset of SC neurons, therefore, prelude activity reflects the difficulty of the direction discrimination in addition to the target of the impending saccade. These results are consistent with the notion that a restricted network of SC neurons plays a role in the process of saccade target selection.     

The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey

Neurons in the lateral intraparietal area of the monkey (LIP) have visual receptive fields in retinotopic coordinates when studied in a fixation task. However, in the period immediately surrounding a saccade these receptive fields often shift, so that a briefly flashed stimulus outside the receptive field will drive the neurons if the eye movement will bring the spatial location of that vanished stimulus into the receptive field. This is equivalent to a transient shift of the retinal receptive field. The process enables the monkey brain to process a stimulus in a spatially accurate manner after a saccade, even though the stimulus appeared only before the saccade. We studied the time course of this receptive field shift by flashing a task-irrelevant stimulus for 100 ms before, during, or after a saccade. The stimulus could appear in receptive field as defined by the fixation before the saccade (the current receptive field) or the receptive field as defined by the fixation after the saccade (the future receptive field). We recorded the activity of 48 visually responsive neurons in LIP of three hemispheres of two rhesus monkeys. We studied 45 neurons in the current receptive field task, in which the saccade removed the stimulus from the receptive field. Of these neurons 29/45 (64%) showed a significant decrement of response when the stimulus appeared 250 ms or less before the saccade, as compared with their activity during fixation. The average response decrement was 38% for those cells showing a significant (P < 0.05 by t-test) decrement. We studied 39 neurons in the future receptive field task, in which the saccade brought the spatial location of a recently vanished stimulus into the receptive field. Of these 32/39 (82%) had a significant response to stimuli flashed for 100 ms in the future receptive field, even 400 ms before the saccade. Neurons never responded to stimuli moved by the saccade from a point outside the receptive field to another point outside the receptive field. Neurons did not necessarily show any saccadic suppression for stimuli moved from one part of the receptive field to another by the saccade. Stimuli flashed <250 ms before the saccade-evoked responses in both the presaccadic and the postsaccadic receptive fields, resulting in an increase in the effective receptive field size, an effect that we suggest is responsible for perisaccadic perceptual inaccuracies.     

Spatial processing in the monkey frontal eye field. II. Memory responses.

Monkeys and humans can easily make accurate saccades to stimuli that appear and disappear before an intervening saccade to a different location. We used the flashed-stimulus task to study the memory processes that enable this behavior, and we found two different kinds of memory responses under these conditions. In the short-term spatial memory response, the monkey fixated, a stimulus appeared for 50 ms outside the neuron's receptive field, and from 200 to 1,000 ms later the monkey made a saccade that brought the receptive field onto the spatial location of the vanished stimulus. Twenty-eight of 48 visuomovement cells and 21/32 visual cells responded significantly under these circumstances even though they did not discharge when the monkey made the same saccade without the stimulus present or when the stimulus appeared and the monkey did not make a saccade that brought its spatial location into the receptive field. Response latencies ranged from 48 ms before the beginning of the saccade (predictive responses) to 272 ms after the beginning of the saccade. After the monkey made a series of 16 saccades that brought a stimulus into the receptive field, 21 neurons demonstrated a longer term, intertrial memory response: they discharged even on trials in which no stimulus appeared at all. This intertrial memory response was usually much weaker than the within-trial memory response, and it often lasted for over 20 trials. We suggest that the frontal eye field maintains a spatially accurate representation of the visual world that is not dependent on constant or continuous visual stimulation, and can last for several minutes.     

Effect of spatial attention on the responses of area MT neurons

This study examines the influence of spatial attention on the responses of neurons in the middle temporal visual area (MT or V5) of extrastriate cortex. Two monkeys were trained to perform a direction-discrimination task. On each trial, two apertures of random-dot stimuli appeared simultaneously at two spatially separated locations; the monkeys were required to discriminate the direction of stimulus motion at one location while ignoring the stimulus at the other location. After extensive training, we recorded the responses of MT neurons in two configurations: 1) Both apertures placed "within" the neuron's receptive field (RF) and 2) one aperture covering the RF while the other was presented at a "remote" location. For each unit we compared the responses to identical stimulus displays when the monkey was instructed to attend to one or the other aperture. The responses of MT neurons were 8.7% stronger, on average, when the monkey attended to the spatial location that contained motion in the "preferred" direction. Attentional effects were equal, on average, in the within RF and remote configurations. The attentional modulations began approximately 300 ms after stimulus onset, gradually increased throughout the trial, and peaked near stimulus offset. An analysis of the neuronal responses on error trials suggests that the monkeys failed to attend to the appropriate spatial location on these trials. The relatively weak attentional effects that we observed contrast strikingly with recent results of Treue and Maunsell, who demonstrated very strong attentional modulations (median effect >80%) in MT in a task that shares many features with ours. Our results suggest that spatial attention alone is not sufficient to induce strong attentional effects in MT even when two competing motion stimuli appear within the RF of the recorded neuron. The difference between our results and those of Treue and Maunsell suggests that the magnitude of the attentional effects in MT may depend critically on how attention is directed to a particular stimulus and on the precise demands of the task.     

Reward-predicting activity of dopamine and caudate neurons--a possible mechanism of motivational control of saccadic eye movement

Recent studies have suggested that the basal ganglia are related to motivational control of behavior. To study how motivational signals modulate motor signals in the basal ganglia, we examined activity of midbrain dopamine (DA) neurons and caudate (CD) projection neurons while monkeys were performing a one-direction-rewarded version (1DR) of memory-guided saccade task. The cue stimulus indicated the goal position for an upcoming saccade and the presence or absence of reward after the trial. Among four monkeys we studied, three were sensitive to reward such that saccade velocity was significantly higher in the rewarded trials than in the nonrewarded trials; one monkey was insensitive to reward. In the reward-sensitive monkeys, both DA and CD neurons responded differentially to reward-indicating and no-reward-indicating cues. Thus DA neurons responded with excitation to a reward-indicating cue and with inhibition to a no-reward-indicating cue. A group of CD neurons responded to the cue in their response fields (mostly contralateral) and the cue response was usually enhanced when it indicated reward. In the reward-insensitive monkey, DA neurons showed no response to the cue, while the cue responses of CD neurons were not modulated by reward. Many CD neurons in the reward-sensitive monkeys, but not the reward-insensitive monkey, showed precue activity. These results suggest that DA neurons, with their connection to CD neurons, modulate the spatially selective signals in CD neurons in the reward-predicting manner and CD neurons in turn modulate saccade parameters with their polysynaptic connections to the oculomotor brain stem.     

Multielectrode evidence for spreading activity across the superior colliculus movement map

The monkey superior colliculus (SC) has maps for both visual input and movement output in the superficial and intermediate layers, respectively, and activity on these maps is generally related to visual stimuli only in one part of the visual field and/or to a restricted range of saccadic eye movements to those stimuli. For some neurons within these maps, however, activity has been reported to spread from the caudal SC to the rostral SC during the course of a saccade. This spread of activity was inferred from averages of recordings at different sites on the SC movement map during saccades of different amplitudes and even in different monkeys. In the present experiments, SC activity was recorded simultaneously in pairs of neurons to observe the spread of activity during individual saccades. Two electrodes were positioned along the rostral-caudal axis of the SC with one being more caudal than the other, and 60 neuron pairs whose movement fields were large enough to see a spread of activity were studied. During individual saccades, the relative time of discharge of the two neurons was compared using 1) the time difference between peak discharge of the two neurons, 2) the difference between the "median activation time" of the two neurons, and 3) the shift required to align the two discharge patterns using cross-correlation. All three analysis methods gave comparable results. Many pairs of neurons were activated in sequence during saccade generation, and the order of activation was most frequently caudal to rostral. Such a sequence of activation was not observed in every neuron pair, but over the sample of neuron pairs studied, the spread was statistically significant. When we compared the time of neuronal activity to the time of saccade onset, we found that the caudal neuronal activity was more likely to be before the saccade, whereas the rostral neuronal activity was more likely to be during the saccade. These results demonstrate that when individual pairs of neurons are examined during single saccades there is evidence of a caudal to rostral spread of activity within the monkey SC, and they confirm the previous inferences of a spread of activity drawn from observations on averaged neuronal activity during multiple saccades. The functional contribution of this spread of activity remains to be determined.     

Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements

The intermediate and deep layers of the monkey superior colliculus (SC) comprise a retinotopically organized map for eye movements. The rostral end of this map, corresponding to the representation of the fovea, contains neurons that have been referred to as "fixation cells" because they discharge tonically during active fixation and pause during the generation of most saccades. These neurons also possess movement fields and are most active for targets close to the fixation point. Because the parafoveal locations encoded by these neurons are also important for guiding pursuit eye movements, we studied these neurons in two monkeys as they generated smooth pursuit. We found that fixation cells exhibit the same directional preferences during pursuit as during small saccades-they increase their discharge during movements toward the contralateral side and decrease their discharge during movements toward the ipsilateral side. This pursuit-related activity could be observed during saccade-free pursuit and was not predictive of small saccades that often accompanied pursuit. When we plotted the discharge rate from individual neurons during pursuit as a function of the position error associated with the moving target, we found tuning curves with peaks within a few degrees contralateral of the fovea. We compared these pursuit-related tuning curves from each neuron to the tuning curves for a saccade task from which we separately measured the visual, delay, and peri-saccadic activity. We found the highest and most consistent correlation with the delay activity recorded while the monkey viewed parafoveal stimuli during fixation. The directional preferences exhibited during pursuit can therefore be attributed to the tuning of these neurons for contralateral locations near the fovea. These results support the idea that fixation cells are the rostral extension of the buildup neurons found in the more caudal colliculus and that their activity conveys information about the size of the mismatch between a parafoveal stimulus and the currently foveated location. Because the generation of pursuit requires a break from fixation, the pursuit-related activity indicates that these neurons are not strictly involved with maintaining fixation. Conversely, because activity during the delay period was found for many neurons even when no eye movement was made, these neurons are also not obligatorily related to the generation of a movement. Thus the tonic activity of these rostral neurons provides a potential position-error signal rather than a motor command-a principle that may be applicable to buildup neurons elsewhere in the SC.     

Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey

We recorded the activity of single neurons in the posterior parietal cortex (area LIP) of two rhesus monkeys while they discriminated the direction of motion in random-dot visual stimuli. The visual task was similar to a motion discrimination task that has been used in previous investigations of motion-sensitive regions of the extrastriate cortex. The monkeys were trained to decide whether the direction of motion was toward one of two choice targets that appeared on either side of the random-dot stimulus. At the end of the trial, the monkeys reported their direction judgment by making an eye movement to the appropriate target. We studied neurons in LIP that exhibited spatially selective persistent activity during delayed saccadic eye movement tasks. These neurons are thought to carry high-level signals appropriate for identifying salient visual targets and for guiding saccadic eye movements. We arranged the motion discrimination task so that one of the choice targets was in the LIP neuron's response field (RF) while the other target was positioned well away from the RF. During motion viewing, neurons in LIP altered their firing rate in a manner that predicted the saccadic eye movement that the monkey would make at the end of the trial. The activity thus predicted the monkey's judgment of motion direction. This predictive activity began early in the motion-viewing period and became increasingly reliable as the monkey viewed the random-dot motion. The neural activity predicted the monkey's direction judgment on both easy and difficult trials (strong and weak motion), whether or not the judgment was correct. In addition, the timing and magnitude of the response was affected by the strength of the motion signal in the stimulus. When the direction of motion was toward the RF, stronger motion led to larger neural responses earlier in the motion-viewing period. When motion was away from the RF, stronger motion led to greater suppression of ongoing activity. Thus the activity of single neurons in area LIP reflects both the direction of an impending gaze shift and the quality of the sensory information that instructs such a response. The time course of the neural response suggests that LIP accumulates sensory signals relevant to the selection of a target for an eye movement.     

Behavioral modulation of neuronal activity in monkey striate cortex: excitation in the absence of active central fixation

Summary Two rhesus monkeys were trained to fixate a small fixation point for randomly varying periods of time using the dimming paradigm. During single unit recording in the striate cortex the fixation point was turned off for a few hundred milliseconds in the presence of a peripheral stimulus. During the disappearance of the fixation point the peripheral stimulus could dim and because of that, in some trials the monkey's saccade to the stimulus right after the offset of the fixation point. In other trials of the same task the monkeys suppressed the execution of a saccade without missing the dimming of the stimulus. During the monkeys performance of this task, striate cortex neurons display an increase of activity after fixation point offset in the presence of a receptive field stimulus, independent of the monkey's decision to look at it or not. Its occurrence can be interpreted as a sign of the monkey having interrupted active fixation of the fixation point and/or having shifted its visual attention towards the peripheral target without necessarily executing a saccade to it. This work was supported by the Deutsche Forschungsgemeinschaft This work was supported by the Deutsche Forschungsgemeinschaft This work was supported by the Deutsche Forschungsgemeinschaft     

Visual and oculomotor functions of monkey subthalamic nucleus.

1. Single-unit recordings were obtained from the subthalamic nuclei of three monkeys trained to perform a series of visuooculomotor tasks. The monkeys were trained to fixate on a spot of light on the screen (fixation task). When the spot was turned off and a target spot came on, they were required to fixate on the target quickly by making a saccade. Visually guided saccades were elicited when the target came on without a time gap (saccade task). Memory-guided saccades were elicited by delivering a brief cue stimulus while the monkey was fixating; after a delay, the fixation spot was turned off and the monkey made a saccade to the remembered target (delayed saccade task). 2. Of 265 neurons tested, 95 showed spike activity that was related to some aspects of the visuooculomotor tasks, whereas 66 neurons responded to active or passive limb or body movements. The task-related activities were classified into the following categories: eye fixation-related, saccade-related, visual stimulus-related, target- and reward-related, and lever release-related. 3. Activity related to eye fixation (n = 22) consisted of a sustained spike discharge that occurred while the animal was fixating on a target light during the tasks. The activity increased after the animal started fixating on the target and abruptly ceased when the target went off. The activity was unrelated to eye position. It was not elicited during eye fixation outside the tasks. The activity decreased when the target spot was removed. 4. Activity related to saccades (n = 22) consisted of a phasic increase in spike frequency that was time locked with a saccade made during the tasks. The greatest increases occurred predominantly after saccade onset. This activity usually was unrelated to spontaneous saccades made outside the task. The changes in activity typically were optimal in one direction, generally toward the contralateral side. 5. Visual responses (n = 14) consisted of a phasic excitation in response to a visual probe stimulus or target. Response latencies usually were 70-120 ms. The receptive fields generally were centered in the contralateral hemifield, sometimes extending into the ipsilateral field. The receptive fields included the foveal region in seven neurons; most of these neurons responded best to parafoveal stimulation. Peripheral stimuli sometimes suppressed the activity of visually responsive neurons. 6. Activity related to target and reward (n = 29) consisted of sustained spike discharge that occurred only when the monkey could expect a reward by detecting the dimming of the light spot that he was fixating.(ABSTRACT TRUNCATED AT 400 WORDS)     

Prefrontal neuronal activity encodes spatial target representations sequentially updated after nonspatial target-shift cues

We examined prefrontal neuronal activity while monkeys performed a sequential target-shift task, in which, after a positional cue indicated the initial saccade target among 8 peripheral positions, the monkeys were required to internally shift the target by one position on every flash of a target-shift cue. The target-shift cue appeared in the center 0 to 3 times within a single trial and was always the same in shape, size, and color. We found selective neuronal activity related to the target position: when the target-shift cue implied the target shift to particular peripheral positions, neurons exhibited early-dominant and late-dominant activity during the following delay period. The early-dominant target-selective activity emerged early in the delay just after the presentation of the target-shift cue, whereas the late-dominant activity gradually built up toward the end of the delay. Because the target-shift cue was not related to any specific target location, the early-dominant target-selective activity could not be a mere visual response to the target-shift cue. We suggest that the early-dominant activity reflects the transitory representation for the saccade target that was triggered by the nonspatial target-shift cue, whereas the late-dominant activity reflects the target representation in the spatial working memory or the preparatory set for the possible impending saccade, being repeatedly updated during sequential target shifts.     

Reaction times of manual responses to a visual stimulus at the goal of a planned memory-guided saccade in the monkey

Monkeys demonstrate improved contrast sensitivity at the goal of a planned memory-guided saccade (Science 299:81–86, 2003). Such perceptual improvements have been ascribed to an endogenous attentional advantage induced by the saccade plan. Speeded reaction times have also been used as evidence for attention. We therefore asked whether the attentional advantage at the goal of a planned memory-guided saccade led to speeded manual reaction times following probes presented at the saccade goal in a simple detection task. We found that monkeys showed slower manual reaction times when the probe appeared at the memorized goal of the planned saccade when compared to manual reaction times following a probe that appeared opposite the saccade goal. Flashing a distractor at the saccade goal after target presentation appeared to slow reaction times further. Our data, combined with prior results, suggest that a spatially localized inhibition operates on the neural representation of the saccade goal. This inhibition may be closely related or identical to the processes underlying inhibition-of-return. We also found that if the same detection task was interleaved with a difficult perceptual discrimination task, manual reaction times became faster when the probe was at the saccade goal. We interpret these results as being an effect of task difficulty; the more difficult interleaved task may have engaged endogenous attentional resources more effectively, allowing it to override the inhibition at the saccade goal. We construct and discuss a simple working hypothesis for the relationship between the effects of prior attention on neural activity in salience maps and on performance in detection and discrimination tasks.     

Functional properties of monkey caudate neurons. II. Visual and auditory responses

1. Visual responses of caudate neurons were studied in monkeys trained to fixate on a small spot of light. A visual stimulus (another spot of light) was presented in various contexts of behavior using different behavioral paradigms. Visual receptive fields were usually large and centered on the contralateral hemifield. Among 217 neurons with visual responses, 184 were further classified into subtypes. 2. Visual responses in 64 neurons were not modulated by changing the paradigms (unconditional visual responses). In the other neurons, visual responses were dependent on the behavioral contexts in which the stimulus was presented. Three types of behavioral modulation were found. 3. A saccade-enhanced visual response (n = 37) was the one that was enhanced if the monkey made a saccade to the stimulus on its appearance. The enhancement was spatially selective: the response was depressed if the saccade was directed away from the stimulus. 4. Memory-contingent visual responses (n = 36) were present preferentially when the monkey remembered the location of the stimulus and a few seconds later made a saccade to the remembered location. Responses were greater when the location of the stimulus was randomized between trials. 5. Expectation-contingent visual responses (n = 46) were present preferentially when the stimulus came on while the monkey was not fixating another spot, and the stimulus was related directly to a reward. Unlike the other types, its receptive field included both contralateral and ipsilateral hemifields without a particular preference. 6. A small number of neurons (n = 16) showed a visual response that easily habituated. 7. Latencies of visual responses were usually between 100 and 200 ms. The latencies of the memory-contingent, expectation-contingent, and habituated visual responses tended to be longer than the others and tended to be more variable between trials. 8. Among auditory responsive neurons only a small proportion were related to the tasks. The response was greater to a contralateral sound. It was enhanced if the monkey used the sound as the cue for the future target location. 9. The results suggest that sensory responses of caudate neurons could be used to guide a subsequent sequence of learned behaviors by confirming predicted environmental states, renewing memory, or establishing a motor set.     

Substantia nigra stimulation influences monkey superior colliculus neuronal activity bilaterally

The inhibitory drive arising from the basal ganglia is thought to prevent the occurrence of orienting movements of the eyes, head, and body in monkeys and other mammals. The direct projection from the substantia nigra pars reticulata (SNr) to the superior colliculus (SC) mediates the inhibition. Since the original experiments in the SNr of monkeys the buildup or prelude neuron has been a focus of SC research. However, whether the SNr influences buildup neurons in SC is unknown. Furthermore, a contralateral SNr-SC pathway is evident in many species but remains unexplored in the alert monkey. Here we introduced electrical stimulation of one or both SNr nuclei while recording from SC buildup neurons. Stimulation of the SNr reduced the discharge rate of SC buildup neurons bilaterally. This result is consistent with activation of an inhibitory drive from SNr to SC. The time course of the influence of ipsilateral SNr on the activity of most SC neurons was longer (approximately 73 ms) than the influence of the contralateral SNr (approximately 34 ms). We also found that the variability of saccade onset time and saccade direction was altered with electrical stimulation of the SNr. Taken together our results show that electrical stimulation activates the inhibitory output of the SNr that in turn, reduces the activity of SC buildup neurons in both hemispheres. However, rather than acting as a gate for saccade initiation, the results suggest that the influence of SNr inhibition on visually guided saccades is more subtle, shaping the balance of excitation and inhibition across the SC.     

Learning increases stimulus salience in anterior inferior temporal cortex of the macaque.

With experience, an object can become behaviorally relevant and thereby quickly attract our interest when presented in a visual scene. A likely site of these learning effects is anterior inferior temporal (aIT) cortex, where neurons are thought to participate in the filtering of irrelevant information out of complex visual displays. We trained monkeys to saccade consistently to one of two pictures in an array, in return for a reward. The array was constructed by pairing two stimuli, one of which elicited a good response from the cell when presented alone ("good" stimulus) and the other of which elicited a poor response ("poor" stimulus). The activity of aIT cells was recorded while monkeys learned to saccade to either the good or poor stimulus in the array. We found that neuronal responses to the array were greater (before the saccade occurred) when training reinforced a saccade to the good stimulus than when training reinforced a saccade to the poor stimulus. This difference was not present on incorrect trials, i.e., when saccades to the incorrect stimulus were made. Thus the difference in activity was correlated with performance. The response difference grew over the course of the recording session, in parallel with the improvement in performance. The response difference was not preceded by a difference in the baseline activity of the cells, unlike what was found in studies of cued visual search and working memory in aIT cortex. Furthermore, we found similar effects in a version of the task in which any of 10 possible pairs of stimuli, prelearned before the recording session, could appear on a given trial, thereby precluding a working memory strategy. The results suggest that increasing the behavioral significance of a stimulus through training alters the neural representation of that stimulus in aIT cortex. As a result, neurons responding to features of the relevant stimulus may suppress neurons responding to features of irrelevant stimuli.     

Directional pursuit deficits following lesions of the foveal representation within the superior temporal sulcus of the macaque monkey

Ibotenic acid lesions of the middle temporal visual area (MT) have previously been shown to impair a monkey's ability to initiate smooth pursuit eye movements to targets moving in the extrafoveal visual field (30). This is a retinotopic deficit: pursuit is impaired in all directions within the affected portion of the contralateral visual field. In the present experiments we analyzed the effects of lesions of the foveal representation of MT on the maintenance of foveal pursuit. Injections of ibotenic acid were directed toward the representation of the fovea within MT but spread into extrafoveal regions of MT and adjacent visual areas within the superior temporal sulcus. Chemical lesions of the foveal representation produced a directional deficit in the maintenance of pursuit: the monkey failed to match eye speed to target speed when pursuing a target that moved toward the side of the brain with the lesion. This deficit was evident regardless of the part of the visual field in which target motion began, and pursuit at higher target speeds was more severely affected. The directional deficit was qualitatively similar to pursuit deficits observed in human patients following large parietal-occipital lesions. Extension of the lesions into extrafoveal regions of the contralateral visual field representation also resulted in retinotopic deficits for pursuit initiation: the monkey was unable to match the speed of its pursuit eye movement to that of a target or to adjust the amplitude of its saccade to compensate for target motion. The errors in pursuit speed and saccade amplitude for initiation of pursuit into the contralateral visual field were linearly related, which supports the hypothesis that both deficits arise from damage to the same underlying visual motion processing mechanism. The selectivity of the retinotopic deficit for motion information was also investigated by reducing retinal motion through the use of a stabilized image. After the lesion, the monkeys continued normal pursuit when a position error was present during stabilization, supporting the view that the deficit was related to loss of motion but not position information.