Evoked Eye Movements Research Articles

The cervico-ocular reflex in intact and chronically labyrinthectomized frogs

Eye movements in response to horizontal oscillation of the body against the stationary head (cervico-ocular reflex) were measured with search coils in the frequency range between 0.02 and 1.0 Hz in intact and chronic bilaterally labyrinthectomized frogs. The evoked eye movements were compensatory in direction but only about 1–2% of the amplitude of the stimulus (± 5–20%). In chronic bilaterally labyrinthectomized frogs ( n = 5) very similar response characteristics were measured. The very small amplitudes of these responses in controls and in frogs with removed labyrinthine organs render this reflex functionally irrelevant for both gaze stabilization and recovery from dynamic vestibular deficits after a loss of labyrinthine function.

Disconnection of parietal and occipital access to the saccadic oculomotor system.

The experiment explored the networks through which signals arising from visual areas of cortex control saccadic eye movements. Electrical stimulation of the inferior parietal and the occipital cortex (here termed the "posterior eye fields") normally evokes saccadic eye movements. We replicated previous reports that these evoked eye movements ceased after large tectal ablations. This initial finding suggested that the "posterior eye fields" depended on a single route of access to the saccade generator, one descending through the superior colliculus (SC). On closer examination, the critical lesion appeared to be one which removed the SC and cut efferents from the frontal eye field (FEF) coursing nearby. Subsequently we confirmed that eye movements evoked from the posterior eye fields ceased after cooling the SC, or cutting its efferents- but only when one of these procedures was combined with FEF ablation. Thus, visual signals from the occipital and inferior parietal cortex have more than one, but perhaps only two routes of access to the oculomotor system. One passes through the superior colliculus, the other through the frontal eye field. Ancillary experiments revealed that inferior parietal and FEF ablations, alone or combined, do not disrupt saccades evoked from the occipital lobe. Striate and prestriate areas can therefore use their own direct input to the SC or to the basal ganglia to drive saccadic eye movements.

Vertical nystagmus provoked by locally applied calorization at the vertical semicircular canals: a study in pigeons.

Calorization of the vertical semicircular canals in pigeons was performed by irrigation of water through a polyethylene cannula, that was attached at a selected site to the bony wall of the anterior or posterior canal of the labyrinth. The temperature differences between the stimulated site and the corresponding location inside the contralateral mastoid were detected by two thermistors. (a) Calorization of an anterior or posterior canal evoked a dissociated vertical nystagmus in both eyes. (b) The direction of the nystagmus and of the vertical slow phase velocity proved to be temperature-dependent. (c) The vertical eye movements disappeared when the stimulated canal was placed horizontally during calorization. (d) During parabolic flight the vertical and horizontal eye movements, elicited by sustained calorization, disappeared during short periods of microgravity and proved to be dependent to the g load. (e) All vertical canal calorizations evoked eye movements in the plane parallel to the stimulated canal. Left and right eye moved in opposite vertical directions, depending on the selected site of calorization on the vertical canal. (f) The same mode (warm or cold) of calorization of an anterior canal provoked similar vertical movements of both eyes as compared to the vertical eye movements that were induced by calorization of the contralateral posterior canal. The results are discussed in view of the 'convection current' and the 'expansion/contraction' theory and they are compared to previously reported results of vestibular nerve stimulation.

Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections

Physiological (intracortical microstimulation) and anatomical (transport of horseradish peroxidase conjugated to wheat germ agglutinin as shown by tetramethyl benzidine) approaches were combined in the same animals to reveal the locations, extents, and cortical connections of the frontal eye fields (FEF) in squirrel, owl, and macaque monkeys. In some of the same owl and macaque monkeys, intracortical microstimulation was also used to evoke eye movements from dorsomedial frontal cortex (the supplementary motor area). In addition, in all of the owl and squirrel monkeys, intracortical microstimulation was also used to evoke body movements from the premotor and motor cortex situated between the central dimple and the FEF. These microstimulation data were directly compared to the distribution of anterogradely and retrogradely transported label resulting from injections of tracer into the FEF in each monkey. Since the injection sites were limited to the physiologically defined FEF, the demonstrated connections were solely those of the FEF. To aid in the interpretation of areal patterns of connections, the relatively smooth cortex of owl and squirrel monkeys was unfolded, flattened, and cut parallel to the flattened surface. Cortex of macaque monkeys, which has numerous deep sulci, was cut coronally. Reciprocal connections with the ipsilateral frontal lobe were similar in all three species: dorsomedial cortex (supplementary motor area), cortex just rostral (periprincipal prefrontal cortex) to the FEF, and cortex just caudal (premotor cortex) to the FEF. In squirrel and owl monkeys, extensive reciprocal connections were made with cortex throughout the caudal half of the lateral fissure and, to a much lesser extent, cortex around the superior temporal sulcus. In macaque monkeys, only sparse connections were present with cortex of the lateral fissure, but extensive and dense connections were made with cortex throughout the caudal one-third to one-half of the superior temporal sulcus. In addition, very dense reciprocal connections were made with the cortex of the lateral, or inferior, bank of the intraparietal sulcus. Contralateral reciprocal connections in all three species were virtually limited to regions that correspond in location to the FEF and the supplementary motor area. The results of this study reveal connections between the physiologically defined frontal eye field and cortical regions known to participate in higher order visual processing, short-term memory, multimodal, visuomotor, and skeletomotor functions.(ABSTRACT TRUNCATED AT 400 WORDS)

Spontaneous and Evoked Eye Movements in Polyphemus Pediculus (Cladocera: Crustacea): A Case of Open-Loop Tracking?

ABSTRACT Polyphemus eye movements were recorded in both pitching and yawing planes, both in a static visual environment and with a sinusoidally moving stimulus. Spontaneous eye movements (average amplitude 1·7°) had different properties in the two planes, with trembling movements predominating in the pitching plane. A contour-sharpening function is proposed for these movements. An attempt to analyse the eye movement response system using a Bode diagram shows a very poor fit to the data, leading to the conclusion that a closed-loop control system is an inappropriate model in this case. The evoked eye movements are most convincingly represented by a model in which the time the stimulus takes to traverse a restricted sensitive zone in the central region of the eye controls the duration of a subsequent constant angular velocity saccade. The direction of the response movement follows the direction of the stimulus. A small-object tracking function is proposed for these movements.

The properties of goal-directed eye movements evoked by microstimulation of the cerebellar vermis in the cat

The properties of eye movements evoked by microstimulation of the cerebellar vermis, lobules V–VII, were investigated in encéphale isolé cats. The evoked eye movements tended to reach the same final goal in the orbit irrespective of initial eye position. The goal position depended on stimulus intensity. In contrast with the monkey, the goal of the eye movement lay within the oculomotor range. The goal position of the eye movements evoked by simultaneous stimuli delivered to two sites corresponded with the point which was obtained by the vectorial addition of the two eye movements evoked by the stimulation of each site. These findings suggest that the cat vermal lobules V–VII play an important role in the control of horizontal and vertical eye position in the orbit.

Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements.

We studied single neurons in the frontal eye fields of awake macaque monkeys and compared their activity with the saccadic eye movements elicited by microstimulation at the sites of these neurons. Saccades could be elicited from electrical stimulation in the cortical gray matter of the frontal eye fields with currents as small as 10 microA. Low thresholds for eliciting saccades were found at the sites of cells with presaccadic activity. Presaccadic neurons classified as visuomovement or movement were most associated with low (less than 50 microA) thresholds. High thresholds (greater than 100 microA) or no elicited saccades were associated with other classes of frontal eye field neurons, including neurons responding only after saccades and presaccadic neurons, classified as purely visual. Throughout the frontal eye fields, the optimal saccade for eliciting presaccadic neural activity at a given recording site predicted both the direction and amplitude of the saccades that were evoked by microstimulation at that site. In contrast, the movement fields of postsaccadic cells were usually different from the saccades evoked by stimulation at the sites of such cells. We defined the low-threshold frontal eye fields as cortex yielding saccades with stimulation currents less than or equal to 50 microA. It lies along the posterior portion of the arcuate sulcus and is largely contained in the anterior bank of that sulcus. It is smaller than Brodmann's area 8 but corresponds with the union of Walker's cytoarchitectonic areas 8A and 45. Saccade amplitude was topographically organized across the frontal eye fields. Amplitudes of elicited saccades ranged from less than 1 degree to greater than 30 degrees. Smaller saccades were evoked from the ventrolateral portion, and larger saccades were evoked from the dorsomedial portion. Within the arcuate sulcus, evoked saccades were usually larger near the lip and smaller near the fundus. Saccade direction had no global organization across the frontal eye fields; however, saccade direction changed in systematic progressions with small advances of the microelectrode, and all contralateral saccadic directions were often represented in a single electrode penetration down the bank of the arcuate sulcus. Furthermore, the direction of change in these progressions periodically reversed, allowing particular saccade directions to be multiply represented in nearby regions of cortex.(ABSTRACT TRUNCATED AT 400 WORDS)

Dynamics of maculo-ocular reflexes in the frog

Compensatory torsional and vertical eye movements were recorded in the frog during sinusoidal linear acceleration along the longitudinal and transverse body axes, respectively. Stimulus frequencies ranged between 0.1 and 1.0 Hz and peak accelerations from 0.01 g to 0.1 g corresponding to body tilts ranging from 0.57 to 5.7°. In addition, static compensatory eye movements were studied during fore-and-aft and lateral body tilt over ranges of± 10°. The evoked eye movements were generally quite small (± 0.5°). Dynamic gain (rotation of the eye/apparent rotation of gravity direction) was 0.10–0.20 at 0.1 Hz and decreased to about 0.05 at 1.0 Hz. The gain of vertical eye movements was somewhat higher than that of torsional eye movements. Phase lag relative to peak accelerations increased from about 10° to about 45° over the same frequency range. Static compensatory eye movements evoked by nose-up and ipsilateral side-up tilt were larger in amplitude than those evoked by nose-down and ipsilateral side-down tilt. Static gain (rotation of the eye/tilt of the whole body) was about 0.10 for vertical and about 0.06 for torsional eye movements. No consistent eye movements could be evoked by vertical sinusoidal accelerations (maximal modulation amplitudes± 0.025g). The results indicate that, as in other vertebrates, maculo-ocular reflexes contribute to gaze stabilization in the frog mainly during low frequency and static head and body tilts.

Effect of amphetamine on optokinetically evoked head and eye movements in the squirrel monkey.

The effect of amphetamine sulfate injection on head and eye movements evoked by optokinetic stimulus was studied in squirrel monkeys. No change was found in the gain of optokinetic-oculomotor and optokinetic-caputomotor functions, even after the maximum dose (0.5 mg/kg) of amphetamine. Also, no change in eye-head coordination was found. However, amphetamine facilitated the frequency of head nystagmus, whereas that of eye nystagmus did not change. When the poststimulus responses were studied in the dark, both nystagmoid head movement and optokinetic after eye nystagmus showed first phase and second phase. A different effect was found in the duration of these two phases suggesting the existence of distinct generators. Moreover, the synchronized onsets of head and eye nystagmus in both phases, and synchronized occurrence of quick phases indicated the existence of shared neural circuitry between head and eye movements.

Compensatory head and eye movements in the frog and their contribution to stabilization of gaze

Compensatory head movements, recorded in unrestrained frogs, were compared to compensatory eye movements recorded from animals that had their head fixed. Movements were evoked by oscillating the animal in the dark (vestibular stimulation) or in the light in front of an earth-fixed, patterned visual background (combined stimulation) or by rotating vertical black and white bars (optokinetic stimulation) around the stationary animal. Oscillations occurred in the horizontal plane at frequencies between 0.025 and 0.5 Hz. Gain and phase values of head and eye movements, relative to stimulus movements were calculated. Evoked eye movements were limited in amplitude to +/- 3-6 degrees, increasing with the size of the animal. Head movements were limited to +/- 30-40 degrees. Resetting fast-phases of both head and eyes were very rarely observed during sinusoidal stimulation and no eye movements were recorded in the absence of intended head movements. Vestibularly evoked head movements exhibited a frequency-dependent threshold that was not observed for vestibulo-ocular responses. Above threshold, the gain of evoked head responses increased and reached a frequency-dependent plateau at which the system behaved approximately linearly. Within the linear range, gain of vestibularly evoked responses increased with frequency (from 0.04 at 0.025 Hz to 0.75 at 0.5 Hz) and phase lead decreased (from about 80 degrees to 0 degrees). Vestibularly evoked eye movements similarly increased in gain from 0.05 to 0.56 and decreased in phase lead from about 56 degrees to 10 degrees over the same frequency range. Optokinetically evoked head and eye movements had their highest gains (about 0.8 and 0.5) at low constant velocities (less than or equal to 1-4 degrees/S) or frequencies (less than or equal to 0.025 Hz). At higher constant velocities or frequencies the gain dropped. The phase lag increased from close to zero (at 0.025 Hz) to about 60 degrees for the head and to about 20 degrees for the eye movements (at 0.25 Hz). These phase lags are explained by reaction times of the evoked movements of about 600 ms (head) and 200 ms (eyes). Combined stimulation evoked compensatory head movements with gain and phase values that were frequency-independent in the linear range. Head movements compensated for about 80-90% of the imposed gaze shift with a small phase lag (0-10 degrees). Evoked eye movements were found to be large enough in amplitude and fast enough in time to enable a frog to stabilize its gaze exclusively with slow phase compensatory movements for a large variety of frequency and amplitude combinations. The two motor systems controlling movements of the head and the eye are matched in such a way that the non-linearities of the evoked eye movements can compensate for the non-linearities of the evoked head movements.

A comparison of the horizontal and vertical optokinetic reflexes of the rabbit.

The horizontal and vertical monocular optokinetic reflexes of the rabbit were measured under closed-loop and open-loop conditions. A random noise, optokinetic stimulus subtending 70×70 deg was presented to the left eye of rabbits placed in front of a rear projection tangent screen. The position of the right eye (nonstimulated) was measured using an infrared light projection technique. During open-loop optokinetic stimulation the eye position signal was fed back to sum with a time-integrated velocity command signal driving the optokinetic stimulus. The dynamics of eye movements evoked by horizontal and vertical optokinetic stimulation were different. Horizontally evoked eye movements never exceeded a deviation of 15 deg before being interrupted by resetting saccades, which returned the eye past the primary position. By contrast, vertical eye deviations greater than 20 deg were often maintained for intervals exceeding 10 s without resetting. The closed-loop gain of optokinetically evoked horizontal eye movements was higher for monocular posterior-anterior optokinetic stimulation than for anterior-posterior stimulation. The vertical optokinetic gain for up-down stimulation was slightly greater than the gain for down-up stimulation. The vertical up-down, open-loop optokinetic gain was greater than the down-up gain over a range of retinal slip velocities of 0.5–5.0 deg/s. Measurement of the horizontal vestibulo-ocular reflex during simultaneous horizontal optokinetic stimulation demonstrated that visual and vestibular information combine linearly to produce reflex eye movements. These data suggest that the higher gain of the horizontal optokinetic reflex may compensate in part for the reduced gain of the horizontal vestibulo-ocular reflex at lower angular accelerations of the head. An equivalent vertical optokinetic gain would be obviated by the contribution of the utricular otoliths to the vertical vestibulo-ocular reflex at low frequencies of head movement.

Eye movements evoked by microstimulation of dorsal cap of inferior olive in the rabbit.

1. Microstimulation was used in an attempt to activate selectively neurons of the dorsal cap of the inferior olive in unanesthetized rabbits, and the eye movements evoked by this microstimulation were recorded. 2. Trains of microstimulation (20--50 microA, 0.1- to 0.2-ms pulses, 10--60 pulses/s, 2--8 s duration) evoked low-velocity conjugate eye movements directed toward the side of the stimulated olive. These evoked eye movements were interrupted by resetting eye movements in the opposite direction and could be evoked only if the rabbit was in darkness. 3. The velocity of the evoked eye movements increased during a stimulus train and gradually decreased after the stimulation was terminated. 4. The low-velocity eye movements appeared to combine with eye movements evoked by vestibular stimulation without any significant interaction. 5. After transection of the olivocerebellar pathway or destruction of the contralateral cerebellar flocculus, dorsal cap microstimulation no longer evoked ipsilaterally directed eye movements.

Frontal ‘oculomotor’ area in alert cat. I. Eye movements and neck activity evoked by stimulation

(1) Stimulation within cat frontal lobe elicited saccadic eye movements whose maximum velocity was significantly greater than that of normal spontaneous saccades. (2) The majority (90%) of stimulated cortical points yielded eye movements whose directions and amplitudes were independent of the position of the eye in the orbit. The direction of these eye movements depended on the site being stimulated, with a discrete and orderly representation of directions existing within the cortex. (3) A lesser number of cortical points (10%) yielded centering movements whose directions and amplitudes depended on the position of the eye in the orbit, rather than on the site being stimulated. (4) Evoked neck muscle activation frequently preceded evoked eye movements by some 15–30 msec. This timing was compatible with a coordinated head-eye orientating response. (5) On the basis of the directions, and the latencies, of evoked eye movements, the cat frontal oculomotor area could be divided into two subregions, a ‘medial’ and a ‘lateral’. (6) The ‘medial’ area included the mesial wall of the hemisphere with a portion of the lower lip of the cruciate sulcus, and the medial wall of the presylvian sulcus. This area yielded contraversive eye movements with shorter latencies (average 45 msec). (7) The ‘lateral’ area included primarily the lateral wall of the presylvian sulcus. It yielded predominantly centering eye movements, and ipsiversive movements with longer latencies (65 msec). (8) The functional characteristics of the ‘medial’ area, as revealed by focal stimulation, resembled those of the monkey frontal eye field.

Visually evoked eye movements: Effects of labyrinthectomy

Nystagmus responses of cats to both optokinetic and flicker stimuli were studied before and after unilateral and bilateral labyrinthectomy. Destruction of the labyrinths served to reduce significantly the number of eye movements to each type of the visual stimuli. The opposite-direction after-nystagmus elicited by the optokinetic stimulus were abolished by bilateral labyrinthectomy. No changes occurred in the frequency of the flash nystagmus response that could be ascribed to body position. Thus, the data confirm previous work by others, but suggest species differences with regard to several properties of visually evoked nystagmus.

Fastigial Evoked Eye Movement and Brain Stem Neuronal Behavior in the Alert Monkey

Single units in the brain stem were recorded in the awake monkey during concomitant adequate vestibular stimulation, eye movement, and electrical stimulation of the fastigial nucleus in areas that produce short-latency horizontal saccades. Forty-eight percent of the recorded brain stem cells were associated with eye movements; 40% respond only to head rotation; and the remainder are unrelated to either. The activity of the majority of the eye movement-related cells was similar for spontaneously and fastigially evoked saccades. The activity of the head rotation and unrelated cells show no consistent relationship to fastigial stimulation.

Discharge properties of neurons in the monkey thalamus tested with angular acceleration, eye movement and visual stimuli

Monkeys were trained to make visually evoked eye movements while undergoing simultaneous head rotation. Single units were recorded in the pregeniculate nucleus (PGN). PGN neurons discharged during each saccade, but there was no change in activity with horizontal head acceleration or with various combinations of head and smooth pursuit eye movements as previously described in the cat. Therefore, the anatomical homology between LGNv and PGN does not appear to have a neurophysiological basis. Neurons in the oral part of VPL or occasionally in VPI discharged as a function of head velocity but not with saccades, smooth pursuit or fixation eye movements, nor after brief light flashes or during smooth pursuit across structured backgrounds. This suggests that VPLo and VPI are only vestibular relay nuclei and not concerned with vestibular/visual or vestibular/oculomotor interactions.

Responses of fibers in medial longitudinal fasciculus (MLF) of alert monkeys during horizontal and vertical conjugate eye movements evoked by vestibular or visual stimuli.

Extracellular recordings were obtained from 37 histologically identified MLF fibers near the trochlear nucleus in alert monkeys trained to perform a visual tracking task and subjected to adequate horizontal and vertical vestibular stimulation. The behavioral paradigm permitted independent quantitative assessment of a fiber's response to eye or head movements. 2. According to their discharge pattern, almost all MLF fibers were placed in one of two classes: 1) Horizontal burst-tonic fibers (n = 20). During both vestibular and visually evoked eye movements, burst-tonic fibers discharged in strict relation to horizontal eye movements, exhibiting a burst of activity prior to on-direction saccades and steady firing related to horizontal eye position during fixations. 2) Vertical vestibular plus eye-position fibers (n = 14). Vertical fibers discharged in relation to vertical head velocity in the absence of eye movements and in relation to vertical eye position in the absence of head movement, and paused with saccades in any direction. 3. The quantitative similarity of horizontal burst-tonic fiber discharge to that of ipsilateral medial rectus oculomotoneurons suggests that burst-tonic fibers provide the major excitatory synaptic drive to medial rectus motoneurons during conjugate eye movements of vestibular or visual origin. 4. The discharge pattern of vertical vestibular plus eye-position fibers is significantly different from that of oculomotoneurons, suggesting that additional neural processing of vertical fiber information must occur in the mesencephalon. 5. The functional dichotomy of horizontal and vertical MLF fibers and their contrasting discharge patterns provide new evidence for the anatomic and functional separation of horizontal and vertical eye movement mechanisms in the pons and mesencephalon, respectively.

Visually evoked eye movements in the mouse ( Mus musculus)

Visually evoked eye movements were observed and measured in one inbred strain of the mouse (C57BL/6J) and in one inter-strain hybrid. This was done by observing pupillary movements while a mouse was restrained inside of a test apparatus that presented the mouse with slowly moving stripes and allowed the experimenter to view the mouse's pupil using i.r. illumination. Slow eye movements (smooth pursuits) occurred only in the direction of drum rotation. Rapid eye movements (saccades) occurred only in the opposite direction. The eye position often appeared to follow a fixed location on the drum while the direction of drum rotation was being reversed. Eye movements did not occur when the stripes were rotated in the dark. Mutants having retinal degeneration (C57BL/6J rd le/rd le) had oscillatory eye movements independent of visual stimulus luminance or motion. Hybrid animals performed more frequent following movements than inbred animals. It is concluded that M. musculus has visually-evoked eye movements, including the optokinetic nystagmus, and that the test described is suited to screen mice for subtle hereditary defects in vision.

Eye movements evoked by focal stimulation of the cats superior colliculus

Focal electrical stimulation through the recording microelectrode was performed in the superior colliculus of spinally anesthetized and of unanesthetized cats. Eye movements were recorded by conventional EOG methods and by a light beam reflected from a corneal mirror. Spontaneous and evoked saccades have a similar amplitude-duration relation, peak velocities of about 300°/sec and maximal amplitudes of 30°. Amplitude, speed and latency of evoked eye movements depend strongly upon strength of stimulating current. With increasing penetration depth, the threshold intensity of the electrical stimulus decreases abruptly when the electrode approaches the intermediate tectal layer, to decrease only slightly with further downward penetration. Some of the characteristics of oculomotor output of a tectal subarea parallel those of the visual response characteristics of single neurons of the same region. Receptive field position and evoked eye position, preferred direction of single neurons, and direction of saccades are in good agreement when the eyes are in primary position at the onset of stimulation. But direction and amplitude of electrically induced saccades change with changing initial eye position to bring the eyes to a constant position. This indicates that the stimulation point determines eye position with reference to the cat's head or body. In a few instances, electrical stimulation elicited nystagmus or suppressed spontaneous nystagmus.

Visual receptive fields of neurons in pulvinar, nucleus lateralis posterior and nucleus suprageniculatus thalami of the cat

In young animals, simple receptive fields (RFs) are experience insensitive, while complex RFs possess certain adaptivity. Complex cells are higher order output neurons, which transmit information to other visual cortical areas and properties of their RFs are formed later during the course of development, but these cells have worse detector characteristics than simple cells. The visual responses of pulvinar-lateral posterior (Pulv-LP) can be increased in situations of interest to visual stimuli, and the activity of Pulv-LP neurons depend on visually evoked eye movements. Experiments with lesions of Pulv-LP also show that this structure is involved in processes of visual discrimination and attention. Consequently, it is concluded from these data that potentiation of pulvinar input results in improvement of visual discrimination. The reduction of the orientation selectivity of complex cells after tetanization of the pulvinar input can mean that the selective attention to visual stimuli (our potentiation of pulvinar input is considered as a model of this process) actively depresses (masks) some reactions of sign detectors, and as a result, sub serves the finer discrimination of visual patterns. The involvement of pulvinar input into the process of the formation of complex RFs is important for providing the plasticity of cortical reactions.