Smooth eye movements evoked by electrical stimulation of the cat's superior colliculus

Head-fixed gaze shifts were evoked by electrical stimulation of the deeper layers of the cat superior colliculus (SC). After a short latency, saccades were triggered with kinematics similar to those of visually guided saccades. When electrical stimulation was maintained for more than 150–200 ms, postsaccadic smooth eye movements (SEMs) were observed. These movements were characterized by a period of approximately constant velocity following the evoked saccade. Depending on electrode position, a single saccade followed by a slow displacement or a staircase of saccades interspersed by SEMs were evoked. Mean velocity decreased with increasing deviation of the eye in the orbit in the direction of the movement. In the situation where a single evoked saccade was followed by a smooth movement, the duration of the latter depended on the duration of the stimulation train. In the situation where evoked saccades converged towards a restricted region of the visual field (goal-directed or craniocentric saccades), the SEMs were directed towards the centre of this region and their mean velocity decreased as the eye approached the goal. The direction of induced SEMs depended on the site of stimulation, as is the case for saccadic eye movements, and was not modified by stimulation parameters (place code). On the other hand, mean velocity of the movements depended on the site of stimulation and on the frequency and intensity of the current (rate code), as reported for saccades in the cat. The kinematics of these postsaccadic SEMs are similar to the kinematics of slow, postsaccadic correction observed during visually triggered gaze shifts of the alert cat. These results support the hypothesis that the SC is not exclusively implicated in the control of fast refixation of gaze but also in controlling postsaccadic conjugate slow eye movements in the cat.     

Stimulation of the superior colliculus in the alert cat

Summary Electrical stimulation of the cat superior colliculus (SC), in conjunction with the accurate measurement of elicited eye movements and histologically verified electrode positions, has revealed a striking antero-posterior variation in collicular organization. Three zones could be defined in the SC on the basis of eye movement patterns and associated neck muscle EMG activity evoked from the deeper layers. The Anterior zone was coextensive with the central 25 ° of the visual retinotopically coded map contained in the superficial layers. Saccades evoked from this zone were also retinotopically coded, and the latency of EMG activity depended on the position of the eye in the orbit. A similar observation applies to the entire monkey SC. The Intermediate zone was coextensive with the 25 °–70 ° of visual projections. Saccades evoked from this region were goal-directed and were associated with invariant, short latency EMG responses. The Posterior zone was found in the extreme caudo-lateral portion of the SC. Eye movements evoked from this zone were centering saccades associated with constant latency EMG activity. The present results in conjunction with previously demonstrated antero-posterior variations in projections to the SC, suggest that the motor strategies controlling gaze shifts toward visual targets vary depending on the location of the target in the visual field.     

The role of the predorsal bundle in head and body movements elicited by electrical stimulation of the superior colliculus in the Mongolian gerbil

Summary Thirty-two Mongolian gerbils received bilateral chronic implants of stainless steel electrodes in the superior colliculus. The movements elicited by electrical stimulation were recorded on videotape and measured by means of a computer-assisted image analyzing procedure. Ipsiversive body movements were elicited by stimulation of the anterior part of the superior colliculus. Contraversive head and body movements could be elicited by stimulation over the entire superior colliculus. Amplitudes of head and body movements were dependent upon both stimulation parameters (current and train duration) and the animal's posture at stimulus onset. In a second experiment, the predorsal bundle was cut at its decussation by means of a stereotaxic microknife. After such cuts, contraversive turns were either abolished or were replaced by ipsiversive movements. Ipsiversive movements were unaffected by the knife cuts. This experiment provides evidence that the distinct types of movements that can be elicited by collicular stimulation are subserved by anatomically separate output pathways. This study was supported by grant no. A6313 from the Natural Sciences and Engineering Research Council of Canada to M. A. Goodale     

Eye position signals in cat superior colliculus

Summary Single unit activity was studied in the intermediate and deep layers of the superior colliculus in two trained cats. Eye movements were recorded with a magnetic search coil, the head being fixed. Discharge rates which varied as a function of eye position were consistently observed in 7 of 67 (about 10%) of the sample of eye movement-related units. These units showed similar changes in firing rate as a function of eye position in total darkness and during task related fixation of visual targets and thus appear to convey an eye position signal. Their activity may originate either from proprioception or from corollary discharge.     

Eye and head movements to auditory targets

Summary Three adult female monkeys were trained to direct their gaze toward auditory targets. When the animals were free to move their heads about the vertical axis, this was accomplished with shortlatency, coordinated eye-head movements reminiscent of responses to visual targets. The similarity of response to auditory and visual targets suggests a common motor program elicited by stimuli of different modalities. Since these modalities do not share the same reference system, this implies a remapping between the two reference systems.This research has been supported by the National Institutes of Health Research Grant NS 09343, awarded by the National Institute of Neurological Diseases and Stroke, National Aeronautics and Space Administration Grant NCR 22-009-798, and the National Institute of General Medical Science, NIGMS 5 T01-GM01064     

Behavior evoked by electrical stimulation of the hamster superior colliculus

Summary Syrian golden hamsters were implanted with fixed or moveable stimulating electrodes aimed at the superior colliculus (SC). Behavior was observed in response to trains of 0.1 ms pulses at 200 Hz while the animals were moving freely in an open arena or in their home cages. At threshold stimulating currents, the responses consisted almost entirely of freezing or contraversive turning, which occurred in two forms: fast turns, resembling orienting movements to sunflower seeds, and slow turns that were smooth and continuous. Other responses, including head raising and lowering, ipsiversive turning and backing movements were seen occasionally. Increasing the stimulating current usually gave a variety of responses, including circling movements, prolonged freezing, ipsilateral movements and running escape behavior. The sites in SC giving freezes at threshold tended to be located superficially (SO and above), or deep (SGP and below), while sites giving turns were in the intermediate layers. Most freeze sites occurred in the rostro-medial SC that represents the upper visual field, while turn sites occurred predominantly in caudo-lateral SC. Apart from the turns, most of the stimulated responses resembled natural defensive behavior, supporting the view that SC in rodents plays a role in organizing responses to predators, as well as in orienting behavior.     

The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem omnipause neurons

The superior colliculus has long been recognized as an important structure in the generation of saccadic displacements of the visual axis. Neurons with presaccadic activity encoding saccade vectors are topographically organized and form a motor map. Recently, neurons with fixation-related activity have been recorded at the collicular rostral pole, at the area centralis representation or fixation area. Another collicular function which deals with the maintenance of fixation behavior by means of active inhibition of orientation commands was then suggested. We tested that hypothesis as it relates to the suppression of gaze saccades (gaze = eye in space = eye in head + head in space) in the head-free cat by increasing the activity of the fixation cells at the rostral pole with electrical microstimulation. Long stimulation trains applied before gaze saccades delayed their initiation. Short stimuli, delivered during the gaze saccades, transiently interrupted both eye and head components. These results provide further support for a role in fixation behavior for collicular fixation neurons. Brainstem omnipause neurons also exhibit fixation-related activity and have been shown to receive a direct excitatory input from the superior colliculus. To determine whether the collicular projection to omnipause neurons arises from the fixation area, the deep layers of the superior colliculus were electrically stimulated either at the rostral pole including the fixation area or in more caudal regions where stimulation evokes orienting responses. Forty-nine neurons were examined in three cats. 61% of the neurons were found to be orthodromically excited by single-pulse stimulation of the rostral pole, whereas only 29% responded to caudal stimulation. In addition, stimuli delivered to the rostral pole activated, on average, omnipause neurons at shorter latencies and with lower currents than those applied in caudal regions. These results suggest that excitatory inputs to omnipause neurons from the superior colliculus are principally provided by the fixation area, via which the superior colliculus could play a role in suppression of gaze shifts.     

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.     

Discharges of superior colliculus neurons during head and eye movements of the alert cat

Summary 452 single neurons from the superior colliculus were recorded in awake and non-paralysed cats. 75 neurons were obtained from cats with unrestrained horizontal head movements.228 neurons remained unaffected by saccadic eye movements. Eye movement related discharge followed the onset of saccades in 156 neurons either only in the presence of a visual pattern (92 neurons) or in darkness, too (64 neurons). The latter reaction type probably depends on eye muscle afferents.In 48 neurons eye movement related activity preceded the onset of eye movements. 12 neurons fired in synchrony with eye movements of any direction (type I). 30 neurons were excited during contralaterally directed eye versions within or into the contralateral head related hemifield. They were inhibited when the eyes moved within or into the ipsilateral head related hemifield (type II). 6 neurons with constant maintained activity during fixation were inhibited by ipsilaterally directed saccades, but remained unaffected by contralateral eye movements.Head movement related discharge followed the onset of head movements in 20 neurons only in presence of a visual pattern and also in darkness in 6 neurons. Ipsilateral head movements or postures strongly suppressed maintained activity and visual responsiveness of some neurons.15 neurons discharged in synchrony with and prior to contralateral head movements. Ipsilateral head movements inhibited these neurons. Activation or inhibition were usually related to movement and to posture, exceptionally to movement or to posture.Electrical stimulation of recording sites of these neurons through the recording microelectrode elicits contralateral head movements.     

Saccadic eye movements following injection of lidocaine into the superior colliculus

Summary Ablation of the superior colliculus (SC) has generally produced limited deficits in the initiation of saccadic eye movements, usually an increase in the latency of saccades. However, recent studies using muscimol, a GABA agonist, to block afferents to the SC showed deficits in not only latency but in amplitude and velocity of saccades as well. These greater deficits might be dependent upon the testing of saccades shortly after the damage of SC before any compensation for the deficits could develop. The present experiments tested this hypothesis by injecting a local anesthetic into SC. The anesthetic inactivated the cells entirely rather than just deafferenting them, but still allowed testing immediately after the injection. Clear deficits were observed following injection of lidocaine into the SC. The amplitudes of saccades to visual targets were shortened, and the peak velocities of the saccades were reduced even if the reduced amplitude of the saccades was taken into account. Latency of saccades usually increased. The deficits were limited to the area of the visual field that overlapped the movement fields of the cells near the injection site. If the movement fields were in the periphery, saccades to the periphery were shortened following the injection of lidocaine. If the movement fields were near the center of gaze, saccades into the area were shortened, but the monkey was able to make saccades over the visual field related to the affected area to more peripheral targets. These experiments support the view that the SC normally conveys information on the amplitude and velocity of saccadic eye movements, but that gradual compensation can be made over time by other pathways when damage to the structure occurs.     

Location of saccade-related neurons in the macaque superior colliculus

Summary The locations of saccade-related neurons were studied in the superior colliculi of two adult rhesus monkeys (Macaco, mulatta) by placing marking lesions at the sites of physiologically characterized cells and comparing these histologically identified sites with the collicular laminae and acetylcholinesterase (AChE)-rich patches. Three major conclusions were drawn on the basis of 39 histologically identified sites at which saccade-related neurons were recorded. First, saccade-related neurons were distributed from the ventral half of the optic layer through the deep gray layer, and were most concentrated in the intermediate gray and white layers. Second, there was a clear relationship between the discharge characteristics of these saccade-related neurons and the depths at which they were found. Neurons having presaccadic bursts, defined as clipped and partially-clipped, tended to be encountered more dorsally, and neurons that did not have bursts (undipped) were encountered more ventrally. Although cells having different discharge characteristics seemed to be organized along a dorsoventral axis, there was no compelling evidence that these properties were specified by their laminar locations. Third, there was no clear correlation between the locations of saccade-related neurons and the distribution of individual AChE-rich patches. Saccade-related cells were found both in the caudal superior colliculus where patches were located and in the rostral superior colliculus where patches were not found; both within and between the two tiers of AChE-rich patches in the caudal superior colliculus; and both within and between individual AChE-rich patches. However, the depth-level at which saccade-related neurons occurred generally matched the region bounded by the two tiers of AChE-rich patches in the intermediate and deep layers, and the dorsal and ventral extent of saccade-related neurons was the same as that of the AChE-rich patches.     

Minimal synaptic delay in the saccadic output pathway of the superior colliculus studied in awake monkey

The synaptic organization of the saccade-related neuronal circuit between the superior colliculus (SC) and the brainstem saccade generator was examined in an awake monkey using a saccadic, midflight electrical-stimulation method. When microstimulation (50–100 A, single pulse) was applied to the SC during a saccade, a small, conjugate contraversive eye movement was evoked with latencies much shorter than those obtained by conventional stimulation. Our results may be explained by the tonic inhibition of premotor burst neurons (BNs) by omnipause neurons that ceases during saccades to allow BNs to burst. Thus, during saccades, signals originating from the SC can be transmitted to motoneurons and seen in the saccade trajectory. Based on this hypothesis, we estimated the number of synapses intervening between the SC and motoneurons by applying midflight stimulation to the SC, the BN area, and the abducens nucleus. Eye position signals were electronically differentiated to produce eye velocity to aid in detecting small changes. The mean latencies of the stimulus-evoked eye movements were: 7.9±1.0 ms (SD; ipsilateral eye) and 7.8±0.9 ms (SD; contralateral eye) for SC stimulation; 4.8±0.5 ms (SD; ipsilateral eye) and 5.1±0.7 ms (SD; contralateral eye) for BN stimulation; and 3.6±0.4 ms (SD; ipsilateral eye) and 5.2±0.8 ms (SD; contralateral eye) for abducens nucleus stimulation. The time difference between SC- and BN-evoked eye movements (about 3 ms) was consistent with a disynaptic connection from the SC to the premotor BNs.     

Stimulation in the rostral pole of monkey superior colliculus: effects on vergence eye movements

Recent studies have indicated that the superior colliculus (SC), traditionally considered to be saccade-related, may play a role in the coding of eye movements in both direction and depth. Similarly, it has been suggested that omnidirectional pause neurons are not only involved in the initiation of saccades, but can also modulate vergence eye movements. These new developments provide a challenge for current oculomotor models that attempt to describe saccade-vergence coordination and the neural mechanisms that may be involved. In this paper, we have attempted to study these aspects further by investigating the role of the rostral pole of the SC in the control of vergence eye movements. It is well-known that, by applying long-duration electrical stimulation to rostral sites in the monkey SC, saccadic responses can be prevented and interrupted. We have made use of these properties to extend this paradigm to eye movements that contain a substantial depth component. We found that electrical intervention in the rostral region also has a clear effect on vergence. For an eye movement to a near target, stimulation leads to a significant suppression and change in dynamics of the pure vergence response during the period of stimulation, but the depth component cannot be prevented entirely. When these paradigms are implemented for 3D refixations, the saccade is inactivated, as expected, while the vergence component is often suppressed more than in the case of the pure vergence. The data lead us to conclude that the rostral SC, presumably indirectly via connections with the pause neurons, can affect vergence control for both pure vergence and combined 3D responses. Suppression of the depth component is incomplete, in contrast to the directional movement, and is often different in magnitude for 3D refixations and pure vergence responses. The results are discussed in connection with current models for saccade-vergence interaction.     

Adjustment of saccade characteristics during head movements

Summary Saccade characteristics have been studied during coordinated eyehead movements in monkeys. Amplitude, duration, and peak velocity of saccades with head turning were compared with saccades executed while the head was artificially restrained. The results indicate that the saccade characteristics are modulated as a function of head movement, hence the gaze movement (eye+head) exactly matches saccades with head fixed. Saccade modulation is achieved by way of negative vestibulo-ocular feedback. The neck proprioceptors, because of their longer latency, are effective only if the head starts moving prior to the onset of saccade. It is concluded that saccades made with head turning are not ballistic movements because their trajectory is not entirely predetermined by a central command.     

Comparison of saccades evoked by visual stimulation and collicular electrical stimulation in the alert monkey

Summary In the alert monkey we have compared the properties of saccades elicited by a visual stimulus (V-saccades) with those generated by electrical stimulation in the superior colliculus (E-saccades). We found that whereas there exists a graded relation betweenE-saccade amplitude and current strength,E-saccade direction is remarkably independent of electrical stimulation parameters. At sufficiently high current strengths (about 20 A),E-saccades are consistently directed toward the center of the movement field of nearby cells, except when stimulation is performed at sites near the collicular borders. Further interesting differences between the amplitude and direction behaviour were observed when the variability inE-saccade vectors, obtained with fixed stimulation parameters, was analyzed. In all cases,E-saccade amplitude scatter exceeds direction scatter, suggesting the possibility of a polar coordinate organization for the coding of saccade metrics. These data are compared withV-saccade scatter data, recently obtained in the human (Van Opstal and Van Gisbergen 1989 c). Finally, an analysis of saccade dynamics shows thatE-saccades can reachV-saccadic velocities at higher current strengths. However, at near-threshold current strengths, whereE-saccade amplitude decreases (see above), we found at most stimulation sites (22/37) thatE-saccades are consistently slower thanV-saccades of the same amplitude. Possible mechanisms underlying the collicular role in saccade generation are discussed.     

Eye position modulates the electromyographic responses of neck muscles to electrical stimulation of the superior colliculus in the alert cat

Rapid gaze shifts are often accomplished with coordinated movements of the eyes and head, the relative amplitude of which depends on the starting position of the eyes. The size of gaze shifts is determined by the superior colliculus (SC) but additional processing in the lower brain stem is needed to determine the relative contributions of eye and head components. Models of eye–head coordination often assume that the strength of the command sent to the head controllers is modified by a signal indicative of the eye position. Evidence in favor of this hypothesis has been recently obtained in a study of phasic electromyographic (EMG) responses to stimulation of the SC in head-restrained monkeys (Corneil et al. in J Neurophysiol 88:2000–2018, 2002b). Bearing in mind that the patterns of eye–head coordination are not the same in all species and because the eye position sensitivity of phasic EMG responses has not been systematically investigated in cats, in the present study we used cats to address this issue. We stimulated electrically the intermediate and deep layers of the caudal SC in alert cats and recorded the EMG responses of neck muscles with horizontal and vertical pulling directions. Our data demonstrate that phasic, short latency EMG responses can be modulated by the eye position such that they increase as the eye occupies more and more eccentric positions in the pulling direction of the muscle tested. However, the influence of the eye position is rather modest, typically accounting for only 10–50% of the variance of EMG response amplitude. Responses evoked from several SC sites were not modulated by the eye position.     

Role of monkey superior colliculus in saccade averaging

Summary We have investigated the involvement of collicular movement cells in the monkey in the execution of averaging saccades, elicited by a visual double-step stimulus. We found that, qualitatively, most (12/14) movement cells were recruited during averaging saccades in roughly the same way as for comparable visually-elicited saccades to single targets (V-saccades). However, movement-cell responses during averaging saccades in trials where the target suddenly changed direction were often less intense than for a comparable V-saccade. In these cases, the averaging responses were observed to be also slower than V-saccades of the same amplitude. Firing rate and double-step saccade dynamics were found to be significantly correlated in 9/14 cells tested. Several hypotheses for the collicular role in the generation of averaging saccades are discussed.     

Target selection and saccade generation in monkey superior colliculus

The superior colliculus (SC) of the monkey has been shown to be involved in not only initiation of saccades but in the selection of the target to which the saccade can be directed. The present experiments examine whether SC neuronal activity related to target selection is also related to saccade generation. In an asynchronous target task, the monkey was required to make a saccade to the first of two spots of light to appear. Using choice probability analysis over multiple trials, we determined the earliest time at which neurons in the SC intermediate layers indicated target selection. We then determined how closely the neuronal selection was correlated to saccade onset by using our asynchronous reaction time task, which allowed the monkey to make a saccade to the target as soon as the selection had been made. We found that the selection became evident at widely differing times for different neurons. Some neurons indicated target selection just before the saccade (close to the pre-saccadic burst of activity), others did so at the time of the visual response, and some showed an increase in their activity even before the target appeared. A fraction of this pre-stimulus bias resulted from a priming effect of the previous trial; a saccade to the target in the movement field on the previous trial produced both a higher level of neuronal activity and a higher probability for a saccade to that target on the current trial. We found that most of the neurons (76%) showed a correlation between selection time and reaction time. Furthermore, within this 76% of neurons, many indicated a selection very early during the visual response. There was no evidence of a sequence from target selection first and saccade selection later, but rather that target selection and saccade initiation are intertwined and are probably inseparable.     

Human gaze shifts in which head and eyes are not initially aligned

Most studies of rapid orienting gaze shifts generated by combined eye and head movements have focused on an experimental condition in which gaze displacements are started with the subject's eyes in the normal straight-ahead position in the orbit. Such an experimental approach does not permit a clear identification of the input signal to the head motor system, because target offset angle is the same for both the eye and head. We have studied gaze shifts in human subjects which began with the visual axis straight ahead relative to the body (i.e., gaze or line of sight aligned with body sagittal plane) and with head offset from straight ahead at various angular positions. In our experimental conditions, the amplitude of head movement during a gaze shift was nearly equal to the angular distance between the target position and the starting head position (target-re-head), even though subjects were not specifically instructed to move their heads. This observation contrasts with other published reports in the literature showing considerable varibility amongst subjects in the amplitude of head rotation within a given task and between tasks. The difference may be related to the initial conditions which required subjects to align the eye and head on specific starting targets, since others have shown that requiring head alignment enhances head displacement. The amplitude of the saccadic eye movement was not determined by either the target's position relative to the starting eye or head positions. The value that best described the eye movement amplitude was the eye position in the orbit at the end of the saccade. This was nearly equal to target-rehead until a saturation eye position in the orbit was attained.     

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.