Grazer Interactions with Invasive Agarophyton vermiculophyllum (Rhodophyta): Comparisons to Related versus Unrelated Native Algae.

Ecosystem responses to invasion are strongly influenced by interactions between invaders and native species. If native species provide biotic resistance by consuming or competing with an invader, the invasion may be slowed, and/or invasive populations may be limited. If local herbivores recognize an invasive plant as being similar to native species, they may graze it more readily. Biotic resistance is thus generally predicted to increase if the invader is phylogenetically related to natives. However, if the native species were unpalatable, then grazers may be predisposed to avoid the invader, thus reducing biotic resistance from consumption. In the marine realm, invertebrate grazers often avoid feeding on invasive algae. However, tests comparing macroalgal invaders to phylogenetically related natives have been rare. Here we present data for invertebrate grazing and habitat use of (i) invasive Agarophyton vermiculophyllum (Rhodophyta: Gracilariales: Gracilarieae), (ii) the native contribal species Gracilaria tikvahiae, and (iii) an unrelated native, Ulva sp., the most common native alga in the system. We find that grazers prefer Ulva over both Gracilarieae, both for feeding and for habitat use. These data suggest that biotic resistance from consumption is low and not enhanced by the presence of a closely related native alga.

Behavioral properties of saccades generated as a choice response.

The behavior characterizing choice response decision-making was studied in monkeys to provide background information for ongoing neurophysiological studies of the neural mechanisms underlying saccadic choice decisions. Animals were trained to associate a specific color from a set of colored visual stimuli with a specific spatial location. The visual stimuli (colored disks) appeared briefly at equal eccentricity from a central fixation position and then were masked by gray disks. The correct target association was subsequently cued by the appearance of a colored stimulus at the fixation point. The animal indicated its choice by saccading to the remembered location of the eccentric stimulus, which had matched the color of the cue. The number of alternative associations (NA) varied from 1 to 4 and remained fixed within a block of trials. After the training period, performance (percent correct responses) declined modestly as NA increased (on average 96, 93 or 84% correct for 1, 2 or 4 NA, respectively). Response latency increased logarithmically as a function of NA, thus obeying Hick's law. The spatial extent of the learned association between color and location was investigated by rotating the array of colored stimuli that had remained fixed during the learning phase to various different angles. Error rates in choice saccades increased gradually as a function of the amount of rotation. The learned association biased the direction of the saccadic response toward the quadrant associated with the cue, but saccade direction was always toward one of the actual visual stimuli. This suggests that the learned associations between stimuli and responses were not spatially exact, but instead the association between color and location was distributed with declining strength from the trained locations. These results demonstrate that the saccade system in monkeys also displays the characteristic dependence on NA in choice response latencies, while more basic features of the eye movements are invariant from those in other tasks. The findings also provide behavioral evidence that spatially distributed regions are established for the sensory-to-motor associations during training which are later utilized for choice decisions.

Neuro-ophthalmology of late-onset Tay-Sachs disease (LOTS).

BACKGROUND: Late-onset Tay-Sachs disease (LOTS) is an adult-onset, autosomal recessive, progressive variant of GM2 gangliosidosis, characterized by involvement of the cerebellum and anterior horn cells. OBJECTIVE: To determine the range of visual and ocular motor abnormalities in LOTS, as a prelude to evaluating the effectiveness of novel therapies. METHODS: Fourteen patients with biochemically confirmed LOTS (8 men; age range 24 to 53 years; disease duration 5 to 30 years) and 10 age-matched control subjects were studied. Snellen visual acuity, contrast sensitivity, color vision, stereopsis, and visual fields were measured, and optic fundi were photographed. Horizontal and vertical eye movements (search coil) were recorded, and saccades, pursuit, vestibulo-ocular reflex (VOR), vergence, and optokinetic (OK) responses were measured. RESULTS: All patients showed normal visual functions and optic fundi. The main eye movement abnormality concerned saccades, which were "multistep," consisting of a series of small saccades and larger movements that showed transient decelerations. Larger saccades ended earlier and more abruptly (greater peak deceleration) in LOTS patients than in control subjects; these changes can be attributed to premature termination of the saccadic pulse. Smooth-pursuit and slow-phase OK gains were reduced, but VOR, vergence, and gaze holding were normal. CONCLUSIONS: Patients with late-onset Tay-Sachs disease (LOTS) show characteristic abnormalities of saccades but normal afferent visual systems. Hypometria, transient decelerations, and premature termination of saccades suggest disruption of a "latch circuit" that normally inhibits pontine omnipause neurons, permitting burst neurons to discharge until the eye movement is completed. These measurable abnormalities of saccades provide a means to evaluate the effects of novel treatments for LOTS.

A distributed model of the saccadic system: simulations of trajectory variations produced by multiple competing visual stimuli.

When multiple competing visual stimuli are present, saccades show more trajectory variations than those produced by single-target stimuli. In particular, variable trajectories including curved and averaging saccades are observed when visual search is required to select and make a saccade to a target. In this paper, based on our behavioral observations and neural recordings in the superior colliculus (SC) in monkeys, we propose a new, distributed SC and cerebellum (CBM) model that accounts for the saccade trajectory variations produced by the presence of multiple visual stimuli. The long-range lateral inhibitory connections between SC units are replaced by local excitatory connections and short-range inhibition. The inhibition to the SC from the substantia nigra (SNr) is assumed to have distributed spatial tuning. The interactions between visually activated populations of SC units and the distributed SNr inhibition produce variable initial directions of saccadic trajectories and these directional variations are partially compensated by the CBM feedback system.

Common inhibitory mechanism for saccades and smooth-pursuit eye movements.

The premotor pathways subserving saccades and smooth-pursuit eye movements are usually thought to be different. Indeed, saccade and smooth-pursuit eye movements have different dynamics and functions. In particular, a group of midline cells in the pons called omnipause neurons (OPNs) are considered to be part of the saccadic system only. It has been established that OPNs keep premotor neurons for saccades under constant inhibition during fixation periods. Saccades occur only when the activity of OPNs has completely stopped or paused. Accordingly, electrical stimulation in the region of OPNs inhibits premotor neurons and interrupts saccades. The premotor relay for smooth pursuit is thought to be organized differently and omnipause neurons are not supposed to be involved in smooth-pursuit eye movements. To investigate this supposition, OPNs were recorded during saccades and during smooth pursuit in the monkey (Macaca mulatta). Unexpectedly, we found that neuronal activity of OPNs decreased during smooth pursuit. The resulting activity reduction reached statistical significance in approximately 50% of OPNs recorded during pursuit of a target moving at 40 degrees /s. On average, activity was reduced by 34% but never completely stopped or paused. The onset of activity reduction coincided with the onset of smooth pursuit. The duration of activity reduction was correlated with pursuit duration and its intensity was correlated with eye velocity. Activity reduction was observed even in the absence of catch-up saccades that frequently occur during pursuit. Electrical microstimulation in the OPNs' area induced a strong deceleration of the eye during smooth pursuit. These results suggest that OPNs form an inhibitory mechanism that could control the time course of smooth pursuit. This inhibitory mechanism is part of the fixation system and is probably needed to avoid reflexive eye movements toward targets that are not purposefully selected. This study shows that saccades and smooth pursuit, although they are different kinds of eye movements, are controlled by the same inhibitory system.

Short-term priming, concurrent processing, and saccade curvature during a target selection task in the monkey.

In human subjects, two mechanisms for improving the efficiency of saccades in visual search have recently been described: color priming and concurrent processing of two saccades. Since the monkey provides an important model for understanding the neural underpinnings of target selection in visual search, we sought to explore the degree to which the saccadic system of monkeys uses these same mechanisms. Therefore, we recorded the eye movements of rhesus monkeys performing a simple color-oddity pop-out search task, similar to that used previously with human subjects. The monkeys were rewarded for making a saccade to the odd-colored target, which was presented with an array of three distractors. The target and distractors were randomly chosen to be red or green in each trial. Similar to what was previously observed for humans, we found that monkeys show the influence of a cumulative, short-term priming mechanism which facilitates saccades when the color of the search target happens to repeat from trial to trial. Furthermore, we found that like humans, when monkeys make an erroneous initial saccade to a distractor, they are capable of executing a second saccade to the target after a very brief inter-saccadic interval, suggesting that the two saccades have been programmed concurrently (i.e. in parallel). These results demonstrate a close similarity between human and monkey performance. We also made a new observation: we found that when monkeys make such two-saccade responses, the trajectory of the initial saccade tends to curve toward the goal of the subsequent saccade. This provides evidence that the two saccade goals are simultaneously represented on a common motor map, supporting the idea that the movements are processed concurrently. It also indicates that concurrent processing is not limited to brain areas involved in higher-level planning; rather, such parallel programming apparently occurs at a low enough level in the saccadic system that it can affect saccade trajectory.

Evidence against direct connections to PPRF EBNs from SC in the monkey.

Direct projections from the superior colliculus (SC) to the paramedian pontine reticular formation (PPRF) have been demonstrated anatomically. The PPRF contains cells called excitatory burst neurons (EBNs) that execute the final premotoneuronal processing for saccadic eye movements, as well as other burst cells called long-lead burst neurons (LLBNs). Previous electrophysiological tests in monkey have failed to find evidence for monosynaptic connections from the SC to EBNs, but have shown that direct projections to LLBNs exist. The validity of these results has been questioned because EBNs are known to be inhibited during periods of fixation by cells called omnipause neurons (OPNs). In later experiments in cat, the stimulus in the SC was triggered during saccades (when OPNs are off) and direct connections to EBNs were found. The present experiments were conducted to determine whether direct connections from the SC to EBNs could be demonstrated in monkey. LLBNs located near EBNs were also recorded. Single-pulse stimuli were delivered at sites in the SC at current levels well above those required to evoke saccades with pulse train stimuli. The stimuli were triggered shortly after the onset of ipsilateral or contralateral saccades and also slightly after the end of saccades. A sample of 21 EBNs was recorded and none were activated by postsaccadic stimulation or during contralateral saccades. The high spontaneous discharge rates of EBNs during ipsilateral saccades made activation of these cells more difficult to detect; however, when the results were quantified by peristimulus time histograms aligned on stimulus onset, only 1/21 EBNs showed evidence of activation in the monosynaptic range of latencies (<1.6 ms), 13 EBNs were activated at di- or polysynaptic latencies, and 7 were not activated. In contrast, 15/21 LLBNs were activated with latencies in the monosynaptic range. Further evidence supporting the absence of direct connections to EBNs was obtained by realigning the peristimulus time histograms for a subset of EBNs with similar firing rates on the time of occurrence of the last spike before stimulus onset. A subset of EBNs was also studied during drowsy ipsilaterally directed eye drifts, during which these cells were firing at low spontaneous rates and OPNs were off. No evidence for direct connections to EBNs was found in this behavioral state. The variance in results obtained for cat and monkey may be due to a species difference that reflects the more complex signal processing required in the monkey's saccadic system.

Activity in deep intermediate layer collicular neurons during interrupted saccades.

The activity of neurons located in the deep intermediate and adjacent deep layers (hereafter called just deep intermediate layer neurons) of the superior colliculus (SC) in monkeys was recorded during saccades interrupted by electrical stimulation of the brainstem omnipause neuron (OPN) region. The goal of the experiment was to determine if these neurons maintained their discharge during the saccadic interruption, and thus, could potentially provide a memory trace for the intended movement which ends accurately on target in spite of the perturbation. The collicular neurons recorded in the present study were located in the rostral three-fifths of the colliculus. Most of these cells tended to show considerable presaccadic activity during a delayed saccade paradigm, and, therefore, probably overlap with the population of SC cells called buildup neurons or prelude bursters in previous studies. The effect of electrical stimulation in the OPN region (which interrupted ongoing saccades) on the discharge of these neurons was measured by computing the percentage reduction in a cell's activity compared to that present during non-interrupted saccades. During saccade interruption about 70% of deep intermediate layer neurons experienced a major reduction (30% or greater) in their activity, but discharge recovered quickly after the termination of the stimulation as the eyes resumed their movement to finish the saccade on the target. Therefore, the pattern of activity recorded in most of the deep intermediate layer neurons during interrupted saccades qualitatively resembled that previously reported for the saccade-related burst neurons which tend to be located more dorsally in the intermediate layer. In contrast, some of our cells (30%) showed little or no perturbation in their activity caused by the saccade interrupting stimulation. Because all the more dorsally located burst neurons and the majority of our deep intermediate layer neurons show a total or major suppression in their discharge during interrupted saccades, it seems unlikely that the colliculus by itself could maintain an accurate memory of the desired saccadic goal or the remaining dynamic motor error required to account for the accuracy of the resumed movement which occurs following the interruption. However, it remains possible that the smaller proportion of our neurons whose activity was not perturbed during interrupted movements could play a role in the mechanisms underlying saccade accuracy in the interrupted saccade paradigm. Interrupted saccades have longer durations than normal saccades to the same target. Therefore, we investigated whether the discharge of our deeper collicular cells was also necessarily prolonged during interrupted saccades, and, if so, how the prolongation compared to the prolongation of the saccade. Sixty percent of our sample neurons showed a prolongation in discharge that was approximately the same as the prolongation in saccade duration (difference < 15 ms in magnitude). The, observation that temporal discharge in our neurons was perturbed to roughly match saccadic temporal perturbation suggests that dynamic feedback about ongoing saccadic motion is provided to the colliculus, but does not necessarily imply that this structure is the site responsible for the computation of dynamic motor error.

Comparison of saccades perturbed by stimulation of the rostral superior colliculus, the caudal superior colliculus, and the omnipause neuron region.

Over the past decade, considerable research efforts have been focused on the role of the rostral superior colliculus (SC) in control of saccades. The most recent theory separates the deeper intermediate layers of the SC into two functional regions: the rostral pole of these layers constitutes a fixation zone and the caudal region comprises the saccade zone. Sustained activity of fixation neurons in the fixation zone is argued to maintain fixation and help prevent saccade generation by exciting the omnipause neurons (OPNs) in the brain stem. This hypothesis is in contrast to the traditional view that the SC contains a topographic representation of the saccade motor map on which the rostral pole of the SC encodes signals for generating small saccades (<2 degrees ) instead of preventing them. There is therefore an unresolved controversy about the specific role on the most rostral region of the SC, and we reexamined its functional contribution by quantifying and comparing spatial and temporal trajectories of 30 degrees saccades perturbed by electrical stimulation of the rostral pole and more caudal regions in the SC and of the OPN region. If the rostral pole serves to preserve fixation, then saccades perturbed by stimulation should closely resemble interrupted saccades produced by stimulation of the OPN region. If it also contributes to saccade generation, then the disrupted movements would better compare with redirected saccades observed after stimulation of the caudal SC. Our experiments revealed two significant findings: 1) the locus of stimulation was the primary factor determining the perturbation effect. If the directions of the target-directed saccade and stimulation-evoked saccade were aligned and if the stimulation was delivered within approximately the rostral 2 mm (<10 degrees amplitude) of SC, the ongoing saccade stopped in midflight but then resumed after stimulation end to reach the original visually specified goal with close to normal accuracy. When stimulation was applied at more caudal sites, the ongoing saccade directly reached the target location without stopping at an intermediate position. If the directions differed considerably, both initial and resumed components were typically observed for all stimulation sites. 2) A quantitative analysis of the saccades perturbed from the fixation zone showed significant deviations from their control spatial trajectories. Thus they resembled redirected saccades induced by caudal SC stimulation and differed significantly from interrupted saccades produced by OPN stimulation. The amplitude of the initial saccade, latency of perturbation, and spatial redirection were greatest for the most caudal sites and decreased gradually for rostral sites. For stimulation sites within the rostral pole of SC, the measures formed a smooth continuation of the trends observed in the saccade zone. As these results argue for the saccade zone concept, we offer reinterpretations of the data used to support the fixation zone model. However, we also discuss scenarios that do not allow an outright rejection of the fixation zone hypothesis.

Activity of the brain stem omnipause neurons during saccades perturbed by stimulation of the primate superior colliculus.

Stimulation of the rostral approximately 2 mm of the superior colliculus (SC) during a large, visual target-initiated saccade produces a spatial deviation of the ongoing saccade and then stops it in midflight. After the termination of the stimulation, the saccade resumes and ends near the location of the flashed target. The density of collicular projections to the omnipause neuron (OPN) region is greatest from the rostral SC and decreases gradually for the more caudal regions. It has been hypothesized that the microstimulation excites the OPNs through these direct connections, and the reactivation of OPNs, which are normally silent during saccades, stops the initial component in midflight by gating off the saccadic burst generator. Two predictions emerge from this hypothesis: 1) for microstimulation triggered on the onset of large saccades, the time from stimulation onset to resumption of OPN discharge should decrease as the stimulation site is moved rostral and 2) the lead time from reactivation of OPNs to the end of the initial saccade on stimulation trials should be equal to the lead time of pause end with respect to the end of control saccades. We tested this hypothesis by recording OPN activity during saccades perturbed by stimulation of the rostral approximately 2 mm of the SC. The distance of the stimulation site from the most rostral extent of the SC and the time of reactivation with respect to stimulation onset were not significantly correlated. The mean lead of reactivation of OPNs relative to the end of the initial component of perturbed saccades (6.5 ms) was significantly less than the mean lead with respect to the end of control (9.6 ms) and resumed saccades (10.4 ms). These results do not support the notion that the excitatory input from SC neurons-in particular, the fixation neurons in the rostral SC-provide the major signal to reactivate OPNs and end saccades. An alternative, conceptual model to explain the temporal sequence of events induced by stimulation of the SC during large saccades is presented. Other OPN activity parameters also were measured and compared for control and stimulation conditions. The onset of pause with respect to resumed saccade onset was larger and more variable than the onset of pause with respect to control saccades, whereas pause end with respect to the end of resumed and control saccades was similar. The reactivated discharge of OPNs during the period between the end of the initial and the onset of the resumed saccades was at least as strong as that following control movements. This latter observation is interpreted in terms of the resettable neural integrator hypothesis.

A distributed model of the saccade system: simulations of temporally perturbed saccades using position and velocity feedback.

Interrupted saccades, movements that are perturbed in mid-flight by pulsatile electrical stimulation in the omnipause neuron region, are known to achieve final eye displacements with accuracies that are similar to normal saccades even in the absence of visual input following the perturbation. In an attempt to explain the neurophysiological basis for this phenomenon, the present paper describes a model of the saccadic system that represents the superior colliculus as a dynamic two-dimensional, topographically arranged array of laterally interconnected units. A distributed feedback pathway to the colliculus from downstream elements, providing both eye position and velocity signals is incorporated in the model. With the help of a training procedure based on a genetic algorithm and gradient descent, the model is optimized to produce both the normal as well as slow saccades with similar accuracy. The slow movements are included in the training set to mimic the accurate saccades that occur despite alterations in alertness, as well as following various degenerative oculomotor diseases. Although interrupted saccades were not included in the training set, the model is able to produce accurate movement of this type as an emergent property for a wide range of perturbed eye velocity trajectories. Our model demonstrates for the first time, that by means of an appropriate feedback mechanism, a single-layered dynamic network can be made to retain a distributed memory of the remaining ocular displacement error even for interrupted and slow saccades. These results support the hypothesis that saccades are controlled by error feedback of signals that code efference copies of eye motion, and further, suggest a possible answer to a long standing question about the kind of the feedback signal, if any, that is received by the superior colliculus during saccadic eye movements.

Dependence on target configuration of express saccade-related activity in the primate superior colliculus.

To help understand how complex visual stimuli are processed into short-latency saccade motor programs, the activity of visuomotor neurons in the deeper layers of the superior colliculus was recorded while two monkeys made express saccades to one target and to two targets. It has been shown previously that the visual response and perimotor discharge characteristic of visuomotor neurons temporally coalesce into a single burst of discharge for express saccades. Here we seek to determine whether the distributed visual response to two targets spatially coalesces into a command appropriate for the resulting saccade. Two targets were presented at identical radial eccentricities separated in direction by 45 degrees. A gap paradigm was used to elicit express saccades. Express saccades were more likely to land in between the two targets than were saccades of longer latency. The speeds of express saccades to two targets were similar to those of one target of similar vector, as were the trajectories of saccades to one and two targets. The movement fields for express saccades to two targets were more broad than those for saccades to one target for all neurons studied. For most neurons, the spatial pattern of discharge for saccades to two targets was better explained as a scaled version of the visual response to two spatially separate targets than as a scaled version of the perimotor response accompanying a saccade to a single target. Only the discharge of neurons with large movement fields could be equally well explained as a visual response to two targets or as a perimotor response for a one-target saccade. For most neurons, the spatial properties of discharge depended on the number of targets throughout the entire saccade-related burst. These results suggest that for express saccades to two targets the computation of saccade vector is not complete at the level of the superior colliculus for most neurons and an explicit process of target selection is not necessary at this level for the programming of an express saccade.

Two-dimensional saccade-related population activity in superior colliculus in monkey.

The two-dimensional distribution of population activity in the superior colliculus (SC) during saccadic eye movements in the monkey was estimated using radial basis functions. To make these ensemble activity estimates, cells in the deeper layers of the SC were recorded over much of the rostrocaudal (caudal to 3.8 mm from the rostral tip), mediolateral extent of this structure. The dynamic movement field of each cell was determined at 2-ms intervals around the time of saccades for a wide variety of horizontal and oblique movements. Collicular neurons were divided into partially overlapping dorsal and ventral cell layers on the basis of recorded depth in SC. The pattern of presaccadic activity was used as an additional discriminant to sort the cells in the two layers into separate burst (dorsal) and buildup (ventral) cell classes. Rostrocaudal and medioventral cell location on the colliculus was estimated from the optimal target vector for a cell's visual response rather than from the optimal motor vector. The former technique was more reliable for locating some buildup neurons because it produced locations that compared better with the locations suggested by electrical stimulation. From the movement field data and from the estimates of each cell's anatomic location, a similar algorithm was used to compute the two-dimensional population activity in the two layers of the SC during horizontal and oblique saccades. A subset of the sample of neurons, located near the horizontal meridian of the SC, first was used to compute one-dimensional dynamic population activity estimates for horizontal saccades to allow partial comparison to previous studies. Statistical analyses on the one-dimensional data were limited to saccades of

Estimation of spatiotemporal neural activity using radial basis function networks.

We report a method using radial basis function (RBF) networks to estimate the time evolution of population activity in topologically organized neural structures from single-neuron recordings. This is an important problem in neuroscience research, as such estimates may provide insights into systems-level function of these structures. Since single-unit neural data tends to be unevenly sampled and highly variable under similar behavioral conditions, obtaining such estimates is a difficult task. In particular, a class of cells in the superior colliculus called buildup neurons can have very narrow regions of saccade vectors for which they discharge at high rates but very large surround regions over which they discharge at low, but not zero, levels. Estimating the dynamic movement fields for these cells for two spatial dimensions at closely spaced timed intervals is a difficult problem, and no general method has been described that can be applied to all buildup cells. Estimation of individual collicular cells' spatiotemporal movement fields is a prerequisite for obtaining reliable two-dimensional estimates of the population activity on the collicular motor map during saccades. Therefore, we have developed several computational-geometry-based algorithms that regularize the data before computing a surface estimation using RBF networks. The method is then expanded to the problem of estimating simultaneous spatiotemporal activity occurring across the superior colliculus during a single movement (the inverse problem). In principle, this methodology could be applied to any neural structure with a regular, two-dimensional organization, provided a sufficient spatial distribution of sampled neurons is available.

Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the omnipause region in monkey.

One proposed role of the superior colliculus (SC) in oculomotor control is to suppress or excite the activity of brain stem omnipause neurons (OPNs) to initiate or terminate saccades, respectively. Although connections from the SC to the OPNs have been demonstrated, the spatial distribution and discharge characteristics of the projecting neurons from the SC remain unknown. We mapped the spatial distribution of the deeper-layer neurons of the SC by stimulating the region of the OPNs to identify antidromic projections and found that the density of direct projections from the SC to the OPNs was greatest in the most rostral region and decreased gradually for more caudal sites. On the basis of saccade-related discharge characteristics, the antidromically driven neurons were predominantly fixation and buildup neurons. The spatially distributed SC projections to the OPNs and the discharge characteristics of the SC neurons suggest that the direct projections from SC to OPNs are excitatory. Finally, we propose how excitation and disfacilitation from SC activity can contribute to modulation of OPN response and control saccades.

Discharge of superior collicular neurons during saccades made to moving targets.

1. The discharge of neurons in the deeper layers of the monkey superior colliculus was recorded during saccades made to stationary and to smoothly moving visual targets. 2. All neurons that discharged for saccades made to stationary targets also discharged during saccades made to moving targets, but there was a systematic shift in the saccade vector yielding maximal activity (i.e. center of the movement field) of collicular neurons for the latter class of movements. The shift moved the center of the movement fields toward larger-amplitude pursuit saccades for target motion away from the fovea, in comparison with saccades made to stationary targets. However, the discharge at the center of the movement field for pursuit saccades was 14% lower when averaged over the sample of recorded cells. 3. The saccades made during pursuit tracking of moving visual stimuli have different dynamics than saccades made to stationary targets. At similar amplitudes pursuit saccades are slower, and their velocity profiles often show secondary velocity peaks or inflection points and have longer-duration decelerating phases. 4. The combined experimental observations of a change in saccade dynamics and the shift in movement fields in collicular neurons for pursuit saccades are compatible with the hypothesis that saccades made to moving targets are controlled by neural processing in two partially separate pathways. In this theory, one path is concerned with correction of a presaccadic retinal position error (a path that includes the colliculus) and another path is concerned with position extrapolations based on the velocity of the moving target (a path that does not include the colliculus).

Endpoint accuracy in saccades interrupted by stimulation in the omnipause region in monkey.

Electrical stimulation of the omnipause neuron region (OPN) at saccade onset results in interrupted saccades (IS)- eye movements which pause in midflight, resume after a brief period, and end near the target location. Details on the endpoint accuracy of IS do not exist, except for a brief report by Becker et al. (1981). Their analysis emphasized the accuracy of IS relative to the visual target which remained on during the interrupted period. We instead quantified the metric properties of IS relative to nonstimulated saccades during a target flash paradigm. Our results show that IS tend to be slightly hypermetric relative to the nonstimulated saccades to the same target location. The amount of overshoot is not correlated with target eccentricity. Detailed analyses also indicate that the standard deviations of the endpoint in IS are not significantly larger than those for nonstimulated saccades, although there was a much larger variability produced in eye position during the interruption. Both these latter observations support the notion that saccades are controlled by an internal negative feedback system. Also, the size of the remaining motor error during the interrupted period is one factor influencing when an IS resumes, but the variability in this measure is large particularly for smaller motor errors. Recent results have suggested that the resettable neural integrator involved in the feedback loop may be reset after each saccade through an exponential decay process. To probe the properties of the neural integrator, we varied the duration of interruption between the initial and resumed saccades and sought a systematic overshoot in the final eye position with increasing interruption period and variable initial saccade size. Our results showed the neural integrator does not decay during the pause period of interrupted saccades.

Activity of visuomotor burst neurons in the superior colliculus accompanying express saccades.

1. We recorded visuomotor burst neurons in the deeper layers of the superior colliculus while two monkeys (Macaca fascicularis) made short-latency saccades known as express saccades to visual targets in order to determine whether the visual discharge normally seen for these cells served as the premotor burst during express saccades. We then compared saccade-related activity during express saccades with that recorded during regular latency saccades and delayed saccades. 2. Saccade latency histograms for two monkeys during trials with a temporal gap between fixation-point offset and target onset showed a distinct peak of saccades around 70-80 ms. One monkey also showed an additional peak around 125 ms. 3. Express saccades were found on the average to have the same relationship of saccade peak velocity to saccade amplitude as regular latency saccades and delayed saccades. Express saccades tended to be somewhat more hypometric than the other classes of saccades. However, express saccades were clearly visually guided and not anticipatory responses. 4. For most cells studied (33/40), express saccades were accompanied by a single, uninterrupted burst of activity beginning 40-50 ms after target onset and continuing until sometime around the end of the saccade. For a smaller group of cells (7/40), two peaks of burst activity were seen, although the second peak was smaller and tended to occur late, after saccade onset. Across all cells, the peak of visuomotor cell activity during express saccades correlated just as well with target onset as it did with saccade onset. 5. When considered as discharge temporally aligned to the onset of the saccade, bursts accompanying express saccades tended to begin at approximately the same time as that for regular and delayed saccades. However, this discharge generally peaked earlier for express than for regular and delayed saccades. Also, the magnitude of discharge for express saccades was higher than that for delayed saccades throughout the burst. 6. When considered as discharge temporally aligned to the appearance of the target, bursts began earlier for express and regular saccade trials than for delayed saccade trials. Peak discharge tended to be greater for express saccades than for the other classes of saccades. 7. The results of this investigation are consistent with the suggestion that the visual burst of visuomotor neurons in the deeper layers of the superior colliculus plays a role in the initiation of express saccades similar to that played by the premotor burst for saccades of longer latency. The elevated discharge for express saccades supports the idea that the superior colliculus plays a more critical role in express saccade generation than in the generation of longer-latency saccades. The elevated discharge also suggests that visuomotor bursters do not code one-to-one for saccade velocity nor for saccade dynamic motor error.

The function of the cerebellar uvula in monkey during optokinetic and pursuit eye movements: single-unit responses and lesion effects.

The cerebellum is known to participate in visually guided eye movements. The cerebellar uvula receives projections from pontine nuclei that have been implicated in visual motion processing and the generation of smooth pursuit. Single-unit and lesion studies were conducted to determine how the uvula might further process these input signals. Purkinje cells and input fibers were recorded during a variety of visual and oculomotor paradigms. Most Purkinje cells were modulated in either an excitatory or inhibitory fashion by prolonged, horizontal optokinetic drum rotation. A small proportion of cells responded during smooth tracking of a small spot of light. As a paradox to the physiological data, lesions of the uvula produced a profound effect on smooth-pursuit eye movements. Initial eye velocity for pursuit in the direction contraversive to the lesion site was increased substantially following lesions in comparison with prelesion controls. The lesions also affected optokinetic nystagmus in the direction contraversive to the lesion, but not as drastically as they did pursuit. Overall the results suggest that the uvula is not in the neuronal pathway that directly controls pursuit, but instead serves to adjust the gain of this system as a result of abnormal periods of motion of the visual world.

Open-loop simulations of the primate saccadic system using burst cell discharge from the superior colliculus.

Saccade-related burst neurons (SRBNs) in the monkey superior colliculus (SC) have been hypothesized to provide the brainstem saccadic burst generator with the dynamic error signal and the movement initiating trigger signal. To test this claim, we performed two sets of open-loop simulations on a burst generator model with the local feedback disconnected using experimentally obtained SRBN activity as both the driving and trigger signal inputs to the model. First, using neural data obtained from cells located near the middle of the rostral to caudal extent of the SC, the internal parameters of the model were optimized by means of a stochastic hill-climbing algorithm to produce an intermediate-sized saccade. The parameter values obtained from the optimization were then fixed and additional simulations were done using the experimental data from rostral collicular neurons (small saccades) and from more caudal neurons (large saccades); the model generated realistic saccades, matching both position and velocity profiles of real saccades to the centers of the movement fields of all these cells. Second, the model was driven by SRBN activity affiliated with interrupted saccades, the resumed eye movements observed following electrical stimulation of the omnipause region. Once again, the model produced eye movements that closely resembled the interrupted saccades produced by such simulations, but minor readjustment of parameters reflecting the weight of the projection of the trigger signal was required. Our study demonstrates that a model of the burst generator produces reasonably realistic saccades when driven with actual samples of SRBN discharges.