Velocity prediction in corrective saccades during smooth-pursuit eye movements in monkey

Summary It has been noted in a variety of studies in both humans and monkeys that saccades made during smooth pursuit eye movements are usually quite accurate. Since saccades are known to be planned on the basis of neuronal information existing at some interval of time before the actual onset of the movement, it is generally accepted that some sort of prediction or use of visual motion velocity is combined with static position error in the execution of these saccades to moving targets. However, statistical treatment of this response in humans has provided evidence for alternative mechanisms, including a strategy of saccading ahead in the direction of target motion without any incorporation of actual speed information about target motion in the response. We reinvestigated this question quantitatively in the monkey on a large data base of saccades. We found evidence that supports the hypothesis that information about target speed per se is used in this species in the production of saccades to moving targets. Multiple linear regression analysis supported the hypothesis that information about the position error and the target velocity that exists at about 100 ms prior to the saccade onset are both required to provide a statistical explanation of saccade size during pursuit eye movements under the conditions of our experiments.     

Dynamic properties of eye position coded neurons in the alert monkey during saccades

Summary Single units in the regions of the III, IV and VI nuclei were recorded together with EOG's for horizontal and vertical eye positions in alert macaques. The sequential analysis of several dynamic parameters of the activity patterns in correlation to the saccade velocity for saccades in the on-direction leads to the results that: 1. eye position coded neurons can clearly be separated into two main classes [early peak (EP) and late peak (LP)] by means of their activity patterns during saccades in the on-direction; 2. the maximum impulse rate of EP neurons shows a better correlation with saccade velocity than the difference between maximum and initial impulse rate while the opposite is valid for LP neurons. EP neurons are likely to be motoneurons which initiate saccadic eye movements whereas LP neurons are too slow for this task because they reach their maximum impulse rate after half the saccadic time. The dynamic properties of LP neurons have several features similar to those of primary stretch receptors during ramp-like stretches. The possible influence of fusimotor activity on the oculomotor system is discussed. The fact that the relationship between dynamic index and saccade velocity shows subgroups of data supports the assumption that the state of alertness changes instantaneously in untrained monkeys.Supported in part by the National Eye Institute, U.S. Public Health Service under grant EY-00592 to Dr. G. Westheimer and by the Deutsche Forschungsgemeinschaft.     

Flexibility of saccade adaptation in the monkey: different gain states for saccades in the same direction

Saccadic accuracy, measured as the ratio of the size of a saccade to the size of the target step that elicits it, i.e., saccade gain, can be altered by jumping the target surreptitiously during the targeting saccade. The gain change produced by this paradigm does not generalize or transfer to saccades of all sizes. Instead, the amount of transfer decreases the more the tested saccade differs in amplitude and direction from that adapted. Here, we tested the limits of this saccade-size specificity by attempting to impose quite different gain states on saccades in the same direction. We altered the saccadic gain by intrasaccadic target jumps of 30% of the initial target step, either forward to produce a gain increase or backward to produce a gain decrease. Three different conditions were studied: (1) saccades to target steps of 20 degrees or 7 degrees were adapted in individual sessions with backward and forward jumps, respectively; (2) saccades to target steps of 20 degrees caused backward target jumps during the same session in which saccades to 7 degrees target steps caused forward steps; (3) the target jumps accompanying 20 and 7 degrees saccades were the same as in (2), but in addition, there were intermediate-sized saccades to 13.5 degrees target steps with no intrasaccadic target jumps. Saccadic gain adaptation was quite flexible. In condition 2, we could simultaneously increase the gain of saccades to 7 degrees target steps while decreasing the gain of saccades to 20 degrees steps in the same direction. Intermediate horizontal saccades to 13.5 degrees target steps experienced gain reductions (average: 6.9%), which were not the sum of gain changes expected from separate 20 degrees gain decreases and 7 degrees gain increases alone, as predicted from condition 1. If adaptation at 20 degrees and 7 degrees occurred while an animal also tracked a non-adapting 13.5 degrees target step (paradigm 3), the gain reduction of saccades to the 13.5 degrees step was reduced considerably (3.4%). Thus, the mechanism that adapts saccade size can support a robust gain increase for saccades of one size while simultaneously supporting a robust gain decrease for saccades only 13 degrees larger. Furthermore, the presence during adaptation of a non-adapted target step with a size intermediate to the two adapting steps reestablishes a nearly normal gain within only 6.5 degrees of a robust gain increase and decrease. These data indicate that saccadic gain adaptation can set very different gain states for saccades with rather similar vectors.     

The misclassification of blinks as saccades: implications for investigations of eye movement dysfunction in schizophrenia

It is important to have a simple. accurate method for recording eye movements. Of the two popular approaches commonly adopted, electro-oculography (EOG) and infrared oculography (IROG), IROG is often accepted as the more accurate, and it is the method that is currently used most frequently to examine eye movements in schizophrenia. This study investigated whether the misclassification of blinks as saccades affects saccade rates when the presence of a blink is determined using only IROG recordings of eye position. Both vertical electro-oculography (VEOG), which can be used to objectively identify blinks, and IROG were recorded while 17 schizophrenia patients and 19 healthy controls were presented with sinusoidal stimuli. Of the blinks identified with the VEOG for the total group of participants, a substantial number (37%) were misclassified as catch-up and anticipatory saccades when only the IROG was used. Furthermore, in the schizophrenia group, but not in the healthy control group, the use of the IROG led to a significant misclassification of blinks as anticipatory saccades. Therefore, when IROG alone is used to identify blinks, the misclassification of blinks as saccades is likely to introduce measurement error into estimates of saccade rates, particularly estimates of anticipatory saccade rates in schizophrenia patients.     

Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades.

Muscimol-induced inactivation of the monkey frontal eye field: effects on visually and memory-guided saccades. Although neurophysiological, anatomic, and imaging evidence suggest that the frontal eye field (FEF) participates in the generation of eye movements, chronic lesions of the FEF in both humans and monkeys appear to cause only minor deficits in visually guided saccade generation. Stronger effects are observed when subjects are tested in tasks with more cognitive requirements. We tested oculomotor function after acutely inactivating regions of the FEF to minimize the effects of plasticity and reallocation of function after the loss of the FEF and gain more insight into the FEF contribution to the guidance of eye movements in the intact brain. Inactivation was induced by microinjecting muscimol directly into physiologically defined sites in the FEF of three monkeys. FEF inactivation severely impaired the monkeys' performance of both visually guided and memory-guided saccades. The monkeys initiated fewer saccades to the retinotopic representation of the inactivated FEF site than to any other location in the visual field. The saccades that were initiated had longer latencies, slower velocities, and larger targeting errors than controls. These effects were present both for visually guided and for memory-guided saccades, although the memory-guided saccades were more disrupted. Initially, the effects were restricted spatially, concentrating around the retinotopic representation at the center of the inactivated site, but, during the course of several hours, these effects spread to flanking representations. Predictability of target location and motivation of the monkey also affected saccadic performance. For memory-guided saccades, increases in the time during which the monkey had to remember the spatial location of a target resulted in further decreases in the accuracy of the saccades and in smaller peak velocities, suggesting a progressive loss of the capacity to maintain a representation of target location in relation to the fovea after FEF inactivation. In addition, the monkeys frequently made premature saccades to targets in the hemifield ipsilateral to the injection site when performing the memory task, indicating a deficit in the control of fixation that could be a consequence of an imbalance between ipsilateral and contralateral FEF activity after the injection. There was also a progressive loss of fixation accuracy, and the monkeys tended to restrict spontaneous visual scanning to the ipsilateral hemifield. These results emphasize the strong role of the FEF in the intact monkey in the generation of all voluntary saccadic eye movements, as well as in the control of fixation.     

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

When a saccade occurs to an interesting object, visual fixation holds its image on the fovea and suppresses saccades to other objects. Electrical stimulation of the frontal eye field (FEF) has been reported to elicit saccades, and recently also to suppress saccades. This study was performed to characterize properties of the suppression of visually guided (Vsacs) and memory-guided saccades (Msacs) induced by electrical stimulation of the FEF in trained monkeys. For any given stimulation site, we determined the threshold for electrically evoked saccades (Esacs) at < or =50 microA and then examined suppressive effects of stimulation at the same site on Vsacs and Msacs. FEF stimulation suppressed the initiation of both Vsacs and Msacs during and about 50 ms after stimulation at stimulus intensities lower than those for eliciting Esacs, but did not affect the vector of these saccades. Suppression occurred for ipsiversive but not contraversive saccades, and more strongly for saccades with larger amplitudes and those with initial eye positions shifted more in the saccadic direction. The most effective stimulation timing for suppression was about 50 ms before saccade onset, which suggests that suppression occurred in the efferent pathway for generating Vsacs at the premotor rather than the motoneuronal level, most probably in the superior colliculus and/or the paramedian pontine reticular formation. Suppression sites of ipsilateral saccades were distributed over the classical FEF where saccade-related movement neurons were observed. The results suggest that the FEF may play roles in not only generating contraversive saccades but also maintaining visual fixation by suppressing ipsiversive saccades.     

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.     

The effects of illusory line motion on incongruent saccades: implications for saccadic eye movements and visual attention

A complex neural problem must be solved before a voluntary eye movement is triggered away from a stimulus (antisaccade). The location code activated by a stimulus must be internally translated into an appropriate signal to direct the eyes into the opposite visual field, while the reflexive tendency to look directly at the stimulus must be suppressed. No doubt these extra processes contribute to the ubiquitous slowing of antisaccades. However, there is no consensus on the cognitive mechanisms that contribute to the antisaccade programme. Visual attention is closely associated with the generation of saccadic eye movements and it has been shown that attention will track an illusion of line motion. A series of experiments combined this illusion with a saccadic eye movement that was congruent (i.e. directed towards), or incongruent with (i.e. direct away from), a peripheral target. Experiment 1 showed that congruent saccades had faster reaction times than incongruent saccades. In contrast, Experiments 2 and 3 demonstrated that, with illusory line motion, incongruent saccades now had faster reaction times than congruent saccades. These findings demonstrate that an illusory phenomenon can accelerate the processing of an incongruent relative to a congruent saccade.     

Representation of averaging saccades in the superior colliculus of the monkey

We tested the hypothesis that averaging saccades occur when two different saccades are prepared and executed simultaneously. The activity of saccade-related burst neurons (SRBNs) in the primate superior colliculus was recorded while monkeys made both non-averaging saccades to single targets and averaging saccades which directed the gaze between two simultaneously presented visual targets. For movements of comparable direction and amplitude, the activity measured during averaging and non-averaging saccades was statistically indistinguishable. These results are not consistent with the hypothesis that averaging saccades result from the simultaneous execution of two different saccades at the level of the collicular SRBNs. Instead, these findings indicate that averaging saccades are represented as single intermediate movements within the topographically organized map of these collicular cells.     

Periodic eye tracking in the monkey

1. Eye movements were measured in monkeys trained for visual tracking.

2. In response to periodic square wave target movements, monkeys do not show a significant reduction in the latency of saccadic movements.

3. Under similar conditions, human beings subconsciously reduce their latency and after several cycles are in step with the target.

4. In response to sinusoidal targets, monkeys show a latency or phase lag which increases monotonically with frequency starting at 0·3 c/s. Human beings can remain in phase with the target at frequencies up to 1·0 c/s.

5. Hence, monkeys do not exhibit the human predictive tracking response.

     

Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey

Recent work has shown that humans and monkeys utilize both retinal error and eye position signals to compute the direction and amplitude of saccadic eye movements (Hallett and Lightstone 1976a, b; Mays and Sparks 1980b). The aim of this study was to examine the role the frontal eye fields (FEF) and the superior colliculi (SC) play in this computation. Rhesus monkeys were trained to acquire small, briefly flashed spots of light with saccadic eye movements. During the latency period between target extinction and saccade initiation, their eyes were displaced, in total darkness, by electrical stimulation of either the FEF, the SC or the abducens nucleus area. Under such conditions animals compensated for the electrically induced ocular displacement and correctly reached the visual target area, suggesting that both a retinal error and eye position error signal were computed. The amplitude and direction of the electrically induced saccades depended not only on the site stimulated but also on the amplitude and direction of the eye movement initiated by the animal to acquire the target. When the eye movements initiated by the animal coincided with the saccades initiated by electrical stimulation, the resultant saccade was the weighted average of the two, where one weighing factor was the intensity of the electrical stimulus. Animals did not acquire targets correctly when their eyes were displaced, prior to their intended eye movements, by stimulating in the abducens nucleus area. After bilateral ablation of either the FEF or the SC monkeys were still able to acquire visual targets when their eyes were displaced, prior to saccade initiation, by electrical stimulation of the remaining intact structure. These results suggest that neither the FEF nor the SC is uniquely responsible for the combined computation of the retinal error and the eye position error signals.     

Different learned coordinate frames for planning trajectories and final positions in reaching

We previously reported that the kinematics of reaching movements reflect the superimposition of two separate control mechanisms specifying the hand's spatial trajectory and its final equilibrium position. We now asked whether the brain maintains separate representations of the spatial goals for planning hand trajectory and final position. One group of subjects learned a 30 degrees visuomotor rotation about the hand's starting point while performing a movement reversal task ("slicing") in which they reversed direction at one target and terminated movement at another. This task required accuracy in acquiring a target mid-movement. A second group adapted while moving to -- and stabilizing at -- a single target ("reaching"). This task required accuracy in specifying an intended final position. We examined how learning in the two tasks generalized both to movements made from untrained initial positions and to movements directed toward untrained targets. Shifting initial hand position had differential effects on the location of reversals and final positions: Trajectory directions remained unchanged and reversal locations were displaced in slicing whereas final positions of both reaches and slices were relatively unchanged. Generalization across directions in slicing was consistent with a hand-centered representation of desired reversal point as demonstrated previously for this task whereas the distributions of final positions were consistent with an eye-centered representation as found previously in studies of pointing in three-dimensional space. Our findings indicate that the intended trajectory and final position are represented in different coordinate frames, reconciling previous conflicting claims of hand-centered (vectorial) and eye-centered representations in reach planning.     

Eccentric eye and head positions in darkness induce deviation from the intended path

Head and gaze are aligned with the actual path during locomotion. Before a turn is made, gaze changes in the direction of the planned trajectory. We investigated whether eccentric horizontal head and/or eye position without vision causes deviations from the intended straight path. Twenty blindfolded healthy volunteers were asked to walk toward a previously seen target 10 m straight ahead. Various combinations of head and eye positions were tested (eye-in-head gaze straight ahead or 35° left or right with head straight ahead or 70° left or right). Head rotation to the left caused a gait deviation to the right (3.7°) and head rotation to the right caused a deviation to the left (2.7°; F(2,40)=34.966; P<0.00001). Eye position also showed a tendency to cause gait deviations opposite in direction to gaze, which was, however, not significant. Deviations from the intended straight path were largest with head rotation and eyes straight ahead (gaze 70° off target) or eyes opposite to head rotation (gaze 35° off target). Notably, when lateral eye deviation added to head rotation (gaze 105° off target), i.e., gaze is directed backward, mean deviations decreased (2.3° to the right and 1.2° to the left). Thus, we show that (1) eccentric head positions induce direction-specific gait deviations that are independent of concurrent environmental visual information, and (2) that gait deviations are contraversive to eye-head gaze rather than ipsiversive as reported by others for visually controlled locomotion. The direction of deviation may reflect the compensation of an expected or perceived deviation in the direction of gaze.     

Detection of different recumbent body positions from the electrocardiogram

Changes in body position alter the relative angle between ECG electrodes and the mean electric axis of the heart. These changes influence the time interval during which the projection of the electric dipole, on any ECG lead, is positive (R-wave). In this study, measurements of R-wave duration (RWD) were used to identify changes in body position, and two of its uncorrelated features were used to classify each heartbeat into four basic groups relating to four body positions (supine, prone, left-side, right-side). Data were acquired from healthy volunteers during controlled condition experiments that included well-defined sequences of body positions and simultaneous recordings of ECG leads I, II and III. Results showed over 90% correct identifications ofbody position changes when using any of the three leads. Lead II had the best performance for theclassification of body position and correctly classified 80% of heartbeats. Classification did not improve for a combination of two leads. The technique can be used to reveal additional important clinical information and can be easily implemented, in a variety of applications where ECG is recorded, such as sleep studies, Holter recordings and ischaemia detection.     

Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds

The neural response to amplitude-modulated sinus sounds (AM sound) was investigated in the auditory cortex and insula of the awake squirrel monkey. It was found that 78.1% of all acoustically driven neurons encoded the envelope of the AM sound; the remaining 21.9% displayed simple On, On/Off or Off responses at the beginning or the end of the stimulus sound. Those neurons with AM coding were able to encode the AM sound frequency in two different ways: (1) the spikes followed the amplitude modulation envelopes in a phaselocked manner; (2) the spike rate changed significantly with changing modulation frequencies. As reported in other species, the modulation transfer functions for rate showed higher modulation frequencies than the phaselocked response. Both AM codings exhibited a filter characteristic for AM sound. Whereas 46.6% of all neurons had the same filter characteristic for both the spike discharge and the phase-locked response, the remaining neurons displayed combinations of different filter types. The discharge pattern of a neuron to simple tone or noise bursts suggests the behaviour of this neuron when AM sound is used as the stimulus. Neurons with strong onset responses to tone/noise bursts tended to have higher phase-locked AM responses than neurons with weak onset responses. The spike rate maxima for AM sound showed no relation to the tone/noise burst discharge patterns. Varying modulation depth was encoded by the neuron's ability to follow the envelope cycles and not by the non-phase-locked spike rate frequency. The organization of the squirrel monkey's auditory cortex has previously been established by an anatomical study. We have added two new fields using physiological parameters. All fields investigated showed a clear functional separation for time-critical information processing. The best temporal resolution was shown by the primary auditory field (AI), the first-temporal field (T1) and the parainsular au ditory field (Pi). The neural data in these fields and the amplitude modulation frequency range of squirrel monkey calls suggest a similar correlation between vocalization and perception as in human psychophysical data for speech and hearing sensation. The anterior fields in particular failed to follow the AM envelopes. For the first time in a primate, the insula was tested with different sound parameters ranging from simple tone bursts to AM sound. It is suggested that this cortical region plays a role in time-critical aspects of acoustic information processing. The observed best frequencies covered the same spectrum as AI. As in the auditory fields, most neurons in the insula encoded AM sound with different filter types. The high proportion of neurons unable to encode AM sound (40.6%) and the low mean best modulation frequency (9.9 Hz) do not support a prominent role of the insula in temporal information processing.     

Punctate chemical lesions of striate cortex in the macaque monkey: effect on visually guided saccades

Summary Chemical agents which reversibly or irreversibly disrupt neural processing offer several advantages over traditional techniques for behavioral studies of the central nervous system. In order to evaluate the utility of chemical agents for a behavioral analysis of visual cortical function in primates, we have tested the effects of muscimol and ibotenic acid on the function of striate cortex in awake, behaving monkeys. We studied the monkey's ability to generate saccadic eye movements to visual targets at various locations in the visual field following an injection of one or the other chemical solution into a topographically identified location in striate cortex. Our results show that deficits in the generation of visually guided saccades following such injections are similar to those that result from surgical ablation of striate cortex, although recovery is more rapid following the injections. The experiments indicate that, with certain restrictions, chemical inactivation is a useful technique for behavioral analysis of visual cortical function.Supported by Schweizerische Stiftung für medizinische biologische Stipendien