Neurons with object-centered spatial selectivity in macaque SEF: do they represent locations or rules?

In macaque monkeys performing a task that requires eye movements to the leftmost or rightmost of two dots in a horizontal array, some neurons in the supplementary eye field (SEF) fire differentially according to which side of the array is the target regardless of the array's location on the screen. We refer to these neurons as exhibiting selectivity for object-centered location. This form of selectivity might arise from involvement of the neurons in either of two processes: representing the locations of targets or representing the rules by which targets are selected. To distinguish between these possibilities, we monitored neuronal activity in the SEF of two monkeys performing a task that required the selection of targets by either an object-centered spatial rule or a color rule. On each trial, a sample array consisting of two side-by-side dots appeared; then a cue flashed on one dot; then the display vanished and a delay ensued. Next a target array consisting of two side-by-side dots appeared at an unpredictable location and another delay ensued; finally the monkey had to make an eye movement to one of the target dots. On some trials, the monkey had to select the dot on the same side as the cue (right or left). On other trials, he had to select the target of the same color as the cue (red or green). Neuronal activity robustly encoded the object-centered locations first of the cue and then of the target regardless of the whether the monkey was following a rule based on object-centered location or color. Neuronal activity was at most weakly affected by the type of rule the monkey was following (object-centered-location or color) or by the color of the cue and target (red or green). On trials involving a color rule, neuronal activity was moderately enhanced when the cue and target appeared on opposite sides of their respective arrays. We conclude that the general function of SEF neurons selective for object-centered location is to represent where the cue and target are in their respective arrays rather than to represent the rule for target selection.     

Impact of experience on the representation of object-centered space in the macaque supplementary eye field

Many neurons in the macaque supplementary eye field (SEF) exhibit object-centered spatial selectivity, firing at different rates when the monkey plans a saccade to the left or right end of a horizontal bar. Is this property natural to the SEF or is it a product of specialized training in the laboratory? To answer this question, we monitored the activity of single SEF neurons in two monkeys before and after training to select eye-movement targets by an object-centered rule. During stage 1, the monkeys performed a color delayed-match-to-sample (DMS) task in which a red or green central cue dictated an eye movement to the matching end of a horizontal bar. Many neurons at this stage exhibited object-centered spatial selectivity. During stage 2, the monkeys performed a color-conditional object-centered task in which a green or red central cue instructed an eye movement to the left or right end of a gray bar. More neurons exhibited object-centered spatial selectivity during this stage than during stage 1. During stage 3, the monkeys again performed the color DMS task. The fraction of neurons exhibiting object-centered spatial selectivity remained at a level comparable to that observed during stage 2 and above that observed during stage 1. Thus object-centered spatial selectivity was present before training on an object-centered rule, was enhanced as a product of object-centered training, and outlasted active use of an object-centered rule. We conclude that neural representations of object-centered space, naturally present in the primate brain, can be sharpened by training.     

Neuronal activity in macaque SEF and ACC during performance of tasks involving conflict

It has been suggested on the basis of previous studies involving functional MRI (fMRI) and single-neuron recording that neurons of the supplementary eye field (SEF) and anterior cingulate cortex (ACC) monitor conflict. To test this idea, we carried out microelectrode recording in monkeys performing a color-conditional eye movement task in which red and green cues instructed leftward and rightward saccades, respectively. In a variant inducing conflict by spatial incompatibility, the cue was presented either at the location of the target (no conflict) or opposite the location of the target (conflict). In a variant inducing conflict by reversal, the foveal cue either remained one color (no conflict) or reversed color after 100 ms (conflict), with the monkey required to follow the instruction conveyed by the second color. In both tasks, conflict was evident in behavioral measures (reduced percent correct and slowed reaction time) and in physiological measures (reduced strength of directional activity among direction-selective neurons). In the SEF, there was a tendency for neurons to fire more strongly on trials involving conflict, but this effect took the form of modulation of task-related activity among direction-selective neurons, not of a pure conflict-monitoring signal. In the ACC, there was no conflict-related enhancement. These results are incompatible with the idea that the SEF and ACC contain populations of neurons specialized for monitoring conflict.     

Combination of neuronal signals representing object-centered location and saccade direction in macaque supplementary eye field

Neurons in the macaque supplementary eye field (SEF) fire at different rates in conjunction with planning saccades in different directions. They also exhibit object-centered spatial selectivity, firing at different rates when the target of the saccade is at the left or right end of a horizontal bar. To compare the rate of incidence of the two kinds of signal, and to determine how they combine, we recorded from SEF neurons while monkeys performed a task in which the target (a dot or the left or right end of a horizontal bar) could appear in any visual field quadrant. During the period when the target was visible on the screen and the monkey was preparing to make a saccade, many neurons exhibited selectivity for saccade direction, firing at a rate determined by the direction of the impending saccade irrespective of whether the target was a dot or the end of a bar. On bar trials, many of the same neurons exhibited object-centered selectivity, firing more strongly when the target was at the preferred end of the bar regardless of saccade direction. The rate of incidence of object-centered selectivity (33%) was lower overall than that of saccade-direction selectivity (56%). Signals related to saccade direction and the object-centered location of the target tended to combine additively. The results suggest that the SEF is at a transitional stage between representing the object-centered command and specifying the parameters of the saccade.     

Neuronal activity in macaque supplementary eye field during planning of saccades in response to pattern and spatial cues

The aim of this study was to determine whether neuronal activity in the macaque supplementary eye field (SEF) is influenced by the rule used for saccadic target selection. Two monkeys were trained to perform a variant of the memory-guided saccade task in which any of four visible dots (rightward, upward, leftward, and downward) could be the target. On each trial, the cue identifying the target was either a spot flashed in superimposition on the target (spatial condition) or a foveally presented digitized image associated with the target (pattern condition). Trials conforming to the two conditions were interleaved randomly. On recording from 439 SEF neurons, we found that two aspects of neuronal activity were influenced by the nature of the cue. 1) Activity reflecting the direction of the impending response developed more rapidly following spatial than following pattern cues. 2) Activity throughout the delay period tended to be higher following pattern than following spatial cues. We consider these findings in relation to the possible involvement of the SEF in processes underlying attention, arousal, response-selection, and motor preparation.     

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.     

Neuronal activity related to visually guided saccades in the frontal eye fields of rhesus monkeys: comparison with supplementary eye fields.

1. The purpose of this study was to analyze the response properties of neurons in the frontal eye fields (FEF) of rhesus monkeys (Macaca mulatta) and to compare and contrast the various functional classes with those recorded in the supplementary eye fields (SEF) of the same animals performing the same go/no-go visual tracking task. Three hundred ten cells recorded in FEF provided the data for this investigation. 2. Visual cells in FEF responded to the stimuli that guided the eye movements. The visual cells in FEF responded with a slightly shorter latency and were more consistent and phasic in their activation than their counterparts in SEF. The receptive fields tended to emphasize the contralateral hemifield to the same extent as those observed in SEF visual cells. 3. Preparatory set cells began to discharge after the presentation of the target and ceased firing before the saccade, after the go/no-go cue was given. These neurons comprised a smaller proportion in FEF than in SEF. In contrast to their counterparts in SEF, the preparatory set cells in FEF did not respond preferentially in relation to contralateral movements, even though most responded preferentially for movements in one particular direction. The time course of the discharge of the FEF set cells was similar to that of their SEF counterparts, except that they reached their peak level of activation sooner. The few preparatory set cells in FEF tested with both auditory and visual stimuli tended to respond preferentially to the visual targets, whereas, in contrast, most set cells in SEF were bimodal. 4. Sensory-movement cells represented the largest population of cells recorded in FEF, responding in relation to both the presentation of the targets and the execution of the saccade. Although some of these sensory-movement cells resembled their counterparts in SEF by exhibiting a sustained elevation of activity, most of the FEF sensory-movement cells gave two discrete bursts, one after the presentation of the target and another before and during the saccade. Like their counterparts in SEF, the sensory-movement cells tended to be tuned for saccades into the contralateral hemifield, but this tendency was more pronounced in FEF than in SEF. The FEF sensory-movement cells discharged more briskly, with a shorter latency relative to the presentation of the target, than their counterparts in SEF. In addition, the FEF sensory-movement neurons reached their peak activation sooner than SEF sensory-movement neurons. Most FEF sensory-movement cells exhibited different patterns of activation in response to visual and auditory targets.(ABSTRACT TRUNCATED AT 400 WORDS)     

Macaque supplementary eye field neurons encode object-centered locations relative to both continuous and discontinuous objects

Many neurons in the supplementary eye field (SEF) of the macaque monkey fire at different rates before eye movements to the right or the left end of a horizontal bar regardless of the bar's location in the visual field. We refer to such neurons as carrying object-centered directional signals. The aim of the present study was to throw light on the nature of object-centered direction selectivity by determining whether it depends on the reference image's physical continuity. To address this issue, we recorded from 143 neurons in two monkeys. All of these neurons were located in a region coincident with the SEF as mapped out in previous electrical stimulation studies and many exhibited task-related activity in a standard saccade task. In each neuron, we compared neuronal activity across trials in which the monkey made eye movements to the right or left end of a reference image. On interleaved trials, the reference image might be either a horizontal bar or a pair of discrete dots in a horizontal array. The dominant effect revealed by this experiment was that neurons selectively active before eye movements to the right (or left) end of a bar were also selectively active before eye movements to the right (or left) dot in a horizontal array. An additional minor effect, present in around a quarter of the sample, took the form of a difference in firing rate between bar and dot trials, with the greater level of activity most commonly associated with dot trials. These phenomena could not be accounted for by minor intertrial differences in the physical directions of eye movements. In summary, SEF neurons carry object-centered signals and carry these signals regardless of whether the reference image is physically continuous or disjunct.     

Macaque SEF neurons encode object-centered directions of eye movements regardless of the visual attributes of instructional cues.

Macaque SEF neurons encode object-centered directions of eye movements regardless of the visual attributes of instructional cues. Neurons in the supplementary eye field (SEF) of the macaque monkey exhibit object-centered direction selectivity in the context of a task in which a spot flashed on the right or left end of a sample bar instructs a monkey to make an eye movement to the right or left end of a target bar. To determine whether SEF neurons are selective for the location of the cue, as defined relative to the sample bar, or, alternatively, for the location of the target, as defined relative to the target bar, we carried out recording while monkeys performed a new task. In this task, the color of a cue-spot instructed the monkey to which end of the target bar an eye movement should be made (blue for the left end and yellow for the right end). Object-centered direction selectivity persisted under this condition, indicating that neurons are selective for the location of the target relative to the target bar. However, object-centered signals developed at a longer latency (by approximately 200 ms) when the instruction was conveyed by color than when it was conveyed by the location of a spot on a sample bar.     

Sequential activity of simultaneously recorded neurons in the superior colliculus during curved saccades

The visual world presents multiple potential targets that can be brought to the fovea by saccadic eye movements. These targets produce activity at multiple sites on a movement map in the superior colliculus (SC), an area of the brain related to saccade generation. The saccade made must result from competition between the populations of neurons representing these many saccadic goals, and in the present experiments we used multiple moveable microelectrodes to follow this competition. We recorded simultaneously from two sites on the SC map where each site was related to a different saccade target. The two targets appeared in rapid sequence, and the monkey was rewarded for making a saccade toward the one appearing first. Our study concentrated on trials in which the monkey made strongly curved saccades that were directed first toward one target and then toward the other. These curved saccades activated both sites on the SC map as they veered from one target to the other. The major finding was that the strongly curved saccades were preceded by sequential activity in the two neurons as indicated by three observations: the firing rate for the neuron related to the first target reached its peak earlier than did the rate of the neuron for the second target; the timing of the peak activity of the two neurons was related to the beginning and end of the saccade curvature; a weighted vector-average model based on the activity of the two neurons predicted the timing of saccade curvature. Straight averaging saccades ended between the targets so that they did not go to either target, and they were accompanied by simultaneous rather than sequential activation of the two neurons. Thus when multiple populations of neurons are active on the SC movement map, the resulting saccade is determined by the relative timing of the activity in the populations as well as their magnitude. In contrast, SC activity at the two sites did not predict the final direction of the saccade, and several control experiments found insufficient activity at other sites on the SC map to account for that final direction. We conclude that the SC neuronal activity predicts the timing of the saccade curvature, but not the final direction of the trajectory. These observations are consistent with SC activity being critical in selecting the goal of the saccade, but not in determining the exact trajectory.     

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.     

Relationship of presaccadic activity in frontal eye field and supplementary eye field to saccade initiation in macaque: Poisson spike train analysis

The purpose of this study was to investigate the temporal relationship between presaccadic neuronal discharges in the frontal eye fields (FEF) and supplementary eye fields (SEF) and the initiation of saccadic eye movements in macaque. We utilized an analytical technique that could reliably identify periods of neuronal modulation in individual spike trains. By comparing the observed activity of neurons with the random Poisson distribution generated from the mean discharge rate during the trial period, the period during which neural activity was significantly elevated with a predetermined confidence level was identified in each spike train. In certain neurons, bursts of action potentials were identified by determining the period in each spike train in which the activation deviated most from the expected Poisson distribution. Using this method, we related these defined periods of modulation to saccade initiation in specific cell types recorded in FEF and SEF. Cells were recorded in SEF while monkeys made saccades to targets presented alone. Cells were recorded in FEF while monkeys made saccades to targets presented alone or with surrounding distractors. There were no significant differences in the time-course of activity of the population of FEF presaccadic movement cells prior to saccades generated to singly presented or distractor-embedded targets. The discharge of presaccadic movement cells in FEF and SEF could be subdivided quantitatively into an early prelude followed by a high-rate burst of activity that occurred at a consistent interval before saccade initiation. The time of burst onset relative to saccade onset in SEF presaccadic movement cells was earlier and more variable than in FEF presaccadic movement cells. The termination of activity of another population of SEF neurons, known as preparatory set cells, was time-locked to saccade initiation. In addition, the cessation of SEF preparatory set cell activity coincided precisely with the beginning of the burst of SEF presaccadic movement cells. This finding raises the possibility that SEF preparatory set cells may be involved in saccade initiation by regulating the activation of SEF presaccadic movement cells. These results demonstrate the utility of the Poisson spike train analysis to relate periods of neuronal modulation to behavior.     

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.     

Different cortical activations during visuospatial attention and the intention to perform a saccade

Everyday life often necessitates dissociation between our directed attention and the intention to direct our gaze. Accordingly, the differential role of visual and motor related areas in the one or the other process is an issue of an ongoing debate. Here we used functional magnetic resonance imaging to elaborate a differentiation between visuospatial attention and the intention for a horizontal saccade in these cortical areas. Subjects fixated a central target, while they directed their attention to a colored cue in the left or right visual field. Regardless of its location, the color of the cue instructed the direction of the upcoming saccade (intention). The attention to the peripheral cue and the intention to perform the saccade were thus either directed to the same side or to opposite sides. A random effects analysis of the imaging data showed that activation of the early visual cortex and the motion sensitive complex was biased by attention to the contralateral cue, whereas activity of the color sensitive complex was modulated by the stimulus instructing a contraversive saccade. The posterior parietal cortex and the proper supplementary eye field (SEF) were most strongly activated in case of spatially congruent attention and intention. In contrast, activity of the pre-SEF and the frontal eye field was enhanced by spatially divergent attention and intention. The results presented here advance our understanding of how the human brain processes spatial information. Noteworthy, the visuomotor related areas show a subtle cortical separation for visual related attention and saccade related intention.     

Target selection and saccade generation in monkey superior colliculus

The superior colliculus (SC) of the monkey has been shown to be involved in not only initiation of saccades but in the selection of the target to which the saccade can be directed. The present experiments examine whether SC neuronal activity related to target selection is also related to saccade generation. In an asynchronous target task, the monkey was required to make a saccade to the first of two spots of light to appear. Using choice probability analysis over multiple trials, we determined the earliest time at which neurons in the SC intermediate layers indicated target selection. We then determined how closely the neuronal selection was correlated to saccade onset by using our asynchronous reaction time task, which allowed the monkey to make a saccade to the target as soon as the selection had been made. We found that the selection became evident at widely differing times for different neurons. Some neurons indicated target selection just before the saccade (close to the pre-saccadic burst of activity), others did so at the time of the visual response, and some showed an increase in their activity even before the target appeared. A fraction of this pre-stimulus bias resulted from a priming effect of the previous trial; a saccade to the target in the movement field on the previous trial produced both a higher level of neuronal activity and a higher probability for a saccade to that target on the current trial. We found that most of the neurons (76%) showed a correlation between selection time and reaction time. Furthermore, within this 76% of neurons, many indicated a selection very early during the visual response. There was no evidence of a sequence from target selection first and saccade selection later, but rather that target selection and saccade initiation are intertwined and are probably inseparable.     

Neurons in the rostral cingulate motor area monitor multiple phases of visuomotor behavior with modest parametric selectivity

We examined the cellular activity in the rostral cingulate motor area (CMAr) with respect to multiple behavioral factors that ranged from the retrieval and processing of associative visual signals to the planning and execution of instructed actions. We analyzed the neuronal activity in monkeys while they performed a behavioral task in which 2 visual instruction cues were given successively with an intervening delay. One cue instructed the location of the target to be reached; the other cue instructed which arm was to be used. After a second delay, the monkey received a motor-set cue to be prepared to initiate the motor task in accordance with instructions. Finally, after a GO signal, the monkey reached for the instructed target with the instructed arm. We found that the activity of neurons in the CMAr changed profoundly throughout the behavioral task, which suggested that the CMAr participated in each of the behavioral processing steps. However, the neuronal activity was only modestly selective for the spatial location of the visual signal. We also found that selectivity for the instructional information delivered with the signals (target location and arm use) was modest. Furthermore, during the motor-set and movement periods, few CMAr neurons exhibited selectivity for such motor parameters as the location of the target or the arm to be used. The abundance and robustness of the neuronal activity within the CMAr that reflected each step of the behavioral task and the modest selectivity of the same cells for sensorimotor parameters are strikingly different from the preponderance of selectivity that we have observed in other frontal areas. Based on these results, we propose that the CMAr participates in monitoring individual behavioral events to keep track of the progress of required behavioral tasks. On the other hand, CMAr activity during motor planning may reflect the emergence of a general intention for action.     

Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward

1. The present paper reports complex neural activities in the monkey caudate nucleus that precede and anticipate visual stimuli and reward in learned visuomotor paradigms. These activities were revealed typically in the delayed saccade task in which memory and anticipation were required. We classified these activities according to their relationships to the task. 2. Activity related to expectation of a cue (n = 46) preceded the presentation of a spot of light (target cue) that signified the future location of saccade target. When the target cue was delayed, the activity was prolonged accordingly. The same spot of light was preceded by no activity if it acted as a distracting stimulus. 3. The sustained activity (n = 80) was a tonic discharge starting after the target cue as if holding the spatial information. 4. The activity related to expectation of target (n = 109) preceded the appearance of the target whose location was cued previously. It started with or after a saccade to the cued target location and ended with the appearance of the target. The activity was greater when the target was expected to appear in the contralateral visual field. 5. The activity related to expectation of reward (n = 57) preceded a task-specific reward. It started with the appearance of the final target and ended with the reward. In most cases, the activity was nonselective for how the monkey obtained the reward, i.e., by visual fixation only, by a saccade, or by a hand movement. The activity was dependent partly on visual fixation. 6. A few neurons showed tonic activity selectively before lever release and are thus considered to be related to the preparation of hand movements. 7. The activity related to breaking fixation (n = 33) occurred phasically if the monkey broke fixation, aborting the trial. 8. Activity related to reward (n = 104) was a phasic discharge that occurred before or after a reward of water was delivered. The activity was not simply related to a specific movement involved in the reward-obtaining behavior (eye, hand, or mouth movement). 9. Fixation-related activity (n = 72) was tonic activity continuing as long as the monkey attentively fixated a spot of light. It was dependent on reward expectancy in most cases. 10. The present results, together with those in the preceding papers, indicate that the activities of individual caudate neurons--sensory, motor, or cognitive--are dependent on specific contexts of learned behavior.(ABSTRACT TRUNCATED AT 400 WORDS)     

Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades

Dorsolateral prefrontal and posterior parietal cortex share reciprocal projections. They also share nearly identical patterns of neuronal activation during performance of memory-guided saccades. To test the hypothesis that the reciprocal projections between parietal and prefrontal neurons may entrain their parallel activation, the present experiments have combined cortical cooling in one cortical area with single-unit recording in the other to more precisely determine the physiological interactions between the two during working memory performance. The activity of 105 cortical neurons during the performance of an oculomotor delayed response (ODR) task (43 parietal neurons during prefrontal cooling, 62 prefrontal neurons during parietal cooling) was compared across two blocks of trials collected while the distant cortical area either was maintained at normal body temperature or cooled. The mean firing rates of 71% of the prefrontal neurons during ODR performance changed significantly when parietal cortex was cooled. Prefrontal neurons the activity of which was modulated during the cue, delay, or saccade periods of the task were equally vulnerable to parietal inactivation. Further, both lower and higher firing rates relative to the precool period were seen with comparable frequency. Similar results were obtained from the converse experiment, in which the mean firing rates of 76% of the parietal neurons were significantly different while prefrontal cortex was cooled, specifically in those task epochs when the activity of each neuron was modulated during ODR performance. These effects again were seen equally in all epochs of the ODR task in the form of augmented or suppressed activity. Significant effects on the latency of neuronal activation during cue and saccade periods of the task were absent irrespective of the area cooled. Cooling was associated in some cases with a shift in the best direction of Gaussian tuning functions fit to neuronal activity, and these shifts were on average larger during parietal than prefrontal cooling. In view of the parallel between the similarity in activity patterns previously reported and the largely symmetrical cooling effects presently obtained, the data suggest that prefrontal and parietal neurons achieve matched activation during ODR performance through a symmetrical exchange of neuronal signals between them; in both cortical areas, neurons activated during the cue, delay, and also saccade epochs of the ODR task participate in reciprocal neurotransmission; and the output of each cortical area produces a mixture of excitatory and inhibitory drives within its target.     

Visual and saccade-related activity in macaque posterior cingulate cortex

Previous neurophysiological studies have reported that neurons in posterior cingulate cortex (PCC) respond after eye movements, and that these responses may vary with ambient illumination. In monkeys, PCC neurons also respond after the illumination of large visual patterns but not after the illumination of small visual targets on either reflexive saccade tasks or peripheral attention tasks. These observations suggest that neuronal activity in PCC is modulated by behavioral context, which varies with the timing and spatial distribution of visual and oculomotor events. To test this hypothesis, we measured the spatial and temporal response properties of single PCC neurons in monkeys performing saccades in which target location and movement timing varied unpredictably. Specifically, an unsignaled delay between target onset and movement onset permitted us to temporally dissociate changes in PCC activity associated with either event. Response fields constructed from these data demonstrated that many PCC neurons were activated after the illumination of small contralateral visual targets, as well as after the onset of contraversive saccades guided by those targets. In addition, the PCC population maintained selectivity for small contralateral targets during delays of up to 600 ms. Overall, PCC activation was highly variable trial to trial and selective for a broad range of directions and amplitudes. Planar functions described response fields nearly as well as broadly tuned 2-dimensional Gaussian functions. Additionally, the overall responsiveness of PCC neurons decreased during delays when both a fixation stimulus and a saccade target were visible, suggesting a modulation by divided attention. Finally, the strength of the neuronal response after target onset was correlated with saccade accuracy on delayed-saccade trials. Thus PCC neurons may signal salient visual and oculomotor events, consistent with a role in visual orienting and attention.     

Quantitative analysis of substantia nigra pars reticulata activity during a visually guided saccade task

Several lines of evidence suggest that the pars reticulata subdivision of the substantia nigra (SNr) plays a role in the generation of saccadic eye movements. However, the responses of SNr neurons during saccades have not been examined with the same level of quantitative detail as the responses of neurons in other key saccadic areas. For this report, we examined the firing rates of 72 SNr neurons while awake-behaving primates correctly performed an average of 136 trials of a visually guided delayed saccade task. On each trial, the location of the visual target was chosen randomly from a grid spanning 40 degrees of horizontal and vertical visual angle. We measured the firing rates of each neuron during five intervals on every trial: a baseline interval, a fixation interval, a visual interval, a movement interval, and a reward interval. We found four distinct classes of SNr neurons. Two classes of neurons had firing rates that decreased during delayed saccade trials. The firing rates of discrete pausers decreased after the onset of a contralateral target and/or before the onset of a saccade that would align gaze with that target. The firing rates of universal pausers decreased after fixation on all trials and remained below baseline until the delivery of reinforcement. We also found two classes of SNr neurons with firing rates that increased during delayed saccade trials. The firing rates of bursters increased after the onset of a contralateral target and/or before the onset of a saccade aligning gaze with that target. The firing rates of pause-bursters increased after the onset of a contralateral target but decreased after the illumination of an ipsilateral target. Our quantification of the response profiles of SNr neurons yielded three novel findings. First, we found that some SNr neurons generate saccade-related increases in activity. Second, we found that, for nearly all SNr neurons, the relationship between firing rate and horizontal and vertical saccade amplitude could be well described by a planar surface within the range of movements we sampled. Finally we found that for most SNr neurons, saccade-related modulations in activity were highly variable on a trial-by-trial basis.