Fixation Neurons Research Articles

Macrosquare-wave Jerks Subsiding after Hydrocephalus Treatment in a Thalamic Hemorrhage Patient

A 54-year-old man suddenly developed impaired consciousness and left hemiplegia due to a right thalamic hematoma. Emergent ventricular drainage for acute hydrocephalus improved the level of consciousness, but macrosquare-wave jerks (MSWJ) consisting of a right-ward intrusive saccade and corrective saccade appeared. The MSWJ disappeared on day 2 when follow-up CT revealed improvement of hydrocephalus. However, on day 36, after ventricular drainage was clamped, the MSWJ reappeared. After ventriculoperitoneal shunt, MSWJ again subsided. In this patient, hydrocephalus may have stretched the superior colliculus, thereby decreasing activity of the fixation neurons and then omnipause neurons, and eventually resulting in the reversible MSWJ.

Suppressive control of optokinetic and vestibular nystagmus by the primate frontal eye field.

When the eyes are fixated on a spot, fixation neurons in the frontal eye field (FEF) show an increase in activity. Our previous study suggested that fixation neurons in the FEF contribute to the suppression of saccades and smooth pursuit eye movements to maintain active fixation. The present study examined the role of the FEF in the suppressive control of reflexive eye movements, optokinetic and vestibular nystagmus, in trained monkeys. Electrical stimulation in the FEF suppressed the quick and slow phases of optokinetic and vestibular nystagmus at an intensity lower than the threshold for eliciting electrically evoked saccades. Relatively weak suppression influenced the slow phase of vestibular nystagmus. During optokinetic or vestibular nystagmus, presentation of a stationary small spot to the eyes followed by fixation is known to suppress both the quick and slow phases of eye movements. We recorded the activity of fixation neurons in the FEF and found that fixation neurons usually showed a decrease in activity during optokinetic and vestibular nystagmus and an increase in activity during the suppression of nystagmus by visual fixation. The present results show that the activity of fixation neurons in the FEF is related to the suppressive control of optokinetic and vestibular nystagmus for maintaining active fixation. We discuss the role of a generalized visual fixation system that can maintain visual attention on an interesting object.NEW & NOTEWORTHY In this study, electrical stimulation in the frontal eye field (FEF) suppressed the quick and slow phases of optokinetic and vestibular nystagmus at an intensity subthreshold for eliciting saccades. Furthermore, the activity of fixation neurons in the FEF was related to the suppression of optokinetic and vestibular nystagmus by visual fixation. This suggests that a common neuronal assembly in the FEF may contribute to the suppressive control of different functional classes of eye movements.

S162. Excessive tonic inhibition of superior colliculus in tourette syndrome suggested by saccade profiles

Tourette syndrome (TS) is a common neurobehavioral disorder starting from childhood characterized by motor and vocal tics. Some suggest primary hypodopaminergic state followed by upward regulation of dopamine receptors for the cause of tics. The visually-guided saccade (VGS) task is a reflexive saccade task triggered by sudden extinction of a fixation spot and appearance of a target, while the memory-guided saccade (MGS) task is a voluntary saccade task to the memorized target. We previously reported slightly prolonged VGS latency and significantly prolonged MGS latency in Parkinson’s disease, presumably due to impaired function of the direct pathway of the basal ganglia (BG) and excessive inhibition of superior colliculus (SC) caused by the increased BG output. We investigated the performance of VGS and MGS to see whether the pathophysiology of TS represented the dopaminergic deficiency. We recruited 62 male drug-naïve participants with TS and 49 normal controls (NC) who were 5–16 years old. In VGS, after illumination of a central spot for 2.0–2.8 s, a target was presented at locations 5°, 10° or 20° to the right or left. The subjects moved their gaze from the spot to the target quickly. In MGS, a target stimulus flashed for 50 ms while they fixated the central spot. Once the spot disappeared, they moved their gaze to the remembered location, where the light re-appeared 600 ms later. Each subject performed at least 36 VGS and 36 MGS trials. Eye movements were recorded by electrooculography. The latency of the saccade from the extinction of the central spot and amplitude of the first saccade were measured in each trial. Age-matched analysis on 29 pairs was performed by Student’s t-test. [VGS] The median of latencies in TS was comparable at 5° (202.0 vs 203.3 ms), whereas it was longer at 20° (251.2 vs 236.0 ms). The difference between latencies towards peripheral (20°) and central (5°) targets was larger (49.1 vs 32.6 ms∗, 16.6 ± 15.5 ms). The median of amplitudes was smaller in TS (4.9 vs 5.4°∗ at 5°, 18.3 vs 19.0°∗ at 20°). [MGS] The median of latencies in TS was shorter at 5° (324.1 vs 338.5 ms), whereas it was longer at 20° (308.4 vs 290.3 ms). The difference between latencies towards central and peripheral targets was smaller (15.8 vs 48.1 ms, −32.4 ± 48.4 ms). The median of amplitudes was comparable (5.0 vs 4.6° at 5°, 16.2 vs 15.4° at 20°). Success rate of MGS was lower (61.5 vs 83.1%†). The occurrence of saccades to cue was comparable (30.2 vs 36.6%). ∗ p < 0.05, † p < 0.01, otherwise not statistically significant. In TS, latencies to peripheral targets in VGS and MGS were longer than in normal subjects. Dopaminergic deficiency may explain the prolonged MGS latency. The resultant excessive tonic inhibition of SC by the increased BG input may decrease the activity of fixation neurons, which may shorten the VGS latency to central targets, while leading to the prolonged latency to peripheral targets through the suppressed activity of saccade neurons.

Fixation target representation in prefrontal cortex during the antisaccade task.

Neurons that discharge strongly during the time period of fixation of a visual target and cease to discharge before saccade initiation have been described in the brain stem, superior colliculus, and cortical areas. In subcortical structures, fixation neurons play a reciprocal role with saccadic neurons during the generation of eye movements. Their role in the dorsolateral prefrontal cortex is less obvious, and it is not known if they are activated by fixation, inhibit saccade generation, or play a role in more complex functions such as the inhibition of inappropriate responses. We examined the properties of prefrontal fixation neurons in the context of an antisaccade task, which requires an eye movement directed away from a prepotent visual stimulus. We tested monkeys with variants of the task, allowing us to dissociate activity synchronized on the fixation offset, presentation of the visual stimulus, and saccadic onset. Fixation neuron activity latency was most strongly tied to the offset of the fixation point across task variants. It was not well predicted by the appearance of the visual stimulus, which is essential for planning of the correct eye movement and inhibiting inappropriate ones. Activity of fixation neurons was generally negatively correlated with that of saccade neurons; however, critical differences in timing make it unlikely that they provide precisely timed signals for the generation of eye movements. These results demonstrate the role of fixation neurons in the prefrontal cortex during tasks requiring timing of appropriate eye movement and inhibition of inappropriate actions.NEW & NOTEWORTHY Properties of neurons that discharge during eye fixation and go silent before saccade initiation have been described in subcortical structures involved in eye movement generation, but their role in the dorsolateral prefrontal cortex presents a puzzle. Our results demonstrate the role of fixation neurons in the prefrontal cortex during tasks requiring precise timing of appropriate eye movement and inhibition of inappropriate actions.

Activity of fixation neurons in the monkey frontal eye field during smooth pursuit eye movements.

We recorded the activity of fixation neurons in the frontal eye field (FEF) in trained monkeys and analyzed their activity during smooth pursuit eye movements. Fixation neurons were densely located in the area of the FEF in the caudal part of the arcuate gyrus facing the inferior arcuate sulcus where focal electrical stimulation suppressed the generation of saccades and smooth pursuit in bilateral directions at an intensity lower than the threshold for eliciting electrically evoked saccades. Whereas fixation neurons discharged tonically during fixation, they showed a variety of discharge patterns during smooth pursuit, ranging from a decrease in activity to an increase in activity. Of these, more than two-thirds were found to show a reduction in activity during smooth pursuit in the ipsilateral and bilateral directions. The reduction in activity of fixation neurons began at pursuit initiation and continued during pursuit maintenance. When catch-up saccades during the initiation of pursuit were eliminated by a step-ramp target routine, the reduced activity of fixation neurons remained. The reduction in activity during pursuit was not dependent on the activity during fixation without a target. Based on these results, we discuss the role of the FEF at maintaining fixation in relation to various other brain areas. We suggest that fixation neurons in the FEF contribute to the suppression of smooth pursuit. These results suggest that FEF fixation neurons are part of a more generalized visual fixation system through which suppressive control is exerted on smooth pursuit, as well as saccades.

Suppression of smooth pursuit eye movements induced by electrical stimulation of the monkey frontal eye field

This study was performed to characterize the properties of the suppression of smooth pursuit eye movement induced by electrical stimulation of the frontal eye field (FEF) in trained monkeys. At the stimulation sites tested, we first determined the threshold for generating electrically evoked saccades (Esacs). We then examined the suppressive effects of stimulation on smooth pursuit at intensities that were below the threshold for eliciting Esacs. We observed that FEF stimulation induced a clear deceleration of pursuit at pursuit initiation and also during the maintenance of pursuit at subthreshold intensities. The suppression of pursuit occurred even in the absence of catch-up saccades during pursuit, indicating that suppression influenced pursuit per se. We mapped the FEF area that was associated with the suppressive effect of stimulation on pursuit. In a wide area in the FEF, suppressive effects were observed for ipsiversive, but not contraversive, pursuit. In contrast, we observed the bilateral suppression of both ipsiversive and contraversive pursuit in a localized area in the FEF. This area coincided with the area in which we have previously shown that stimulation suppressed the generation of saccades in bilateral directions and also where fixation neurons that discharged during fixation were concentrated. On the basis of these results, we compared the FEF suppression of pursuit with that of saccades with regard to several physiological properties and then discussed the role of the FEF in the suppression of both pursuit and saccades, and particularly in the maintenance of visual fixation.

Optimal performance in a countermanding saccade task

Countermanding an action is a fundamental form of cognitive control. In a saccade-countermanding task, subjects are instructed that, if a stop signal appears shortly after a target, they are to maintain fixation rather than to make a saccade to the target. In recent years, recordings in the frontal eye fields and superior colliculus of behaving non-human primates have found correlates of such countermanding behavior in movement and fixation neurons. In this work, we extend a previous neural network model of countermanding to account for the high pre-target activity of fixation neurons. We propose that this activity reflects the functioning of control mechanisms responsible for optimizing performance. We demonstrate, using computer simulations and mathematical analysis, that pre-target fixation neuronal activity supports countermanding behavior that maximizes reward rate as a function of the stop signal delay, fraction of stop signal trials, intertrial interval, duration of timeout, and relative reward value. We propose experiments to test these predictions regarding optimal behavior.

Response Properties of Fixation Neurons and Their Location in the Frontal Eye Field in the Monkey

Electrical stimulation of the frontal eye field (FEF) has recently been reported to suppress the generation of saccades, which supports the idea that the FEF plays a role in maintaining attentive fixation. This study analyzed the activity of fixation neurons that discharged during fixation in the FEF in relation to visual fixation and saccades in trained monkeys. The neural activity of fixation neurons increased at the start of fixation and was maintained during fixation. When a fixation spot of light disappeared during steady fixation, different fixation neurons exhibited different categories of response, ranging from a decrease in activity to an increase in activity, indicating that there is a continuum of fixation neurons, from neurons with foveal visual-related activity to neurons with activity that is related to the motor act of fixating. Fixation neurons usually showed a decrease in their firing rate before the onset of visually guided saccades (Vsacs) and memory-guided saccades in any direction. The reduction in activity of fixation neurons nearly coincided with, or occurred slightly before, the increase in the activity of saccade-related movement neurons in the FEF in the same monkey. Although fixation neurons were scattered in the FEF, about two thirds of fixation neurons were concentrated in a localized area in the FEF at which electrical stimulation induced strong suppression of the initiation of Vsacs bilaterally. These results suggest that fixation neurons in the FEF are part of a suppression mechanism that could control the maintenance of fixation and the initiation of saccades.

Proactive Inhibitory Control and Attractor Dynamics in Countermanding Action: A Spiking Neural Circuit Model

Flexible behavior depends on the brain's ability to suppress a habitual response or to cancel a planned movement whenever needed. Such inhibitory control has been studied using the countermanding paradigm in which subjects are required to withhold an imminent movement when a stop signal appears infrequently in a fraction of trials. To elucidate the circuit mechanism of inhibitory control of action, we developed a recurrent network model consisting of spiking movement (GO) neurons and fixation (STOP) neurons, based on neurophysiological observations in the frontal eye field and superior colliculus of behaving monkeys. The model places a premium on the network dynamics before the onset of a stop signal, especially the experimentally observed high baseline activity of fixation neurons, which is assumed to be modulated by a persistent top-down control signal, and their synaptic interaction with movement neurons. The model simulated observed neural activity and fit behavioral performance quantitatively. In contrast to a race model in which the STOP process is initiated at the onset of a stop signal, in our model whether a movement will eventually be canceled is determined largely by the proactive top-down control and the stochastic network dynamics, even before the appearance of the stop signal. A prediction about the correlation between the fixation neural activity and the behavioral outcome was verified in the neurophysiological data recorded from behaving monkeys. The proposed mechanism for adjusting control through tonically active neurons that inhibit movement-producing neurons has significant implications for exploring the basis of impulsivity associated with psychiatric disorders.

A Code for Spatial Alternation During Fixation in Rat Hippocampal CA1 Neurons

The classical notion of hippocampal CA1 "place cells," whose activity tracks physical locations, has undergone substantial revision in recent years. Here, we provide further evidence of an abstract spatial code in hippocampal CA1, which relies on memory and adds complexity to the basic "place cell." Using a nose-poking paradigm with four male Wistar rats, we specifically concentrated on activity during fixation, when the rat was immobile and waiting for the next task event in a memory-guided spatial alternation task. The rat had to alternate between choosing the right and left holes on a trial-by-trial basis, without any sensory cue, and relying on an internal representation of the sequence of trials. Twelve tetrodes were chronically implanted for single-unit recording in the right CA1 of each rat. We focus on 76 single neurons that showed significant activation during the fixation period compared with baseline activity between trials. Among these 76 fixation neurons, we observed 38 neurons that systematically changed their fixation activity as a function of the alternation sequence. That is, even though these rats were immobile during the fixation period, the neurons fired differently for trials in which the next spatial choice should be left (i.e., RIGHT-TO-LEFT trials) compared with trials in which the next spatial choice should be right (i.e., LEFT-TO-RIGHT trials), or vice versa. Our results imply that these neurons maintain a sequential code of the required spatial response during the alternation task and thus provide abstract information, derived from memory, that can be used for efficient navigation.

Suppression of saccades and response properties of fixation neurons in the monkey frontal eye field

Suppression of saccades and response properties of fixation neurons in the monkey frontal eye field

Control of oculomotor reflexes: independent effects of strategic and automatic preparation

The reduction in saccade latency when the fixation point is removed (fixation offset effect-FOE) reflects the degree to which fixation neurons are under influence by a stimulus at fixation. Strategic manipulations of oculomotor readiness that bring these neurons under endogenous control reduce the magnitude of the FOE. Using an aging foreperiod paradigm, and the FOE as a marker for cortical control of reflexive fixation, we showed that, for both prosaccades and antisaccades, increasing preparation across the foreperiod reduced both saccade latency and the FOE. Consistent with Los's trace conditioning account, these effects reflected greater preparation for trials when the current short foreperiod was preceded by a trial with a short foreperiod. The FOE was also smaller for antisaccades than for prosaccades demonstrating strategic modulation. However, the effects of trace conditioning were comparable in the two tasks, demonstrating that strategic and unconscious priming effects both independently modulate the control of ocular fixation.

Controversy on “Fixation Zone” of the Superior Colliculus

The superior colliculus (SC) plays an important role in generating saccades. The rostral pole of the SC contains neurons whose discharge increases during visual fixation and decreases just before and during saccades, and is called the fixation zone. Fixation neurons are related to maintaining fixation and suppressing saccades. The more caudal SC contains saccade-related neurons that show burst activity at the onset of saccades, and is called the saccade zone. However, the functional independence of the rostral “fixation zone” is not necessarily accepted. This review will deal with controversies on the “fixation zone” of the rostral SC.

Responses of Collicular Fixation Neurons to Gaze Shift Perturbations in Head-Unrestrained Monkey Reveal Gaze Feedback Control

A prominent hypothesis in motor control is that endpoint errors are minimized because motor commands are updated in real time via internal feedback loops. We investigated in monkey whether orienting saccadic gaze shifts made in the dark with coordinated eye-head movements are controlled by feedback. We recorded from superior colliculus fixation neurons (SCFNs) that fired tonically during fixation and were silent during gaze shifts. When we briefly (<or=700 ms) interrupted gaze shifts by transiently braking head movements, SCFNs fired steadily during brake-induced gaze immobility, and their mean frequency was inversely related to the remaining distance between current gaze position and the target. After head release, a corrective gaze saccade brought gaze on the unseen goal, and SCFN firing frequency peaked. The results support gaze feedback control and show that the SC is part of a network that encodes, during orientation, the distance between eye and target, irrespective of gaze trajectory characteristics.

Discharge Properties of Monkey Tectoreticular Neurons

The intermediate layers of the superior colliculus (SC) contain neurons that clearly play a major role in regulating the production of saccadic eye movements: a burst of activity from saccade neurons (SNs) is thought to provide a drive signal to set the eyes in motion, whereas the tonic activity of fixation neurons (FNs) is thought to suppress saccades during fixation. The exact contribution of these neurons to saccade control is, however, unclear because the nature of the signals sent by the SC to the brain stem saccade generation circuit has not been studied in detail. Here we tested the hypothesis that the SC output signal is sufficient to control saccades by examining whether antidromically identified tectoreticular neurons (TRNs: 33 SNs and 13 FNs) determine the end of saccades. First, TRNs had discharge properties similar to those of nonidentified SC neurons and a proportion of output SNs had visually evoked responses, which signify that the saccade generator must receive and process visual information. Second, only a minority of TRNs possessed the temporal patterns of activity sufficient to terminate saccades: Output SNs did not cease discharging at the time of saccade end, possibly continuing to drive the brain stem during postsaccadic fixations, and output FNs did not resume their activity before saccade end. These results argue against a role for SC in regulating the timing of saccade termination by a temporal code and suggest that other saccade centers act to thwart the extraneous SC drive signal, unless it controls saccade termination by a spatial code.

Commissural Excitation and Inhibition by the Superior Colliculus in Tectoreticular Neurons Projecting to Omnipause Neuron and Inhibitory Burst Neuron Regions

Previous electrophysiological studies have shown that the commissural connections between the two superior colliculi are mainly inhibitory with fewer excitatory connections. However, the functional roles of the commissural connections are not well understood, so we sought to clarify the physiology of tectal commissural excitation and inhibition of tectoreticular neurons (TRNs) in the "fixation " and "saccade " zones of the superior colliculus (SC). By recording intracellular potentials, we identified TRNs by their antidromic responses to stimulation of the omnipause neuron (OPN) and inhibitory burst neuron (IBN) regions and analyzed the effects of stimulation of the contralateral SC on these TRNs in anesthetized cats. TRNs in the caudal SC (saccade neurons) projected to the IBN region, and received mono- or disynaptic inhibition from the entire rostrocaudal extent of the contralateral SC. In contrast, TRNs in the rostral SC projected to the OPN or IBN region and received monosynaptic excitation from the most rostral level of the contralateral SC, and mono- or disynaptic inhibition from its entire rostrocaudal extent. Among the rostral TRNs with commissural excitation, IBN-projecting TRNs also projected to Forel's field H (vertical gaze center), suggesting that they were most likely saccade neurons related to vertical saccades. In contrast, TRNs projecting only to the OPN region were most likely fixation neurons. Most putative inhibitory neurons in the rostral SC had multiple axon branches throughout the rostrocaudal extent of the contralateral SC, whereas excitatory commissural neurons, most of which were rostral TRNs, distributed terminals to a discrete region in the rostral SC.

Effects of Structured Nontarget Stimuli on Saccadic Latency

It has been suggested that the remote distractor effect is the result of nontarget stimulation of a central region representing a collicular fixation zone near the time of target onset. The distributed network of the cells responsible for this effect is believed to extend over a large area, responding to distractors < or =10 deg in the periphery. Several studies also implicate the superior colliculus as the substrate behind an inhibited saccadic response arising from a display change. We investigated this further by using a patch of pink noise of various sizes as a nontarget stimulus. We show that the onset of a small patch (2.3 x 2.3 deg) of centrally displayed pink noise can produce a significant increase in saccadic latency to a simultaneously presented peripheral Gabor target. In contrast, a large patch (36 x 36 deg) of pink noise did not increase latency despite the fact that it also stimulated the region representing the fixation zone. Furthermore, only the large patch of noise facilitated latency when presented before target onset. We also examined the effect of patch sizes between these two extremes and found a steady decrease in latency as patch size increased. This confirms that nontarget stimulation of the region representing the fixation zone near the time of target onset is not in itself sufficient to produce the increase in latency typically found with remote distractors. The results are consistent with the idea that only a spatially confined object leads to a discharge of collicular fixation neurons.

Physiological Characterization of Synaptic Inputs to Inhibitory Burst Neurons From the Rostral and Caudal Superior Colliculus

The caudal superior colliculus (SC) contains movement neurons that fire during saccades and the rostral SC contains fixation neurons that fire during visual fixation, suggesting potentially different functions for these 2 regions. To study whether these areas might have different projections, we characterized synaptic inputs from the rostral and caudal SC to inhibitory burst neurons (IBNs) in anesthetized cats. We recorded intracellular potentials from neurons in the IBN region and identified them as IBNs based on their antidromic activation from the contralateral abducens nucleus and short-latency excitation from the contralateral caudal SC and/or single-cell morphology. IBNs received disynaptic inhibition from the ipsilateral caudal SC and disynaptic inhibition from the rostral SC on both sides. Stimulation of the contralateral IBN region evoked monosynaptic inhibition in IBNs, which was enhanced by preconditioning stimulation of the ipsilateral caudal SC. A midline section between the IBN regions eliminated inhibition from the ipsilateral caudal SC, but inhibition from the rostral SC remained unaffected, indicating that the latter inhibition was mediated by inhibitory interneurons other than IBNs. A transverse section of the brain stem rostral to the pause neuron (PN) region eliminated inhibition from the rostral SC, suggesting that this inhibition is mediated by PNs. These results indicate that the most rostral SC inhibits bilateral IBNs, most likely via PNs, and the more caudal SC exerts monosynaptic excitation on contralateral IBNs and antagonistic inhibition on ipsilateral IBNs via contralateral IBNs. The most rostral SC may play roles in maintaining fixation by inhibition of burst neurons and facilitating saccadic initiation by releasing their inhibition.

Suppression of visually and memory-guided saccades induced by electrical stimulation of the monkey frontal eye field. II. Suppression of bilateral saccades.

To understand the neural mechanism of fixation, we investigated effects of electrical stimulation of the frontal eye field (FEF) and its vicinity on visually guided (Vsacs) and memory-guided saccades (Msacs) in trained monkeys and found that there were two types of suppression induced by the electrical stimulation: suppression of ipsilateral saccades and suppression of bilateral saccades. In this report, we characterized the properties of the suppression of bilateral Vsacs and Msacs. Stimulation of the bilateral suppression sites suppressed the initiation of both Vsacs and Msacs in all directions during and approximately 50 ms after stimulation but did not affect the vector of these saccades. The suppression was stronger for ipsiversive larger saccades and contraversive smaller saccades, and saccades with initial eye positions shifted more in the saccadic direction. The most effective stimulation timing for the suppression of ipsilateral and contralateral Vsacs was approximately 40-50 ms before saccade onset, indicating that the suppression occurred most likely in the superior colliculus and/or the paramedian pontine reticular formation. Suppression sites of bilateral saccades were located in the prearcuate gyrus facing the inferior arcuate sulcus where stimulation induced suppression at < or =40 microA but usually did not evoke any saccades at 80 microA and were different from those of ipsilateral saccades where stimulation evoked saccades at < or =50 microA. The bilateral suppression sites contained fixation neurons. The results suggest that fixation neurons in the bilateral suppression area of the FEF may play roles in maintaining fixation by suppressing saccades in all directions.

Neural activity in the primate superior colliculus and saccadic reaction times in double-step experiments

Although primates including humans can do 2-3 saccades per second while observing their environment, this seems to be more complicated when the same visual target is displaced twice in brief succession. When the subject has to follow this target with its gaze, the reaction time of the second saccade is longer than that of the first. We present data from electrophysiological recordings in the superior colliculus of a monkey that is performing a double-step saccade task. Analysis of the neuronal activity shows that the fixation neurons and the saccadic neurons respond differently in single- and double-step tasks. Fixation neurons are not as active between the two saccades as could be expected from single-step trials. Therefore, the fixation neurons are not likely to cause the increase in reaction time. The recorded saccadic neurons usually showed a presumably visual activation about 70 ms after target appearance and a motor burst starting briefly before the saccade. A target-aligned response was encountered in half of the neurons about 150 ms after the second target appearance. The early visual target-aligned response is often lost before the second saccade in a double-step task with short stimulus delay. The rise of activity was slower before the second than before the first saccade. The neural latency was therefore longer before the second saccade. The motor burst coincides with the second saccade although it is delayed. Thus, the motor burst was always predictive of the occurrence of the saccade. We conclude that the fixation neurons in the superior colliculus are not likely to cause the delay of the second saccade, and that the activity in the saccadic neurons in the superior colliculus encodes the timing of the second saccade even if it is delayed.