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.     

Eye movements induced by linear acceleration on a parallel swing

1. Horizontal and vertical eye movements were induced in normal human subjects by sinusoidal linear acceleration on a parallel swing. The swing frequency was 0.3 Hz and the peak horizontal and vertical acceleration ranged from 0.17 to 0.48 and 0.03 to 0.34 g, respectively. Eye movements were recorded with the scleral search coil technique. 2. With the subjects seated in the dark to stimulate the otolith-ocular reflex, swing displacement along the interaural axis induced horizontal eye movements with a mean sensitivity to translation (ST) (peak eye velocity/peak swing velocity) of 3.8 to 4.7 degrees/m and a mean phase shift (eye velocity re swing velocity) of -152 to -160 degrees. Vertical eye movements had ST and phase values comparable to those of the horizontal eye movements. When the subjects sat facing forward so that the horizontal linear accelerations occurred in the occipitonasal axis, almost identical vertical but no consistent horizontal eye movements were induced. In each case the horizontal and vertical eye movements were proportional to the horizontal and vertical displacement of the swing. 3. With the subject seated in the light looking to an earth-fixed target (synergistic visual-vestibular interaction), the gain (peak eye velocity/peak target velocity) of induced eye movements was near 1, and the phase was compensatory (i.e., approximately -180 degrees) for all stimuli (even at target velocities at which the pursuit gain was less than 1). Subjects were able to suppress the otolith-ocular responses by fixating on a target attached to the swing. The ST decreased by an order of magnitude compared with measurements in the dark without a fixation target. 4. Subjects were able to augment the ST (horizontal and vertical) by imagining an earth-fixed target. Halving the distance of the imagined target approximately doubled the ST. 5. In two of three subjects tested, the ST measured with mental alerting in the dark adaptively increased (approximately doubled) after 20 min of continuous synergistic visual-vestibular interaction. The subject who did not show an adaptive increase in ST began with the highest value of the 10 normal subjects. 6. We conclude that during linear accelerations of the head the otolith signal is correctly interpreted as head movement and not rotation of the gravity vector. The otolith-ocular reflex interacts with the visual pursuit system to improve ocular stability during translational head movements.     

Eye and head movements evoked by electrical stimulation of monkey superior colliculus

Summary In unrestrained animals of many species, electrical stimulation at sites in the superior colliculus evokes motions of the head and eyes. Collicular stimulation in monkeys whose heads are rigidly fixed is known to elicit a saccade whose characteristics depend on the site stimulated and are largely independent of electrical stimulation parameters and initial eye position.This study examined what role the colliculus plays in the coding of head movements. A secondary aim was to demonstrate the effects of such electrical stimulation parameters as pulse frequency and intensity. Rhesus monkeys were free to move their heads in the horizontal plane; head and eye movements were monitored. As in previous studies, eye movements evoked by collicular stimulation were of short latency, repeatable, had a definite electrical threshold, and did not depend on the initial position of the eye in the orbit. By contrast, evoked head movements were extremely variable in size and latency, had no definite electrical threshold, and did depend on initial eye position. Thus when the eyes approached positions of extreme deviation, a head movement in the same direction became more likely. These results suggest that the superior colliculus does not directly code head movements in the monkey.     

Eye movements evoked by proprioceptive stimulation along the body axis in humans

Proprioceptive input arising from torsional body movements elicits small reflexive eye movements. The functional relevance of these eye movements is still unknown so far. We evaluated their slow components as a function of stimulus frequency and velocity. The horizontal eye movements of seven adult subjects were recorded using an infrared device, while horizontal rotations were applied at three segmental levels of the body [i.e., between head and shoulders (neck stimulus), shoulders and pelvis (trunk stimulus), and pelvis and feet (leg stimulus)]. The following results were obtained: (1) Sinusoidal leg stimulation evoked an eye response with the slow component in the direction of the movement of the feet, while the response to trunk and neck stimulation was oriented in the opposite direction (i.e., in that of the head). (2) In contrast, the gain behavior of all three responses was similar, with very low gain at mid- to high frequencies (tested up to 0.4 Hz) but increasing gain at low frequencies (down to 0.0125 Hz). We show that this gain behavior is mainly due to a gain nonlinearity for low angular velocities. (3) The responses were compatible with linear summation when an interaction series was tested in which the leg stimulus was combined with a vestibular stimulus. (4) There was good correspondence of the median gain curves when eye responses were compared with psychophysical responses (perceived body rotation in space; additionally recorded in the interaction series). However, correlation of gain values on a single-trial basis was poor. (5) During transient neck stimulation (smoothed position ramp), the neck response noticeably consisted of two components – an initial head-directed eye shift (phasic component) followed by a shift in the opposite direction (compensatory tonic component). Both leg and neck responses can be described by one simple, dynamic model. In the model the proprioceptive input is fed into the gaze network via two pathways which differ in their dynamics and directional sign. The model simulates either leg or neck responses by selecting an appropriate weight for the gain of one of the pathways (phasic component). The interaction results can also be simulated when a vestibular path is added. This model has similarities to one we recently proposed for human self-motion perception and postural control. A major difference, though, is that the proprioceptive input to the gaze-stabilizing network is weak (restricted to low velocities), unlike that used for perception and postural control. We hold that the former undergoes involution during ontogenesis, as subjects depend on the functionally more appropriate vestibulo-ocular reflex. Yet, the weak proprioceptive eye responses that remain may have some functional relevance. Their tonic component tends to stabilize the eyes by slowly shifting them toward the primary head position relative to the body support. This applies solely to the earth-horizontal plane in which the vestibular signal has no static sensitivity. Received: 10 October 1997 / Accepted: 22 January 1998     

Shift in saccadic direction induced in humans by proprioceptive manipulation: a comparison between memory-guided and visually guided saccades

It is nowadays generally recognized that saccades to remembered targets are planned in a craniotopic frame of reference by combining retinal input with eye position signal. The origin of the eye position signal is still a matter of controversy, however. Does it arise from an efferent copy or is it supplied by the sensory receptors with which the extraocular muscles are endowed? When applied to skeletal muscles, vibration elicits spindle responses simulating a stretching of the vibrated muscle. When vibration is applied to the inferior rectus muscle (IR), it induces the illusion that a stationary fixating point is moving upward. Here we attempted to change the initial eye position signal supplied to the oculomotor system before a memory- or visuo-guided saccade to a 10° left target by applying mechanical vibration to the IR muscle. We wanted to determine whether modifying extraocular proprioceptive cues during the programming phase of a saccade might affect the latter's trajectory. In the memory-guided condition, it was observed that the saccades ended lower down when vibration was applied than in the control condition. Conversely, the visuo-guided saccades were not affected by the vibration. The above results mean first that extraocular proprioceptive cues are used as an initial eye position signal when a memory guided saccade has to be planned. Secondly, they suggest that extraocular proprioception may not be used to produce a visuo-guided saccade, or that this type of saccade is computed solely on the basis of retinal cues.     

Temporary inactivation in the primate motor thalamus during visually triggered and internally generated limb movements

To better understand the contribution of cerebellar- and basal ganglia-receiving areas of the thalamus [ventral posterolateral nucleus, pars oralis (VPLo), area X, ventral lateral nucleus, pars oralis (VLo), or ventral anterior nucleus, pars parvicellularis (VApc)] to movements based on external versus internal cues, we temporarily inactivated these individual nuclei in two monkeys trained to make visually triggered (VT) and internally generated (IG) limb movements. Infusions of lignocaine centered within VPLo caused hemiplegia during which movements of the contralateral arm rarely were performed in either task for a short period of time ( approximately 5-30 min). When VT responses were produced, they had prolonged reaction times and movement times and a higher incidence of trajectory abnormalities compared with responses produced during the preinfusion baseline period. In contrast, those IG responses that were produced remained relatively normal. Infusions centered within area X never caused hemiplegia. The only deficits observed were an increase in reaction time and movement amplitude variability and a higher incidence of trajectory abnormalities during VT trials. Every other aspect of both the VT and IG movements remained unchanged. Infusions centered within VLo reduced the number of movements attempted during each block of trials. This did not appear to be due to hemiplegia, however, as voluntary movements easily could be elicited outside of the trained tasks. The other main deficit resulting from inactivation of VLo was an increased reaction time in the VT task. Finally, infusions centered within VApc caused IG movements to become slower and smaller in amplitude, whereas VT movements remained unchanged. Control infusions with saline did not cause any consistent deficits. This pattern of results implies that VPLo and VLo play a role in the production of movements in general regardless of the context under which they are performed. They also suggest that VPLo contributes more specifically to the execution of movements that are visually triggered and guided, whereas area X contributes specifically to the initiation of such movements. In contrast, VApc appears to play a role in the execution of movements based on internal cues. These results are consistent with the hypothesis that specific subcircuits within the cerebello- and basal ganglio-thalamo-cortical systems preferentially contribute to movements based on external versus internal cues.     

Eye movements elicited by electrical stimulation of area PG in the monkey.

1. Eye positions of monkeys were tracked while low-current electrical stimulation was delivered to area PG of the posterior parietal cortex. Stimulation was delivered while monkeys were in darkness, while they were in a dimly illuminated room, or while they actively fixated on small lamps to receive a liquid reward. 2. Resulting eye movements fell into one of three categories, depending roughly on the area stimulated. Stimulation of caudal regions generally resulted in saccades that were of approximately equivalent amplitudes and directions. When more rostral areas were stimulated, saccades were generally produced that directed the eyes toward roughly the same position in the head. Distributed throughout all regions were sites for which elicited saccades did not fall clearly into either of these coordinate bases. Stimulation of lateral areas produced low-velocity eye movements that were directed ipsilaterally from the stimulated hemisphere. 3. Stimulation made while monkeys fixated on target lamps produced saccades with more variability and less amplitude than those produced while monkeys were in darkness. Low-velocity eye movements could only be elicited while monkeys were in darkness. 4. Craniocentric saccades typically brought the eyes to within a 10-20 degrees area, and saccades could not be produced when the initial eye position was near this area. Craniocentric saccades were always greater than 5 degrees in amplitude. 5. It is concluded that area PG is organized into at least two zones that differ in the way by which they code saccades. A caudal region codes saccades in a way similar to that found in the frontal cortex and superior colliculus of primates. A rostral region codes saccades in a craniocentric manner, although it is restricted only to gross redirection of gaze without the accuracy monkeys are capable of using in directing their eyes.     

Role of the monkey substantia nigra pars reticulata in orienting behaviour and visually triggered arm movements

The role of the substantia nigra pars reticulata (SNpr) has been studied in the head-free monkey during orienting behaviour in response to visual instruction signals triggering head positioning and conditioned arm movement. During the behavioural responses we recorded the electromyographic activities of neck muscles and triceps brachii, head movement, horizontal electrooculogram and single unit activity of SNpr neurons. Activity of 38 neurons located in the medial part of SNpr were analysed during the visuo-motor task. Forty percent of these units showed a moderate decrease in tonic firing rate during postural preparation preceding the orientation toward eccentric visual signal. This decrease, unrelated with saccadic eye movements per se, was followed by a marked pause observed when the rewarded stimulus was switched on and the conditioned arm movement was executed to get the reward. These data suggest that the pause in discharge of these SNpr neurons are time locked with behaviourally relevant visual stimuli and/or appropriate motor responses.     

Neuronal activity in the primate motor thalamus during visually triggered and internally generated limb movements.

Single-unit recordings were made from the basal-ganglia- and cerebellar-receiving areas of the thalamus in two monkeys trained to make arm movements that were either visually triggered (VT) or internally generated (IG). A total of 203 neurons displaying movement-related changes in activity were examined in detail. Most of these cells (69%) showed an increase in firing rate in relation to the onset of movement and could be categorized according to whether they fired in the VT task exclusively, in the IG task exclusively, or in both tasks. The proportion of cells in each category was found to vary between each of the cerebellar-receiving [oral portion of the ventral posterolateral nucleus (VPLo) and area X] and basal-ganglia-receiving [oral portion of the ventral lateral nucleus (VLo) and parvocellular portion of the ventral anterior nucleus (VApc)] nuclei that were examined. In particular, in area X the largest group of cells (52%) showed an increase in activity during the VT task only, whereas in VApc the largest group of cells (53%) fired in the IG task only. In contrast to this, relatively high degree of task specificity, in both VPLo and VLo the largest group of cells ( approximately 55%) burst in relation to both tasks. Of the cells that were active in both tasks, a higher proportion were preferentially active in the VT task in VPLo and area X, and the IG task in VLo and VApc. In addition, cells in all four nuclei became active earlier relative to movement onset in the IG task compared with the VT task. These results demonstrate that functional distinctions do exist in the cerebellar- and basal-ganglia-receiving portions of the primate motor thalamus in relation to the types of cues used to initiate and control movement. These distinctions are most clear in area X and VApc, and are much less apparent in VPLo and VLo.     

Eye movements in the cat evoked by electrical stimulation of the outer geniculate body

New data were obtained in experiments with unanesthetized animals showing that electrical stimulation of the structures of the outer geniculate body of the cat elicits goal-directed eye movements. Relationships were found between eye-movement amplitude and direction and the position of the eye at the instant of stimulation, as well as the position of the stimulating electrodes in the outer geniculate body. A scheme is proposed for the multilevel interaction of the visual and oculomotor systems during their functioning, and a possible relation is discussed between the described phenomenon and the mechanisms responsible for the foveation of objects during their recognition.Translated from Fiziologicheskii Zhurnal SSSR imeni I. M. Sechenova, Vol. 69, No. 2, pp. 167–175, February, 1983.     

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

Constant frequency microstimulation of the paramedian pontine reticular formation (PPRF) in head-restrained monkeys evokes a constant velocity eye movement. Since the PPRF receives significant projections from structures that control coordinated eye-head movements, we asked whether stimulation of the pontine reticular formation in the head-unrestrained animal generates a combined eye-head movement or only an eye movement. Microstimulation of most sites yielded a constant-velocity gaze shift executed as a coordinated eye-head movement, although eye-only movements were evoked from some sites. The eye and head contributions to the stimulation-evoked movements varied across stimulation sites and were drastically different from the lawful relationship observed for visually-guided gaze shifts. These results indicate that the microstimulation activated elements that issued movement commands to the extraocular and, for most sites, neck motoneurons. In addition, the stimulation-evoked changes in gaze were similar in the head-restrained and head-unrestrained conditions despite the assortment of eye and head contributions, suggesting that the vestibulo-ocular reflex (VOR) gain must be near unity during the coordinated eye-head movements evoked by stimulation of the PPRF. These findings contrast the attenuation of VOR gain associated with visually-guided gaze shifts and suggest that the vestibulo-ocular pathway processes volitional and PPRF stimulation-evoked gaze shifts differently.     

Amplitude of human head movements associated with horizontal saccades

 Human saccades may or may not be associated with head movements. To date, little attention has been devoted to the mechanisms determining head movement recruitment and scaling. Normal human subjects made horizontal, centrifugal saccades along an encircling array of light-emitting diodes. Measurements of gaze, head, and eye-in-head angle were made at the conclusion of the head movement (or at the end of the eye movement in eye-only saccades). We found that head movement amplitude (ΔH) related in a simple fashion to the eye eccentricity that would have resulted if the gaze shift had been performed without a head movement. Plots of ΔH vs this predicted eye eccentricity (E _PRED) had a central flat region in which gaze shifts were unaccompanied by head movements (the eye-only range) and two flanking lobes in which ΔH was a linear function of E _PRED (the eye-head ranges). ΔH correlated with E _PRED better than with gaze shift amplitude, as would be expected if head movements were controlled so as to keep eye eccentricity within a particular range. Head movement tendencies were quantified by the width of the eye-only range, the slope of the eye-head range, and the width of the region within which the eye was likely to be found at the conclusion of the completed gaze-shifting behavior (the customary ocular motor range). The measures ranged widely in these normal subjects: 35.8±31.9° for the eye-only range (mean±SD), 0.77±0.16 for the slope of the eye-head range, and 44.0±23.8° for the customary ocular motor range. Yet for a given subject, the measurements were reproducible across experimental sessions, with the customary ocular motor range being the most consistent measure of the three. The form of the ΔH vs E _PRED plots suggests that the neural circuitry underlying eye-head coordination carries out two distinct functions – gating the head movement and scaling the head movement. The reason for the large intersubject variability of head movement tendencies is unknown. It does not parallel intersubject differences in full-scale eye (in orbit) range or full-scale neck range. Received: 25 June 1998 / Accepted: 23 November 1998     

Short-latency fixational saccades induced by luminance increments

We investigated the effect of peripheral visual stimulation on small-amplitude saccades that occur naturally during fixation. Two macaque monkeys were rewarded for fixating while a colorful stimulus flickered randomly in the periphery. Reverse correlation revealed a lawful relationship between the stimulus sequence and saccade occurrences: on average, a transient increase in stimulus intensity evoked saccades at a latency of approximately 70 ms. The spectral tuning of this increase was roughly, but not exactly, consistent with a pure luminance increase. We conclude that peripheral luminance increases can evoke fixational saccades.     

Eye movements induced by lateral acceleration steps Effect of visual context and acceleration levels

 Eye movement responses were obtained from six normal subjects exposed to randomly ordered rightwards/leftwards linear acceleration steps of 0.05 g, 0.1 g or 0.24 g amplitude and 650 ms duration along the inter-aural axis. With the instruction to gaze passively into the darkness, compensatory nystagmus was evoked with slow-phase velocity sensitivity of 49° s⁻¹ g ⁻¹. When subjects viewed earth-fixed targets at 30 cm, 60 cm or 280 cm, eye movements at 130 ms from motion onset were proportional to acceleration and inversely proportional to target distance, before the onset of visually guided eye movements. Our results show that a modulation with viewing distances of the earliest human otolith-ocular reflexes occurs in the presence of pure linear acceleration. However, full compensation was not attained for the nearer targets and higher accelerations. Received: 31 January 1996 / Accepted: 30 September 1996