Center for Neural Science, New York University, New York 10003
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ABSTRACT |
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Platt, Michael L. and Paul W. Glimcher. Responses of intraparietal neurons to saccadic targets and visual distractors. J. Neurophysiol. 78: 1574-1589, 1997. Current evidence suggests that neuronal activity in the lateral intraparietal area (LIP) reflects sensory-motor processes, but it remains unclear whether LIP activation participates directly in the planning of future eye movements or encodes data about both sensory events and the behavioral significance of those sensory events. To examine this issue, 31 intraparietal neurons were studied in awake, behaving monkeys trained to perform two tasks that independently controlled the location of a saccadic target and the location and behavioral relevance of a visual distractor. In both of these tasks, two eccentric light-emitting diodes (LEDs) were illuminated yellow, one above and one below a fixation stimulus. Shortly after the eccentric LEDs were illuminated, a change in the color of the fixation stimulus indicated which of these LEDs served as the saccadic goal and which served as a visual distractor. In the first or distractor-irrelevant task, fixation offset indicated that the subject must initiate a saccade shifting gaze to the saccadic goal. In the second or distractor-relevant task, distractor offset served as the saccade initiation cue. Intraparietal neurons responded more strongly in association with an LED that served as a saccadic target than in association with the same LED when it served as a visual distractor. Neuronal responses in association with either target or distractor stimuli on distractor-relevant and distractor-irrelevant blocks of trials were statistically indistinguishable. When the location of either the target or the distractor was varied across trials, the response of each neuron in association with a particular stimulus location was always greater for targets than for distractors and the magnitude of this response difference was independent of distractor relevance; however, distractors were nearly always associated with some intraparietal neuronal activity. A target/distractor selectivity index was computed for each neuron as the difference between responses associated with targets minus responses associated with distractors divided by the sum of these values. When the selectivity of each neuron on the distractor-relevant task was plotted against the selectivity of the same neuron on the distractor-irrelevant task, activity in the population of intraparietal neurons was found to be independent of distractor relevance. These data suggest that LIP neuronal activation represents saccadic targets and, at a lower level of activity, visual distractors, but does not encode the relevance of distractor stimuli on these tasks.
Several covert psychological processes have been postulated to participate in the cascade of neural events that begins with the transduction of a visual stimulus and ends with an eye movement. For example, coordinate transformations, which shift signals gathered by the sensory epithelium into coordinate systems appropriate for the guidance of movement, have been identified as processes that intervene between sensation and action (cf. Gnadt and Andersen 1988 Two juvenile male rhesus macaques (Macaca mulatta) served as subjects in the following experiments. All animal procedures were developed in association with the University Veterinarian and these procedures were approved by the New York University Institutional Animal Care and Use Committee. These procedures were designed and conducted in compliance with the Public Health Service's Guide for the Care and Use of Animals.
Surgical and training procedures
In an initial sterile surgical procedure performed under isoflurane and nitrous oxide inhalant anesthesia, a head restraint prosthesis and scleral search coil (Fuchs and Robinson 1966 Microelectrode recording techniques
Before each experimental recording session, the stainless steel receptacle was opened under aseptic conditions and flushed repeatedly with sterile saline, and then an X-Y micropositioner (Crist Instruments) and hydraulic microdrive (Kopf) were mounted to the receptacle. A 23-gauge hypodermic tube, into which was withdrawn a tungsten steel 6- to 8-M Behavioral techniques
To ascertain whether intraparietal neurons encode the behavioral relevance of an eccentric visual stimulus when the metrics of a reinforced saccade have been specified by a second eccentric visual stimulus, we used a two-part process to study each cell. First, we measured the basic response properties of each neuron as a function of target location/movement metrics with the use of a delayed saccade task. After this basic analysis was completed, each neuron was studied with a pair of tasks that presented animals with two eccentric visual stimuli, one of which would be identified as the eventual saccadic goal and the other as a visual distractor. In the cued saccade task, offset of the fixation stimulus cued the animal to initiate a movement that shifted gaze into alignment with the specified saccadic goal an unpredictable time after the saccadic goal was identified to receive reinforcement. In the distributed cue task, offset of the distractor stimulus provided the saccade initiation cue. Data collected on cued saccade and distributed cue trials were compared to determine whether the neuron under study responded differentially when the behavioral relevance of the visual distractor was altered.
DELAYED SACCADE TASK.
Delayed saccade trials (Fig. 1A) were used to assess the spatial tuning of physiologically identified intraparietal neurons. Each trial began with the illumination of a central yellow LED that subjects were required to fixate within 1,000 ms. Two hundred to 800 ms after gaze was aligned within 3° of the fixation stimulus, a single eccentric yellow LED was illuminated. After a further 200- to 800-ms delay, the fixation stimulus was extinguished, cueing the subject to shift gaze to the eccentric target (±6°) within 350 ms to receive a reinforcer.
CUED SACCADE TASK.
These trials (Fig. 1B) began with the illumination of a central yellow fixation LED to which subjects were required to direct gaze (±3°) within 1,000 ms. After a variable fixation interval of 200-800 ms, two eccentric yellow LEDs were coilluminated (200-800 ms), one above and one below the fixation stimulus. The saccadic goal, however, was not specified until the fixation stimulus changed color to either red or green. A change to red indicated that eventually a saccade that shifted gaze to the upper eccentric LED would be rewarded and that the lower eccentric LED was an irrelevant visual distractor. A change to green identified the lower eccentric LED as the saccadic target and the upper eccentric LED as an irrelevant visual distractor. Subjects were required to withhold the cued saccade for 200-800 ms. After this delay, the fixation LED was extinguished, indicating that the subject should direct gaze to the location of the cued target (±6°) within 500 ms to receive a reinforcer.1 The precise target and distractor locations and the color of the fixation stimulus were varied randomly from trial to trial.
DISTRIBUTED CUE TASK.
Although the cued saccade task enabled us to assess whether LIP neurons responded differentially to targets and distractors, it alone could not determine the effects of altering the behavioral relevance of nontarget stimuli (distractors) on the firing patterns of LIP neurons. To examine whether LIP neurons encode the behavioral relevance of distractors, we employed the distributed cue task. This task (Fig. 1C) was identical to the cued saccade task except that the offset of the visual distractor, rather than the offset of the fixation stimulus, cued the subject to initiate a saccade shifting gaze to the location of the specified saccadic goal. Thus a change in the color of the fixation stimulus to red specified that the upper eccentric LED would be the eventual target of the saccade and that the offset of the lower eccentric LED would provide the cue to initiate the required saccade. Similarly, a change in the color of the fixation stimulus to green specified that the lower eccentric LED would be the eventual saccadic goal and that the offset of the upper eccentric LED would indicate the time at which the required saccade must be initiated. After the offset of the distractor LED, the subject was required to redirect gaze into alignment with the cued target LED (±6°) within 750 ms to receive a reinforcement.2
Recording protocol
Electrodes were lowered, under physiological guidance, until units with visual and/or saccade-associated activity were encountered. Most penetrations were made so that electrodes first passed through tissue containing neurons with skeletomuscular related activity, presumably located in Brodmann's area 5 and therefore dorsal to area LIP. This increased the probability that subsequently encountered visual or saccade-related neurons were located in area LIP and not in area 7a (cf. Barash et al. 1991a Single-trial analysis
We compared reinforced single cued saccade trials in which the locations of the eccentric LEDs were the same but the color of the fixation LED was different. Because these trials used displays that differed only in the color of the fixation LED, which was outside the response field of the neuron, changes in neuronal activity could be attributed to whether the variable eccentric LED served as a saccadic target or a visual distractor. This attribution could be strengthened by comparing delayed saccade trials and cued saccade trials that shared a common eccentric LED as the saccadic goal. If the responses of a neuron on delayed saccade trials were similar to those elicited by cued saccade trials with the same saccadic target, it could be inferred that the neuron encoded some saccade-associated aspect of the task and not simply the color of the fixation LED.
Target and distractor field analysis
Comparison of single trials can provide qualitative evidence about relative neuronal responses to a particular pair of eccentric LEDs, but it provides neither quantitative data regarding the effects of the spatial location of LEDs identified as targets and distractors nor estimates of average LIP neuronal responses to a particular stimulus/movement configuration. To provide systematic, quantitative analyses of the effects of varying the locations of target and distractor LEDs on LIP neuronal activity, we subjected the trials recorded from each neuron to a two-stage analysis.
Statistical analysis of target/distractor selectivity
Although generating target and distractor fields permits us to assess whether intraparietal neurons respond differentially to LEDs identified as targets and distractors, it does not provide a quantitative measure of this discrimination. To quantify the differential activation of intraparietal neurons by the variable LED when it served as a target versus when that same LED served as a distractor, a measure of target/distractor selectivity was calculated for trials during which either the target or the distractor was located within the center of the response field of each unit. To accomplish this, the spatial tuning of each intraparietal neuron was estimated by fitting a Cartesian two-dimensional Gaussian model to the combined target and distractor data sets measured for each cell during each interval (Gnadt and Breznen 1996 Effects of distractor relevance
Although selectivity indexes provide an estimate of intraparietal neuronal target selectivity on each task, they cannot provide a direct estimate of the effects of altering the relevance of the distractor on the selectivity of a particular neuron. To determine whether individual LIP neurons represent stimuli differently when distractor relevance is altered, selectivity ratios computed from distributed cue trials for each neuron during each interval were plotted as a function of selectivity on cued saccade trials for that same neuron during that same interval. If intraparietal neurons did not alter their responses to distractors when distractor relevance was changed, then a graph of distributed cue task selectivity as a function of cued saccade task selectivity would describe a diagonal line passing through the origin and having a slope of 1. If intraparietal neurons were more strongly activated by distractors that cued movement initiation than by irrelevant distractors, then selectivity should be lower on distributed cue trials than on cued saccade trials, and the points on a bivariate plot of selectivity would fall below the line having a slope of 1. Thus, by generating a two-dimensional plot of selectivity on distributed cue trials as a function of selectivity on cued saccade trials, we can determine whether, on our tasks, intraparietal neurons encoded the behavioral significance of distractor stimuli that did not serve as saccadic goals.
Single-trial data
Thirty-one intraparietal neurons with saccade-associated activity were examined while subjects were presented with a minimum of 100 cued saccade trials and 100 distributed cue trials. The mean number of cued saccade trials performed correctly was 245 ± 57 (SD) (minimum = 103; maximum = 398). The mean number of correctly executed distributed cue trials was 278 ± 96 (SD) (minimum = 91; maximum = 584).
Target and distractor fields
The trials presented in Figs. 2-5 suggest that the neurons in our sample did not discriminate relevant from irrelevant distractors in our tasks. These results further indicate that distractors of both types were represented by our parietal population. Single trials, however, cannot tell us how intraparietal neuronal activity varies as a function of the spatial position of the target or distractor, nor can they provide a sense of the mean response of the neuron on many similar trials. To provide that information, we generated three target fields and three distractor fields for each neuron from both the cued saccade and distributed cue sets of trials.
Population data
To quantify the relative responses of each neuron to targets and distractors across trials, we computed the average response of the neuron on all trials on which either the target or the distractor was located within ±1 horizontal SD and ±1 vertical SD of the center of the response field (see METHODS). Figure 10 plots the population mean ± SE of the average neuronal response in association with targets(
An examination of reinforced cued saccade trials indicated that intraparietal neurons responded more strongly in association with an appropriately placed LED when it was identified as the saccadic goal than when the same LED was identified as an irrelevant visual distractor. Comparison of distributed cue trials with cued saccade trials on which the same LEDs were identified as distractors showed that intraparietal neurons did not become more strongly activated when distractor offset cued movement initiation than when the same LED was completely irrelevant to the task.
Comparison with previous studies
Previous studies that have attempted to relate LIP neuronal responses to attention typically employed tasks that presented subjects with only one eccentric visual stimulus, which was either completely irrelevant or provided information that the subject could use to obtain a reward (cf. Goldberg et al. 1990 Summary
Our data suggest that when an animal is presented with two eccentric visual stimuli, two populations of LIP neurons become active, one activated in association with each of the two eccentric LED locations or with each of two simultaneously planned movements guided by these stimuli. After one of these LEDs has been identified as a saccadic goal, the population of LIP neurons associated with the target stimulus, or the movement it specifies, responds more strongly than the population of neurons associated with the irrelevant distractor. In the tasks examined here, this target-over-distractor selectivity was unaffected by changes in distractor relevance. These data provide some evidence in support of the hypothesis (Bracewell et al. 1996
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Hallett and Lightstone 1976
; Mays and Sparks 1980
). The explicit planning of an eye movement for future execution also has been proposed as a neurobiologically separable element in the sensory-motor process (Glimcher and Sparks 1993
; Gnadt and Andersen 1988
). It has even been argued that the psychological process of selective attention, which is presumed to participate in sensory-motor processing, might be observable at the single-neuron level as sensory responses that are modulated by the relevance of saccade-related stimuli (Bushnell et al. 1981
; Goldberg and Wurtz 1972
; Goldberg et al. 1990
; Robinson et al. 1978
; Wurtz and Mohler 1976
).
; Goldberg et al. 1990
; Shadlen and Newsome 1996
). LIP receives direct projections from multiple extrastriate visual areas (Andersen et al. 1990
; Blatt et al. 1990
) and projects directly to principal oculomotor control areas in the frontal eye fields and the superior colliculus (Andersen et al. 1985
, 1990
; Cavada and Goldman-Rakic 1989a
,b
; May and Andersen 1986
). LIP thus seems appropriately situated anatomically to intervene between sensation and action in the generation of saccades guided by visual targets.
were among the first to suggest that neurons in area LIP participate in a specific covert presaccadic process. In a series of studies (Andersen et al. 1990
; Barash et al. 1991a
,b
; Bracewell et al. 1996
; Gnadt and Andersen 1988
; Mazzoni et al. 1996
), these investigators and colleagues examined the activity of single neurons while monkeys made saccades that shifted gaze into alignment with the locations of previously viewed targets. Gnadt and Andersen (1988)
demonstrated that most neurons in area LIP responded strongly before saccadic eye movements having a limited range of amplitudes and directions. Further, these authors found that for many cells in area LIP an increase in firing rate that was correlated with the onset of an eccentric visual target was maintained after target offset if a gaze shift to the eccentric location was required. Because this activity accurately predicted the amplitude and direction of a future saccade and was maintained in the absence of the visual stimulus, these authors suggested that neurons in LIP might encode the metrics of planned future movements.
; Gnadt and Andersen 1988
; Mazzoni et al. 1996
). These studies employed a double-saccade task (cf. Hallett and Lightstone 1976
; Mays and Sparks 1980
) in which subjects were required to make two saccades that sequentially fixated two briefly flashed visual targets. In one of these studies, Mazzoni et al. (1996)
arranged the targets so that one stimulus was illuminated within and the other outside of the response field of the neuron under study. By varying the sequence in which the two targets were presented, Mazzoni et al. could compare the responses of LIP neurons on trials in which the first saccade was directed toward the response field with trials in which the first saccade was directed away from the response field. The authors reported that most (77%) LIP neurons were more strongly activated when the first saccade was directed toward the response field than when the first saccade was directed away from the response field, even though a visual stimulus had appeared within the response field in both conditions. These data led the authors to suggest that most LIP neurons encoded the direction and amplitude of the next saccade the animal intended to make, although it was noted that in a minority of LIP neurons (16%) the neural response was identical for either saccade.
designed a task in which subjects were instructed to plan a movement for future execution and then, on occasion, to change that plan before the movement was executed. While a monkey maintained fixation of a central stimulus a target was flashed briefly at an eccentric location. If the central target was extinguished, the subject was rewarded for shifting gaze to the eccentric target location. If, however, a second eccentric target was briefly presented, then, on fixation stimulus offset, the animal was rewarded for making a saccade that shifted gaze into alignment with this second target. Thus a subject could be sequentially instructed to prepare saccades of different metrics simply by illuminating multiple eccentric visual targets in series. Bracewell et al. determined that most LIP neurons responded with maintained activation after the presentation of a target placed at the center of the neuronal response field but became inactive as soon as a new saccadic target was flashed at a location outside of the neuronal response field. From these data, Bracewell et al. concluded that the activity of most LIP neurons principally signals the intention of an animal to generate saccades having a limited range of directions and amplitudes.
). In the experiments of Gnadt and Andersen (1988)
, the single light-emitting diode (LED) that served as both the visual stimulus and the saccadic target was also the only behaviorally relevant eccentric visual stimulus. Thus neurons may have responded after the onset of the saccadic target because it was a behaviorally meaningful stimulus or because it specified the metrics of a future saccade. Even in the experiments of Bracewell et al. (1996)
, LIP neurons may have signaled the relevance to the animal of each sequentially illuminated stimulus rather than the actual metrics of a planned movement. Similarly, in the experiments of Goldberg et al. (1990)
, LIP neurons may have represented the metrics of saccades that the animal planned but never produced, just as many LIP neurons in the study by Bracewell et al. (1996)
responded for saccades that were instructed but never executed.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
) were implanted. First, the rostral dorsum of the skull was exposed and four 2.5-mm holes were drilled through the skull with standard orthopedic surgical instruments. These holes were then tapped for 3.5-mm fine-thread orthopedic cortical bone screws. Four titanium screws (Zimmer) were inserted into the tapped holes and a custom-fabricated titanium bar was lowered to just above the skull surface between these screws. The restraint bar and the four screws were then bonded together with sterile orthopedic bone cement (Smith and Nephew: Palacos). The Teflon-insulated stainless steel scleral search coil was implanted underneath the conjunctiva, passing just rostral to the insertions of the extraocular muscles (Judge et al. 1980
). The search coil wire exited the conjunctiva temporally, formed a subdermic stress-relief loop just inside the temporal bone of the orbit, exited the orbit subdermically, passed through the temporalis muscle, and then passed through the bone cement that formed the restraint prosthesis, terminating in a gold and plastic electrical connector. After surgery, animals received analgesics for a minimum of 3 days. Antibiotic prophylaxis was initiated intraoperatively and continued for a minimum of 3 days.
electrode (Frederick Haer), was used to puncture the intact dura. Electrophysiological signals were amplified and band-pass filtered to exclude both power line noise and the signals of the magnetic fields (passband ~200-5,000 Hz). Individual action potentials were identified in hardware by time and amplitude criteria. Times of spike occurrence were recorded by computer with the use of a 1-µs internal clock.
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FIG. 1.
A: delayed saccade trials began with onset of centrally located fixation light-emitting diode (LED). Subjects had 1,000 ms to align gaze with this stimulus, after which eccentric LED (T1) was illuminated. After 200-800 ms, fixation stimulus was extinguished and animals had 500 ms to shift gaze from alignment with now-extinguished fixation position into alignment with eccentric target. B: cued saccade trials began with illumination of central yellow fixation stimulus with which subjects aligned gaze within 1,000 ms. After delay of 200-800 ms, 2 eccentric LEDs (T1 and T2) were coilluminated yellow, 1 above and 1 below fixation. After 2nd delay of 200-800 ms, fixation stimulus changed color to either red or green. Change to red identified upper eccentric LED as saccadic goal and lower eccentric LED as irrelevant distractor; change to green identified lower eccentric LED as saccadic goal and upper eccentric LED as irrelevant distractor. After final delay of 200-800 ms, fixation stimulus was extinguished and subjects had 500 ms to shift gaze into alignment with eccentric LED specified by color of extinguished fixation LED. C: distributed cue trials began with onset of centrally located yellow fixation LED, with which subjects had 1,000 ms to align gaze. After delay of 200-800 ms, 2 eccentric LEDs were coilluminated yellow, 1 above and 1 below horizontal meridian. After 2nd delay of 200-800 ms, fixation stimulus changed color to either red, identifying upper eccentric LED as saccadic target and lower eccentric LED as distractor, or green, identifying lower eccentric LED as saccadic target and upper eccentric LED as distractor. After final delay of 200-800 ms, eccentric LED identified as distractor by color of fixation LED was extinguished and animals had 750 ms to shift gaze into alignment with saccadic target.
,b
). When penetrations did not pass through area 5, neurons with vigorous visual/saccade-associated activity could be recorded for up to 8 mm, presumably because the electrode was traveling parallel to the surface of the cortical sheet within the lateral intraparietal sulcus. Because the electrode guide tube was constructed to penetrate 2-3 mm into cortex, neurons with visual/saccade-associated activity in the gyral portion of area 7a were probably not encountered. On the basis of the physiological characteristics and relative depths of recorded neurons, the lateral border of area 5 and the medial and lateral borders of area LIP were drawn on a map of the recording chamber grid. Neurons with visual/saccade-associated activity lying ventral to area 5 or located lateral to the border of the intraparietal sulcus were considered to lie in area LIP. Neurons located within this physiologically identified area LIP typically fired action potentials before visually guided saccades having a limited range of amplitudes and directions. Moreover, many of these neurons fired action potentials during the delay period on memory saccade trials for saccades having a similar range of metrics, as has been documented previously for LIP neurons (cf. Barash et al. 1991b
; Gnadt and Andersen 1988
).
). The Gaussian model had six free parameters: horizontal and vertical position of the center, horizontal and vertical SDs, baseline firing rate, and peak amplitude. The model was constrained so that the center of the Gaussian lay within ±40° of the plot origin (the location of the fixation LED).
Mean Distractor Response)/(Mean Target Response + Mean Distractor Response). In principle, the minimum selectivity was
1, indicating that the neuron under study responded infinitely more strongly for distractors than for targets located within the estimated center of the response field. The theoretical maximum selectivity was +1, indicating that the neuron under study was activated infinitely more strongly for targets than for distractors located within the center of the estimated response field. A selectivity of 0 indicated that the unit under study responded equally to targets and distractors. Selectivity ratios were compared across visual, cue, and premovement intervals to determine whether intraparietal neurons discriminated between stimuli that would eventually serve as saccadic targets and those that would eventually serve as distractors, and if so, whether this discrimination was associated with any trial events.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
2,4) and (0,
10), respectively. Figure 2, A and C, left, each plot the horizontal and vertical position of the eye above an instantaneous frequency histogram of neuronal activity for a single trial. Arrows below the time axis identify events during the trial. The first arrow indicates the onset of the eccentric LEDs, the second arrow indicates the change in the color of the fixation stimulus, and the third arrow indicates the offset of the fixation stimulus. Figure 2, A and C, right, plot the point of gaze at successive 2-ms intervals during each trial. The disk shaded in dark gray identifies the boundaries of the response field at ±1 SD from the center as estimated by the sigma parameters of the Gaussian model for this cell (see METHODS).
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FIG. 2.
Responses of single intraparietal neuron (unit HX951128) during 12 single cued saccade trials. In A and C, horizontal and vertical eye position are plotted as functions of time above instantaneous frequency histogram for 2 single trials. The 3 arrows under each histogram indicate, respectively, time of onset of eccentric LEDs (Targets), change in color of fixation LED (Cue), and offset of fixation LED (Go). In C, light gray box highlights cue interval for comparison with Fig. 3C. Right: point of gaze is plotted every 2 ms. Dark gray disk: center of response field (±1 horizontal and ±1 vertical SD) of neuron estimated by 2-dimensional Gaussian fit to combined cued saccade and distributed cue data. In A, fixation stimulus changed color to red, identifying upper eccentric LED (located 2° to left and 4° upward from fixation stimulus) as saccadic target and lower eccentric LED (located 10° straight down from fixation stimulus) as irrelevant distractor. In C, fixation stimulus changed color to green, identifying lower eccentric LED as saccadic target and upper eccentric LED as irrelevant distractor. Below single trial presented in A, B plots spike rasters for 5 additional trials on which target was located within ±1 horizontal and ±1 vertical SD of center of response field. In all spike raster plots, T indicates onset of eccentric LEDs, C indicates time at which fixation stimulus changed color, G indicates offset of fixation stimulus, and S indicates saccade onset. Below single trial presented in C, D plots spike rasters for 5 additional trials on which distractor was located within ±1 horizontal and ±1 vertical SD of response field center. Note that on all 12 trials, neuron responded briskly after presentation of 2 eccentric LEDs and continued to respond at high frequency when color of fixation stimulus cued movement that aligned gaze with upper eccentric LED (A and B); when color of fixation stimulus cued movement that would align gaze with lower eccentric LED (C and D), however, neuron responded at diminished frequency.
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FIG. 3.
Responses of single intraparietal neuron (HX951128) on 12 distributed cue trials. Go: offset of distractor LED. For single trials presented in A and C, eccentric LEDs were located in same positions as on trials presented in Fig. 2, A and C. Below single trial presented in A, B presents spike rasters for 5 additional trials on which target was located within ±1 horizontal and ±1 vertical SD of center of neuronal response field. Beneath single trial presented in C, D presents spike rasters for 5 additional trials on which distractor was located within ±1 horizontal and ±1 vertical SD of center of neuronal response field. As in Fig. 2, neuron responded strongly after presentation of 2 eccentric LEDs and continued to respond when color of fixation stimulus cued movement that would align gaze with upper eccentric LED (A and B); when color of fixation stimulus cued movement that would align gaze with lower eccentric LED, neuron responded at reduced frequency (C and D). Note that neuronal activity during cue interval (light gray box) was largely identical in Figs. 2C and 3C.
10,
10). One eccentric LED was positioned in the center of the neuronal response field (indicated by the dark gray ellipses at right), whereas the other was located in the lower left visual hemifield, where it elicited no increased response from the cell on delayed saccade trials. The two trials presented in Fig. 4, A and C, differed visually only in the color of the fixation stimulus: in A, a change in the color of the fixation stimulus to red (at the time-marked cue) indicated that the upper eccentric LED would be the saccadic goal, whereas in C a change in the color of the fixation stimulus to green indicated that the upper eccentric LED would be an irrelevant distractor. In A, the neuronal response became elevated after a change in the color of the fixation stimulus indicated that the upper LED would be the saccadic goal. In contrast, when the same LED was specified as an irrelevant distractor in C, the neuron was only weakly activated.
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FIG. 4.
Responses of single intraparietal neuron (unit YY960305) on 12 cued saccade trials. For single trials presented in A and C, eccentric LEDs were located at (10,8) and ( 10,
10), respectively. In A, color of fixation LED changed from yellow to red, indicating that animal would be rewarded for shifting gaze into alignment with upper eccentric LED. In C, color of fixation LED changed from yellow to green, identifying lower eccentric LED as saccadic goal. Below single trial presented in A, B presents spike rasters for 5 additional trials on which target was located within ±1 horizontal and ±1 vertical SD of center of neuronal response field (indicated by dark gray ellipse in point-of-gaze plot on right). Neuron responded with increase in activity when cue identified upper LED as saccadic goal (A and B) but fired at reduced rate when cue identified lower LED as saccadic goal (C and D).
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FIG. 5.
Responses of single intraparietal neuron (unit YY960305) on 12 distributed cue trials. On trials presented in A and C, 2 eccentric LEDs were located in same positions as in Fig. 4, A and C. In A, cue identified upper eccentric LED as saccadic goal, whereas in C, cue identified lower eccentric LED as saccadic target. As in Fig. 4, neuron responded with increase in activity when cue identified upper eccentric LED as target (A and B) but responded with diminished activity after cue identified lower eccentric LED as target (C and D). Neuronal activity was approximately equal during cue interval (light gray box) in Figs. 4C and 5C, regardless of which task animal was performing.
10) while the location of the other eccentric LED varied within the upper hemifield from trial to trial. Figure 6A presents trials on which the eccentric LED that was fixed in the lower hemifield served as the distractor and on which the eccentric LED located in the upper hemifield served as the target. These graphs plot neuronal activity as a function of target position (in Cartesian degrees of visual angle relative to fixation) during the visual, cue, and premovement epochs. Figure 6B presents the trials on which the eccentric LED fixed in the lower hemifield served as the saccadic target and the variable upper hemifield LED served as the irrelevant distractor. In these graphs, neuronal activity is plotted as a function of the position of the distractor.
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FIG. 6.
Target and distractor fields from 194 cued saccade trials for unit HX951128. A: trials on which eccentric LED that varied in position was identified as saccadic target. B: trials on which variable eccentric LED was identified as irrelevant distractor. Data were averaged in 4 × 4° blocks and smoothed by interpolation (Axum). In A, firing rate is plotted as function of location of saccadic target. In B, firing rate is plotted as function of location of irrelevant distractor. Target and distractor fields are plotted for 3 time intervals: visual (200 ms from eccentric targets onset), cue (200 ms preceding fixation LED offset), and premovement (100 ms preceding saccade onset). Note that neuron responded briskly in association with both targets and distractors located within central upper hemifield during visual interval, but response for distractors became reduced during cue and premovement intervals (B). Maximum firing rate for surfaces: 32.0, 30.0, and 36 Hz (A); 38, 27.0, and 25 Hz (B). Mean firing rates within ±1 horizontal and ±1 vertical SD of center of neuronal response field: 26.8, 27.7, and 34.6 Hz (A); 31.6, 26.8, and 25 Hz (B). Spatial tuning radii (see METHODS): 3.6, 3.2, and 3.0° in visual, cue, and premovement intervals, respectively.
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FIG. 7.
Target and distractor fields computed from 91 distributed cue trials for unit HX951128. Note that neuronal response was similar during cue interval whether distractor was relevant (Fig. 7B) or irrelevant (Fig. 6B) to task. Maximum firing rate for surfaces: 32.0, 33.0, and 33 Hz (A); 32, 20, and 14 Hz (B). Mean firing rates within center of neuronal response field: 35.7, 30.7, and 50 Hz (A); 29, 21.6, and 12.2 Hz (B). Spatial tuning radii: 3.4, 3.0, and 1.6° during visual, cue, and premovement intervals, respectively.
10,
10) while the location of the other LED varied within the upper hemifield across trials. Target fields were constructed from trials on which the LED located within the upper hemifield was identified as the target, whereas distractor fields were constructed from trials on which the LED located in the upper hemifield was identified as a distractor. In contrast with the activity of the neuron presented in Figs. 6 and 7, this neuron was characterized by a tonic firing rate that was influenced only weakly by the initial presentation of the two eccentric visual stimuli. During the cue and premovement intervals, however, this neuron responded at an increased frequency in association with targets located in the upper right visual hemifield but responded weakly in association with distractors located in this same region. Note that the response of this neuron to distractors during the cue interval also appears not to depend on the relevance of the distractor.
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FIG. 8.
Target and distractor fields computed from 239 cued saccade trials for unit YY960305. Note that neuron responded when LEDs located in right upper hemifield were identified as saccadic targets but responded weakly when LEDs located in same region were identified as irrelevant distractors. Maximum firing rate for surfaces: 10.0, 17.0, and 19.0 Hz (A); 9.4, 10.2, and 9.5 Hz (B). Mean firing rates within center of neuronal response field: 10.8, 14.1, and 16.2 Hz (A); 10.5, 9.7, and 9.5 Hz (B). Spatial tuning radii: 10.8, 23.1, and 24.1° during visual, cue, and premovement intervals, respectively.
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FIG. 9.
Target and distractor fields computed from 275 distributed cue trials for unit YY960305. Note that ratio of target/distractor response was largely independent of whether visual distractor was relevant (Fig. 9) or irrelevant (Fig. 8). Maximum firing rate for surfaces: 13.0, 17.5, and 18.8 Hz (A); 12.2, 9.0, and 8.5 Hz (B). Mean firing rates within center of neuronal response field: 12.7, 13.7, and 14.6 Hz (A); 11.8, 8.1, and 7.6 Hz (B). Spatial tuning radii: 23.0, 15.4, and 24.8° during visual, cue, and premovement intervals, respectively.
) and distractors (- - -) located within the center of the response field for our population of 31 neurons during visual, cue, and premovement intervals on both cued saccade (
) and distributed cue (
) trials. The average neuronal response in association with targets and distractors was equivalent during the visual interval on both tasks. During the cue and premovement intervals, average responses increased in association with targets but decreased in association with distractors on both tasks. In a three-way analysis of variance, the main effect of target/distractor was significant (F = 22.12, df = 1, P < 0.00001), as was the interaction between target/distractor and task interval (F = 6.30, df = 13, P < 0.005). The average neuronal response, however, was unaffected by modulations in distractor relevance (F = 0.38, df = 1, P > 0.5).
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FIG. 10.
Population mean ± SE of neuronal response rate in association with targets ( ) and distractors (- - -) located within ±1 SD of center of each neuronal response field on both cued saccade (
) and distributed cue (
) trials during visual, cue, and premovement intervals. On cued saccade trials, mean firing rate differed significantly between visual and premovement intervals on target plot (t-test, P < 0.01) but showed no significant differences across intervals on distractor plot. Responses differed significantly between target and distractor trials during cue (P < 0.0001) and premovement (P < 0.0001) intervals. On distributed cue trials, mean firing rate differed significantly between visual and premovement intervals on both target plot (P < 0.01) and distractor plot (P < 0.05). Responses differed significantly between target and distractor trials during cue (P < 0.001) and premovement (P < 0.00001) intervals. Mean firing rate did not differ significantly between the 2 tasks (analysis of variance: F = 0.38, df = 1, P > 0.54).
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FIG. 11.
Average neuronal response rates in association with targets and distractors located within ±1 horizontal and ±1 vertical SD of center of neuronal response field during visual, cue, and premovement intervals for 10 randomly selected neurons on cued saccade (A) and distributed cue (B) trials. Solid lines connect responses of each neuron across intervals. Most neurons showed both target-associated increases and distractor-associated decreases in mean firing rate on both tasks.
0.01 ± 0.03 (SE). During the cue interval, the population was more active for targets than for irrelevant visual distractors (0.15, ± 0.03, mean ± SE), whereas during the premovement interval the population was even more selective for targets (0.21 ± 0.04,mean ± SE). The selectivity indexes for the cue and premovement intervals did not differ significantly by t-test (t =
1.16, df = 60, P > 0.25), but both were significantly different from the selectivity index calculated for the visual interval (cue: t = 5.51, df = 30, P < 0.001; premovement: t =
4.42, df = 60, P < 0.001).
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FIG. 12.
A: frequency histogram for selectivity indexes on cued saccade trials during visual, cue, and premovement epochs calculated for 31 intraparietal neurons. Selectivity index: +1 for neurons responding infinitely more for targets than for distractors, 1 for neurons responding infinitely more for distractors than for targets, 0 for neurons responding equally strongly for targets and distractors. Average selectivity: visual interval,
0.01 ± 0.03 (SE); cue interval, 0.15 ± 0.03 (SE); premovement interval, 0.21 ± 0.04 (SE). B: frequency histogram for selectivity indexes computed during distributed cue trials for 31 intraparietal neurons. Average selectivity: visual interval, 0.02 ± 0.02 (SE); cue interval, 0.14 ± 0.03 (SE); premovement interval, 0.27 ± 0.04 (SE).
2.48, df = 60, P < 0.02) and were significantly different from the selectivity index calculated for the visual interval (cue: t =
3.34, df = 60, P < 0.005; premovement: t =
5.62, df = 60, P < 0.00001).
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FIG. 13.
Two-dimensional plot of selectivity on cued saccade trials as function of selectivity on distributed cue trials for each of 31 intraparietal neurons. Solid diagonal line: expected distribution of neurons showing equivalent selectivity index on both trial types irrespective of relevance of visual distractor. Neurons showing increased response to relevant distractors would fall below line. Note that in A-C, selectivity of most neurons was nonnegative and largely independent of behavioral significance of distractor. In D, average neuronal selectivity (mean ± SE) is plotted during all 3 sequential time epochs. Average selectivity was near 0 on both tasks during visual interval, shifted up along main diagonal into 1st quadrant during cue interval, and shifted up above main diagonal during premovement interval.
) the average population selectivity index (mean ± SE on each axis) on each task during the three measured intervals. Notice that the average neuronal selectivity began near (0,0) in the visual interval, moved out along the main diagonal into the first quadrant during the cue interval, and peaked during the premovement interval, slightly above the main diagonal. The enhancement of neuronal selectivity during the premovement interval was due to a relative increase in the target representation on distributed cue trials (Fig. 10), whereas responses to distractors remained unchanged between the two tasks. Thus the response of the population during both the cue and premovement epochs was largely unaffected by whether the distractor was irrelevant or served as the movement initiation signal at the end of the cue epoch (t-test: visual interval: t =
0.88, df = 60, P > 0.38.; cue interval: t = 0.14, df = 60, P > 0.88; premovement interval: t =
1.07, df = 60, P > 0.29).
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). Alternatively, attempts to relate LIP responses to planned movement metrics presented subjects with a single visual stimulus that specified the metrics of a required saccade (cf. Gnadt and Andersen 1988
). Although these earlier studies suggested that LIP activity participated in some covert sensory-motor processes, significant uncertainty remains about whether LIP activity reflects the application of selective visual attention or simply represents the planning of an upcoming eye movement.
; Goldberg and Wurtz 1972
; Robinson et al. 1978
; Wurtz and Mohler 1976
) in the neuronal spike rate associated with relevant versus irrelevant distractors suggests that, on our tasks, intraparietal neuronal responses were more strongly correlated with the metrics of upcoming saccades than with the relevance of a stimulus to the subject, although appropriately placed distractors were almost always associated with some intraparietal activity.
). Of course we cannot exclude the possibility that LIP neurons respond to some manipulations of stimulus relevance but not to others and that our stimulus manipulation was simply not effective. If, as Goldberg et al. (1990)
have proposed, LIP neuronal activity reflects the attentional state of the animal, then only direct measures of attentional state made simultaneously with direct measures of neuronal state can completely resolve this issue.
).
) that most LIP neurons carry a signal that has been filtered by the specification of a saccadic goal but is insensitive to the behavioral significance of visual distractors, although these stimuli are almost always represented (Goldberg et al. 1990
).
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ACKNOWLEDGEMENTS |
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The authors thank H. Bayer for excellent assistance in data collection, L. O'Keefe for help in data analysis, A. Handel for helpful commentary on the manuscript, and J. Mones and H. Tamm for technical assistance.
This work was supported by a grant from the Whitehall Foundation and by National Eye Institute Grant EY-06595-03 to M. L. Platt.
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FOOTNOTES |
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1 In typical data sets, monkey YY (YY960305) made these responses with a mean latency of 137 ± 39 (SD) ms and monkey HX (HX951128) with a mean latency of 207 ± 119 (SD) ms. 2 In typical data sets, monkey YY (YY960305) made these responses with an average latency of 252 ± 128 (SD) ms and monkey HX (HX951128) with an average latency of 325 ± 250 (SD) ms.
Address for reprint requests: M. L. Platt, Center for Neural Science, New York University, 4 Washington Place, Room 809, New York, NY 10003.
Received 4 November 1996; accepted in final form 8 May 1997.
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REFERENCES |
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