Response of neurons in the lateral intraparietal area to a distractor flashed during the delay period of a memory-guided saccade

Recent experiments raised the possibility that the lateral intraparietal area (LIP) might be specialized for saccade planning. If this was true, one would expect a decreased sensitivity to irrelevant visual stimuli appearing late in the delay period of a memory-guided delayed-saccade task to a target outside the neurons' receptive fields. We trained two monkeys to perform a standard memory-guided delayed-saccade task and a distractor task in which a stimulus flashed for 200 ms at a predictable time 300-100 ms before the end of the delay period. We used two locations, one in the most active part of the receptive field and another well outside the receptive field. We used six kinds of trials randomly intermixed: simple delayed-saccade trials into or away from the receptive field and distractor trials with saccade target and distractor both in the receptive field, both out of the receptive field, or one at each location. This enabled us to study the response to the distractor as a function of the monkey's preparation of a memory-guided delayed-saccade task. We had assumed that the preparation of a saccade away from the receptive field would result in an attenuation of the response to the distractor, i.e., a distractor at the location of the saccade goal would evoke a greater response than when it appeared at a location far from the saccade goal. Instead we found that neurons exhibited either a normal or an enhanced visual response to the distractor during the memory period when the target flashed outside the receptive field. When the distractor flashed at the location of the saccade target, the response to the distractor was either unchanged or diminished. The response to a distractor away from the target location of a memory-guided saccade was even greater than the response to the same target when it was the target for the memory-guided saccade task. Immediate presaccadic activity did not distinguish between a saccade to the receptive field when there was no distractor and a distractor in the receptive field when the monkey made a saccade elsewhere. Nonetheless the distractor had no significant effect on the saccade latency, accuracy, or velocity despite the brisk response it evoked immediately before the saccade. We suggest that these results are inconsistent with a role for LIP in the specific generation of saccades, but they are consistent with a role for LIP in the generation of visual attention.     

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.     

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)     

Visual responses of thalamic neurons depending on the direction of gaze and the position of targets in space

Summary Visual receptive field properties of neurons in the region of the thalamic internal medullary lamina were studied in alert cats while they fixated in various directions. In slightly more than 50% of the cells, the responsiveness of the cells was found to depend on the location of the stimulus with respect to the head-body axis (stimulus absolute position). A cell could ignore a stimulus outside its absolute field even if it was well placed within its receptive field.Three types of neurons were distinguished. Neurons with small central receptive fields were tonically activated when the animal fixated the stimulus in one half of the screen (usually contralateral). The firing rate of these cells was related to the stimulus absolute position measured along a preferred axis. Similarly, neurons with large receptive fields fired as a function of stimulus absolute position but stimulus fixation was not required. Neurons with eccentric fields responded to stimuli located in a target area defined in head-body coordinates. Such cells gave presaccadic bursts with eye movements terminating in the target area.The conclusion proposed is that neurons exist which code visual spatial information in a non-retinal frame of reference. This coding takes place at the time of stimulus presentation. Its role may be seen in the initiation of visually guided movements.     

Discharge patterns of neurons in the rostral superior colliculus of cat: activity related to fixation of visual and auditory targets

Neurons in the rostral superior colliculus (SC) of alert cats exhibit quasi-sustained discharge patterns related to the fixation of visual targets. Because some SC neurons also respond to auditory stimuli, we investigated whether there is a population of neurons in the rostral SC which is active in relation to fixation of both auditory and visual targets. We identified cells which were active with visual fixation and which continued to discharge if the fixation stimulus was briefly extinguished. The population of neurons exhibited similar discharge characteristics when the fixation stimulus was auditory. Few neurons were significantly more active during fixation of visual targets than during fixation of auditory targets. Most fixation neurons showed a diminished discharge rate during spontaneous (self-generated) saccadic eye movements away from a visual fixation stimulus, regardless of the direction of the saccade. this diminished discharge rate (or pause) typically began, on average, 12.2 ms before saccade onset and the duration of the pause was Ionger than the duration of the saccade. These observations are consistent with the hypothesis that increased discharge of these neurons is related to active fixation and that reductions in their activity are important for the generation of saccades. However, the lack of a precise relationship between pause duration and saccade duration implies that these neurons would be unlikely to project directly to the saccadic burst generator. The mean interval from the beginning of the pauses of fixation neurons to be beginning of the saccades away from fixation targets is also shorter than has been found in brainstem omnipause neurons. By analogy with the concept of a receptive field, agaze position error field depicts the range of gaze position error for which a cell is active. Although fixation neurons appear to encode the magnitude and direction of the error between visual targets and the visual axis, visual error fields at the end of fixating eye movements were significantly larger than those at stimulus onset. For auditory stimuli, this difference was not significant. These observations are compatible with a number of recent experiments indicating that neural signals of eye position are damped or delayed with respect to current eye position.     

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.     

Temporal processing of saccade targets in parietal cortex area LIP during visual search

We studied whether the lateral intraparietal (LIP) area-a subdivision of parietal cortex anatomically interposed between visual cortical areas and saccade executive centers-contains neurons with activity patterns sufficient to contribute to the active process of selecting saccade targets in visual search. Visually responsive neurons were recorded while monkeys searched for a color-different target presented concurrently with seven distractors evenly distributed in a circular search array. We found that LIP neurons initially responded indiscriminately to the presentation of a visual stimulus in their response fields, regardless of its feature and identity. Their activation nevertheless evolved to signal the search target before saccade initiation: an ideal observer could reliably discriminate the target from the individual activation of 60% of neurons, on average, 138 ms after stimulus presentation and 26 ms before saccade initiation. Importantly, the timing of LIP neuronal discrimination varied proportionally with reaction times. These findings suggest that LIP activity reflects the selection of both the search target and the targeting saccade during active visual search.     

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)     

Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal

1. We studied the activity of single neurons in the monkey frontal eye fields during oculomotor tasks designed to assess the activity of these neurons when there was a dissonance between the spatial location of a target and its position on the retina. 2. Neurons with presaccadic activity were first studied to determine their receptive or movement fields and to classify them as visual, visuomovement, or movement cells with the use of the criteria described previously (Bruce and Goldberg 1985). The neurons were then studied by the use of double-step tasks that dissociated the retinal coordinates of visual targets from the dimensions of saccadic eye movements necessary to acquire those targets. These tasks required that the monkeys make two successive saccades to follow two sequentially flashed targets. Because the second target disappeared before the first saccade occurred, the dimensions of the second saccade could not be based solely on the retinal coordinates of the target but also depended on the dimensions of the first saccade. We used two versions of the double-step task. In one version neither target appeared in the cell's receptive or movement field, but the second eye movement was the optimum amplitude and direction for the cell (right-EM/wrong-RF task). In the other the second stimulus appeared in the cell's receptive field, but neither eye movement was appropriate for the cell (wrong-EM/right-RF task). 3. Most frontal-eye-field cells discharged in the right-EM/wrong-RF version of the double-step task. Their discharge began after the first saccade and continued until the second saccade was made. They usually discharged even on occasional trials in which the monkey failed to make the second saccade. They discharged much less, or not at all, in the wrong-EM/right-RF version of the double-step paradigm. Thus most presaccadic cells in the frontal eye fields were tuned to the dimensions of saccadic eye movements rather than to the coordinates of retinal stimulation. 4. Eleven movement cells (including 1 which also had independent postsaccadic activity for saccades opposite its presaccadic movement field) were studied, and all had significant activity in the right-EM/wrong-RF task. 5. Almost all (28/32) visuomovement cells, including 12 with independent postsaccadic activity, discharged in the right-EM/wrong-RF task. None of the four that failed had independent postsaccadic activity. 6. The majority (26/40) of visual cells were responsive in the right-EM/wrong-RF task.(ABSTRACT TRUNCATED AT 400 WORDS)     

Short-term changes in movement frequency do not alter the spatial tuning of saccade-related neurons in intraparietal cortex

Modulations of the firing rates of neurons in the lateral intraparietal area (LIP) have been observed during experiments designed to examine decision-processing, movement planning, and visual attention. These modulations have been assumed to reflect a uniform scaling of spatially stationary response fields, which describe firing rate as a function of either visual target location or movement metrics. However, because complete response fields are rarely collected, the possibility exists that these modulations may reflect shifts in response field location or changes in response field size. Moreover, many of these observed changes in LIP neuronal activity are also correlated with experimental practices that alter the frequency with which particular visual stimuli are viewed and particular movements are produced. The effects of repeatedly presenting a particular target and eliciting a particular movement on the response fields of LIP neurons warrant closer inspection because manipulations of this type are known to alter both the location and size of the receptive fields of many cortical sensory neurons. To address this issue, we measured the response fields of neurons in intraparietal cortex under two conditions over a period of up to 2 h: one in which each of nearly 200 stimulus locations was equally likely to serve as the saccade target on a trial, and a second in which one stimulus location was up to 750 times likelier to serve as the saccade target on a trial than were any of the other stimulus locations. We found no shifts in response field location or changes in response field size when we altered the frequency with which particular movements were produced or particular visual stimuli were presented. These data suggest that the response fields of intraparietal neurons are stationary over short periods of time and under conditions similar to those typically used to study LIP neuronal activity.     

Primate antisaccade. II. Supplementary eye field neuronal activity predicts correct performance

Neuronal activities were recorded in the supplementary eye field (SEF) of 3 macaque monkeys trained to perform antisaccades pseudorandomly interleaved with prosaccades, as instructed by the shape of a central fixation point. The prosaccade goal was indicated by a peripheral stimulus flashed anywhere on the screen, whereas the antisaccade goal was an unmarked site diametrically opposite the flashed stimulus. The visual cue was given immediately after the instruction cue disappeared in the immediate-saccade task, or during the instruction period in the delayed-saccade task. The instruction cue offset was the saccade gosignal. Here we focus on 92 task-related neurons: visual, eye-movement, and instruction/fixation neurons. We found that 73% of SEF eye-movement-related neurons fired significantly more before anti-saccades than prosaccades. This finding was analyzed at 3 levels: population, single neuron, and individual trial. On individual antisaccade trials, 40 ms before saccade, the firing rate of eye-movement-related neurons was highly predictive of successful performance. A similar analysis of visual responses (40 ms astride the peak) gave less-coherent results. Fixation neurons, activated during the initial instruction period (i.e., after the instruction cue but before the stimulus) always fired more on antisaccade than on prosaccade trials. This trend, however, was statistically significant for only half of these neurons. We conclude that the SEF is critically involved in the production of antisaccades.     

Spatial updating in area LIP is independent of saccade direction

We explore the world around us by making rapid eye movements to objects of interest. Remarkably, these eye movements go unnoticed, and we perceive the world as stable. Spatial updating is one of the neural mechanisms that contributes to this perception of spatial constancy. Previous studies in macaque lateral intraparietal cortex (area LIP) have shown that individual neurons update, or "remap," the locations of salient visual stimuli at the time of an eye movement. The existence of remapping implies that neurons have access to visual information from regions far beyond the classically defined receptive field. We hypothesized that neurons have access to information located anywhere in the visual field. We tested this by recording the activity of LIP neurons while systematically varying the direction in which a stimulus location must be updated. Our primary finding is that individual neurons remap stimulus traces in multiple directions, indicating that LIP neurons have access to information throughout the visual field. At the population level, stimulus traces are updated in conjunction with all saccade directions, even when we consider direction as a function of receptive field location. These results show that spatial updating in LIP is effectively independent of saccade direction. Our findings support the hypothesis that the activity of LIP neurons contributes to the maintenance of spatial constancy throughout the visual field.     

Ocular fixation and visual activity in the monkey lateral intraparietal area

The macaque lateral intraparietal area (LIP) has been implicated in visuospatial attention and saccade planning. Since area LIP also contains a representation of the central visual field, we investigated its possible role in fixation and foveal attention in a visual fixation task with gap (momentary disappearance of fixation point). In addition to the expected visual neurons ( n=119), two main categories were identified: (1) cells responding tonically both during the presence and momentary absence of the fixation stimulus( n=47); a subset of these neurons studied in a saccade task showed perisaccadic inhibition in half of the cases (14/27). The timing of this inhibition, however, is only loosely related to saccade timing; (2) cells responding mainly to the absence of the fixation stimulus, with either abrupt or gradual onset of activity during the gap ( n=62). During saccades, these neurons showed presaccadic buildup and/or postsaccadic activity, which was spatially tuned in about half of the tested cells (28/53). Ninety-one percent of the cells in the first category and 59% of the cells in the second category were located in the dorsal portion of area LIP (LIPd). These results are consistent with the hypothesis of an oculomotor-attentional network contributing to fixation engagement and disengagement in a subregion of LIP.     

Modulation of shifting receptive field activity in frontal eye field by visual salience

In the monkey frontal eye field (FEF), the sensitivity of some neurons to visual stimulation changes just before a saccade. Sensitivity shifts from the spatial location of its current receptive field (RF) to the location of that field after the saccade is completed (the future field, FF). These shifting RFs are thought to contribute to the stability of visual perception across saccades, and in this study we investigated whether the salience of the FF stimulus alters the magnitude of FF activity. We reduced the salience of the usually single flashed stimulus by adding other visual stimuli. We isolated 171 neurons in the FEF of 2 monkeys and did experiments on 50 that had FF activity. In 30% of these, that activity was higher before salience was reduced by adding stimuli. The mean magnitude reduction was 16%. We then determined whether the shifting RFs were more frequent in the central visual field, which would be expected if vision across saccades were only stabilized for the visual field near the fovea. We found no evidence of any skewing of the frequency of shifting receptive fields (or the effects of salience) toward the central visual field. We conclude that the salience of the FF stimulus makes a substantial contribution to the magnitude of FF activity in FEF. In so far as FF activity contributes to visual stability, the salience of the stimulus is probably more important than the region of the visual field in which it falls for determining which objects remain perceptually stable across saccades.     

Visual responses with and without fixation: neurons in premotor cortex encode spatial locations independently of eye position

 The ventral premotor cortex (PMv) of the macaque monkey contains neurons that respond both to visual and to tactile stimuli. For almost all of these “bimodal” cells, the visual receptive field is anchored to the tactile receptive field on the head or the arms, and remains stationary when the eyes fixate different locations. This study compared the responses of bimodal PMv neurons to a visual stimulus when the monkey was required to fixate a spot of light and when no fixation was required. Even when the monkey was not fixating and the eyes were moving, the visual receptive fields remained in the same location, near the associated tactile receptive field. For many of the neurons, the response to the visual stimulus was significantly larger when the monkey was not performing the fixation task. In control tests, the presence or absence of the fixation spot itself had little or no effect on the response to the visual stimulus. These results show that even when the monkey’s eye position is continuously changing, the neurons in PMv have visual receptive fields that are stable and fixed to the relevant body part. The reduction in response during fixation may reflect a shift of attention from the visual stimulus to the demands of the fixation task. Received: 8 April 1997 / Accepted: 16 July 1997     

Neurons in the lateral intraparietal area create a priority map by the combination of disparate signals

Primates search for objects in the visual field with eye movements. We recorded the activity of neurons in the lateral intraparietal area (LIP) in animals performing a visual search task in which they were free to move their eyes, and reported the results of the search with a hand movement. We distinguished three independent signals: (1) a visual signal describing the abrupt onset of a visual stimulus in the receptive field; (2) a saccadic signal predicting the monkey’s saccadic reaction time independently of the nature of the stimulus; (3) a cognitive signal distinguishing between the search target and a distractor independently of the direction of the impending saccade. The cognitive signal became significant on average 27 ms after the saccadic signal but before the saccade was made. The three signals summed in a manner discernable at the level of the single neuron. A.E. Ipata and A.L. Gee have contributed equally to this work.     

The dorsomedial frontal cortex of the macaca monkey: fixation and saccade-related activity

Summary The activity of 249 neurons in the dorsomedial frontal cortex was studied in two macaque monkeys. The animals were trained to release a bar when a visual stimulus changed color in order to receive reward. An acoustic cue signaled the start of a series of trials to the animal, which was then free to begin each trial at will. The monkeys tended to fixate the visual stimuli and to make saccades when the stimuli moved. The monkeys were neither rewarded for making proper eye movements nor punished for making extraneous ones. We found neurons whose discharge was related to various movements including those of the eye, neck, and arm. In this report, we describe the properties of neurons that showed activity related to visual fixation and saccadic eye movement. Fixation neurons discharged during active fixation with the eye in a given position in the orbit, but did not discharge when the eye occupied the same orbital positions during nonactive fixation. These neurons showed neither a classic nor a complex visual receptive field, nor a foveal receptive visual field. Electrical stimulation at the site of the fixation neurons often drove the eye to the orbital position associated with maximal activity of the cell. Several different kinds of neurons were found to discharge before saccades: 1) checking-saccade neurons, which discharged when the monkeys made self-generated saccades to extinguish LED's; 2) novelty-detection saccade neurons, which discharged before the first saccade made to a new visual target but whose activity waned with successive presentations of the same target. These results suggest that the dorsomedial frontal cortex is involved in attentive fixation. We hypothesize that the fixation neurons may be involved in codifying the saccade toward a target. We propose that their involvement in arm-eye-head motor-planning rests primarily in targeting the goal of the movement. The fact that saccaderelated neurons discharge when the saccades are self initiated, implies that this area of the cortex may share the control of voluntary saccades with the frontal eye fields and that the activation is involved in intentional motor processes.     

Neural correlates of attention and distractibility in the lateral intraparietal area

We examined the activity of neurons in the lateral intraparietal area (LIP) during a task in which we measured attention in the monkey, using an advantage in contrast sensitivity as our definition of attention. The animals planned a memory-guided saccade but made or canceled it depending on the orientation of a briefly flashed probe stimulus. We measured the monkeys' contrast sensitivity by varying the contrast of the probe. Both subjects had better thresholds at the goal of the saccade than elsewhere. If a task-irrelevant distractor flashed elsewhere in the visual field, the attentional advantage transiently shifted to that site. The population response in LIP correlated with the allocation of attention; the attentional advantage lay at the location in the visual field whose representation in LIP had the greatest activity when the probe appeared. During a brief period in which there were two equally active regions in LIP, there was no attentional advantage at either location. This time, the crossing point, differed in the two animals, proving a strong correlation between the activity and behavior. The crossing point of each neuron depended on the relationship of three parameters: the visual response to the distractor, the saccade-related delay activity, and the rate of decay of the transient response to the distractor. Thus the time at which attention lingers on a distractor is set by the mechanism underlying these three biophysical properties. Finally, we showed that for a brief time LIP neurons showed a stronger response to signal canceling the planned saccade than to the confirmation signal.     

Direction selectivity of neurons in the macaque lateral intraparietal area

The lateral intraparietal area (LIP) of the macaque is believed to play a role in the allocation of attention and the plan to make saccadic eye movements. Many studies have shown that LIP neurons generally encode the static spatial location demarked by the receptive field (RF). LIP neurons might also provide information about the features of visual stimuli within the RF. For example, LIP receives input from cortical areas in the dorsal visual pathway that contain many direction-selective neurons. Here we examine direction selectivity of LIP neurons. Animals were only required to fixate while motion stimuli appeared in the RF. To avoid spatial confounds, the motion stimuli were patches of randomly arrayed dots that moved with 100% coherence in eight different directions. We found that the majority (61%) of LIP neurons were direction selective. The direction tuning was fairly broad, with a median direction-tuning bandwidth of 136 degrees. The average strength of direction selectivity was weaker in LIP than that of other areas of the dorsal visual stream but that difference may be because of the fact that LIP neurons showed a tonic offset in firing whenever a visual stimulus was in the RF, independent of direction. Direction-selective neurons do not seem to constitute a functionally distinct subdivision within LIP, because those neurons had robust, sustained delay-period activity during a memory delayed saccade task. The direction selectivity could also not be explained by asymmetries in the spatial RF, in the hypothetical case that the animals attended to slightly different locations depending on the direction of motion in the RF. Our results show that direction selectivity is a distinct attribute of LIP neurons in addition to spatial encoding.     

Responses to auditory stimuli in macaque lateral intraparietal area. II. Behavioral modulation.

The lateral intraparietal area (LIP), a region of posterior parietal cortex, was once thought to be unresponsive to auditory stimulation. However, recent reports have indicated that neurons in area LIP respond to auditory stimuli during an auditory-saccade task. To what extent are auditory responses in area LIP dependent on the performance of an auditory-saccade task? To address this question, recordings were made from 160 LIP neurons in two monkeys while the animals performed auditory and visual memory-saccade and fixation tasks. Responses to auditory stimuli were significantly stronger during the memory-saccade task than during the fixation task, whereas responses to visual stimuli were not. Moreover, neurons responsive to auditory stimuli tended also to be visually responsive and to exhibit delay or saccade activity in the memory-saccade task. These results indicate that, in general, auditory responses in area LIP are modulated by behavioral context, are associated with visual responses, and are predictive of delay or saccade activity. Responses to auditory stimuli in area LIP may therefore be best interpreted as supramodal responses, and similar in nature to the delay activity, rather than as modality-specific sensory responses. The apparent link between auditory activity and oculomotor behavior suggests that the behavioral modulation of responses to auditory stimuli in area LIP reflects the selection of auditory stimuli as targets for eye movements.