scholarly journals Reversible Inactivation of Monkey Superior Colliculus. I. Curvature of Saccadic Trajectory

1998 ◽  
Vol 79 (4) ◽  
pp. 2082-2096 ◽  
Author(s):  
Hiroshi Aizawa ◽  
Robert H. Wurtz

Aizawa, Hiroshi and Robert H. Wurtz. Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. J. Neurophysiol. 79: 2082–2096, 1998. The neurons in the intermediate layers of the monkey superior colliculus (SC) that discharge before saccadic eye movements can be divided into at least two types, burst and buildup neurons, and the differences in their characteristics are compatible with different functional contributions of the two cell types. It has been suggested that a spread of activity across the population of the buildup neurons during saccade generation may contribute to the control of saccadic eye movements. The influence of any such spread should be on both the horizontal and vertical components of the saccade because the map of the movement fields on the SC is a two-dimensional one; it should affect the trajectory of saccade. The present experiments used muscimol injections to inactivate areas within the SC to determine the functional contribution of such a spread of activity on the trajectory of the saccades. The analysis concentrated on saccades made to areas of the visual field that should be affected primarily by alteration of buildup neuron activity. Muscimol injections produced saccades with altered trajectories; they became consistently curved after the injection, and successive saccades to the same targets had similar curvatures. The curved saccades showed changes in their direction and speed at the very beginning of the saccade, and for those saccades that reached the target, the direction of the saccade was altered near the end to compensate for the initially incorrect direction. Postinjection saccades had lower peak speeds, longer durations, and longer latencies for initiation. The changes in saccadic trajectories resulting from muscimol injections, along with the previous observations on changes in speed of saccades with such injections, indicate that the SC is involved in influencing the eye position during the saccade as well as at the end of the saccade. The changes in trajectory when injections were made more rostral in the SC than the most active burst neurons also are consistent with a contribution of the buildup neurons to the control of the eye trajectory. The results do not, however, support the hypothesis that the buildup neurons in the SC act as a spatial integrator.

1994 ◽  
Vol 72 (6) ◽  
pp. 2754-2770 ◽  
Author(s):  
E. L. Keller ◽  
J. A. Edelman

1. We recorded the spatial and temporal dynamics of saccade-related burst neurons (SRBNs) found in the intermediate layers of the superior colliculus (SC) in the alert, behaving monkey. These burst cells are normally the first neurons recorded during radially directed microelectrode penetrations of the SC after the electrode has left the more dorsally situated visual layers. They have spatially delimited movement fields whose centers describe the well-studied motor map of the SC. They have a rather sharp, saccade-locked burst of activity that peaks just before saccade onset and then declines steeply during the saccade. Many of these cells, when recorded during saccade trials, also have an early, transient visual response and an irregular prelude of presaccadic activity. 2. Because saccadic eye movements normally have very stereotyped durations and velocity trajectories that vary systematically with saccade size, it has been difficult in the past to establish quantitatively whether the activity of SRBNs temporally codes dynamic saccadic control signals, e.g., dynamic motor error or eye velocity, where dynamic motor error is defined as a signal proportional to the instantaneous difference between desired final eye position and the actual eye position during a saccade. It has also not been unequivocally established whether SRBNs participate in an organized spatial shift of ensemble activity in the intermediate layers of the SC during saccadic eye movements. 3. To address these issues, we studied the activity of SRBNs using an interrupted saccade paradigm. Saccades were interrupted with pulsatile electrical stimulation through a microelectrode implanted in the omnipauser region of the brain stem while recordings were made simultaneously from single SRBNs in the SC. 4. Shortly after the beginning of the stimulation (which was electronically triggered at saccade onset), the eyes decelerated rapidly and stopped completely. When the high-frequency (typically 300-400 pulses per second) stimulation was terminated (average duration 12 ms), the eye movement was reinitiated and a resumed saccade was made accurately to the location of the target. 5. When we recorded from SRBNs in the more caudal colliculus, which were active for large saccades, cell discharge was powerfully and rapidly suppressed by the stimulation (average latency = 3.8 ms). Activity in the same cells started again just before the onset of the resumed saccade and continued during this saccade even though it has a much smaller amplitude than would normally be associated with significant discharge for caudal SC cells.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 69 (3) ◽  
pp. 965-979 ◽  
Author(s):  
K. Hepp ◽  
A. J. Van Opstal ◽  
D. Straumann ◽  
B. J. Hess ◽  
V. Henn

1. Although the eye has three rotational degrees of freedom, eye positions, during fixations, saccades, and smooth pursuit, with the head stationary and upright, are constrained to a plane by ListingR's law. We investigated whether Listing's law for rapid eye movements is implemented at the level of the deeper layers of the superior colliculus (SC). 2. In three alert rhesus monkeys we tested whether the saccadic motor map of the SC is two dimensional, representing oculocentric target vectors (the vector or V-model), or three dimensional, representing the coordinates of the rotation of the eye from initial to final position (the quaternion or Q-model). 3. Monkeys made spontaneous saccadic eye movements both in the light and in the dark. They were also rotated about various axes to evoke quick phases of vestibular nystagmus, which have three degrees of freedom. Eye positions were measured in three dimensions with the magnetic search coil technique. 4. While the monkey made spontaneous eye movements, we electrically stimulated the deeper layers of the SC and elicited saccades from a wide range of initial positions. According to the Q-model, the torsional component of eye position after stimulation should be uniquely related to saccade onset position. However, stimulation at 110 sites induced no eye torsion, in line with the prediction of the V-model. 5. Activity of saccade-related burst neurons in the deeper layers of the SC was analyzed during rapid eye movements in three dimensions. No systematic eye-position dependence of the movement fields, as predicted by the Q-model, could be detected for these cells. Instead, the data fitted closely the predictions made by the V-model. 6. In two monkeys, both SC were reversibly inactivated by symmetrical bilateral injections of muscimol. The frequency of spontaneous saccades in the light decreased dramatically. Although the remaining spontaneous saccades were slow, Listing's law was still obeyed, both during fixations and saccadic gaze shifts. In the dark, vestibularly elicited fast phases of nystagmus could still be generated in three dimensions. Although the fastest quick phases of horizontal and vertical nystagmus were slower by about a factor of 1.5, those of torsional quick phases were unaffected. 7. On the basis of the electrical stimulation data and the properties revealed by the movement field analysis, we conclude that the collicular motor map is two dimensional. The reversible inactivation results suggest that the SC is not the site where three-dimensional fast phases of vestibular nystagmus are generated.(ABSTRACT TRUNCATED AT 400 WORDS)


1976 ◽  
Vol 39 (4) ◽  
pp. 722-744 ◽  
Author(s):  
C. W. Mohler ◽  
R. H. Wurtz

1. We investigated the characteristics of cells in the intermediate layers of the superior colliculus that increase their rate of discharge before saccadic eye movements. Eye movements were repeatedly elicited by training rhesus monkeys to fixate on a spot of light and to make saccades to other spots of light when the fixation spot was turned off. 2. The eye movement cells showed consistent variations with their depth within the colliculus. The onset of the cell discharge led the eye movement by less time and the duration of the discharge was shorter as the cell was located closer to the dorsal edge of the intermediate layers. The movements fields (that area of the visual field where a saccade into the area is preceded by a burst of cell discharges) of each successive cell also became smaller as the cells were located more dorsally. The profile of peak discharge frequency remained fairly flat throughout the movement field of the cells regardless of depth of the cell within the colliculus. 3. A new type of eye movement-related cell has been found which usually lies at the border between the superficial and intermediate layers. This cell type, the visually triggered movement cell, increased its rate of discharge before saccades made to a visual stimulus but not before spontaneous saccades of equal amplitude made in the light or the dark. A vigorous discharge of these cells before an eye movement was dependent on the presence of a visual target; the cells seemed to combine the visual input of superficial layer cells and the movement-related input of the intermediate layer cells. The size of the movement fields of these cells were about the same size as the visual fields of superficial layer cells just above them...


1980 ◽  
Vol 44 (6) ◽  
pp. 1175-1189 ◽  
Author(s):  
P. H. Schiller ◽  
S. D. True ◽  
J. L. Conway

1. This study investigated the effects of frontal eye-field and superior colliculus ablations on fixation patterns and saccadic eye movements. Monkeys were trained to pick apple pieces out of a multiple-slotted apple board while their heads were fixed. Eye movement records were obtained using predominantly the implanted search-coil method. 2. Both unilateral and bilateral frontal eye-field lesions produced only temporary deficits in eye movements. Following surgery monkeys tended to neglect the contralateral peripheral visual field and made fewer saccades to peripheral targets. Recovery was virtually completed in 2-4 wk. 3. Superior colliculus ablation reduced fixation accuracy, saccade frequency, and saccade velocity. These deficits showed little recovery with time. 4. Paired frontal eye-field and superior colliculus lesions produced dramatic deficits in visually triggered eye movements. Animals could no longer fixate their eyes on visual targets with any degree of accuracy. The range of eye movements was greatly reduced, as was the frequency and velocity of saccades. These deficits showed little recovery with time. 5. These results suggest that visually triggered saccadic eye movements are controlled by two parallel channels, one involving the superior colliculus and the other the frontal eye field.


2017 ◽  
Author(s):  
Ricky R Savjani ◽  
Elizabeth Halfen ◽  
Jung Hwan Kim ◽  
David Ress

SummaryThe superior colliculus (SC) is a layered midbrain structure involved in directing eye movements and coordinating visual attention. Electrical stimulation and neuronal recordings in the intermediate layers of monkey SC have shown a retinotopic organization for the mediation of saccadic eye-movements. However, in human SC the topography of saccades is unknown. Here, a novel experimental paradigm and highresolution (1.2-mm) functional magnetic resonance imaging methods were used to measure activity evoked by saccadic eye movements within SC. Results provide three critical observations about the topography of the human SC: (1) saccades along the superior-inferior visual axis are mapped across the medial-lateral anatomy of the SC; (2) the saccadic eye-movement representation is in register with the retinotopic organization of visual stimulation; and (3) activity evoked by saccades occurs deeper within SC than that evoked by visual stimulation. These approaches lay the foundation for studying the organization of human subcortical eye-movement mechanisms.HighlightsHigh-resolution functional MRI enabled imaging from intermediate layers of human SCSaccades along superior-inferior visual field are mapped across medial-lateral SCSaccadic eye movement maps lie deeper in SC and are in alignment with retinotopyeTOC BlurbSavjani et al. found the polar angle representation of saccadic eye movements in human SC. The topography is similar in monkey SC, is in register with the retinotopic organization evoked by visual stimulation, but lies within deeper layers. These methods enable investigation of human subcortical eye-movement organization and visual function.


2021 ◽  
Author(s):  
Sebastian H. Zahler ◽  
David E. Taylor ◽  
Julia M. Adams ◽  
Evan H. Feinberg

AbstractHumans read text, recognize faces, and process emotions using targeted saccadic eye movements. In the textbook model, this innate ability to make targeted saccades evolved in species with foveae or similar high-acuity retinal specializations that enable scrutiny of salient stimuli. According to the model, saccades made by species without retinal specializations (such as mice) are never targeted and serve only to reset the eyes after gaze-stabilizing movements. Here we show that mice innately make touch-evoked targeted saccades. Optogenetic manipulations revealed the neural circuit mechanisms underlying targeted saccades are conserved. Saccade probability is a U-shaped function of current eye position relative to the target, mirroring the simulated relationship between an object’s location within the visual field and the probability its next movement carries it out of view. Thus, a cardinal sophistication of our visual system may have had an unexpectedly early origin as an innate behavior that keeps stimuli in view.


1998 ◽  
Vol 79 (3) ◽  
pp. 1193-1209 ◽  
Author(s):  
Douglas P. Munoz ◽  
Peter J. Istvan

Munoz, Douglas P. and Peter J. Istvan. Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J. Neurophysiol. 79: 1193–1209, 1998. The intermediate layers of the monkey superior colliculus (SC) contain neurons the discharges of which are modulated by visual fixation and saccadic eye movements. Fixation neurons, located in the rostral pole of the SC, discharge action potentials tonically during visual fixation and pause for most saccades. Saccade neurons, located throughout the remainder of the intermediate layers of the SC, discharge action potentials for saccades to a restricted region of the visual field. We defined the fixation zone as that region of the rostral SC containing fixation neurons and the saccade zone as the remainder of the SC. It recently has been hypothesized that a network of local inhibitory interneurons may help shape the reciprocal discharge pattern of fixation and saccade neurons. To test this hypothesis, we combined extracellular recording and microstimulation techniques in awake monkeys trained to perform oculomotor paradigms that enabled us to classify collicular fixation and saccade neurons. Microstimulation was used to electrically activate the fixation and saccade zones of the ipsilateral and contralateral SC to test for inhibitory and excitatory inputs onto fixation and saccade neurons. Saccade neurons were inhibited at short latencies following electrical stimulation of either the ipsilateral (1–5 ms) or contralateral (2–7 ms) fixation or saccade zones. Fixation neurons were inhibited 1–4 ms after electrical stimulation of the ipsilateral saccade zone. Stimulation of the contralateral saccade zone led to much weaker inhibition of fixation neurons. Stimulation of the contralateral fixation zone led to short-latency (1–2 ms) excitation of fixation neurons. Only a small percentage of saccade and fixation neurons were activated by the electrical stimulation (latency: 0.5–2.0 ms). These responses were confirmed as either orthodromic or antidromic responses using collision testing. The results suggest that a local network of inhibitory interneurons may help shape not only the reciprocal discharge pattern of fixation and saccade neurons but also permit lateral interactions between all regions of the ipsilateral and contralateral SC. These interactions therefore may be critical for maintaining stable visual fixation, suppressing unwanted saccades, and initiating saccadic eye movements to targets of interest.


2000 ◽  
Vol 83 (4) ◽  
pp. 2374-2391 ◽  
Author(s):  
Alexandra Battaglia-Mayer ◽  
Stefano Ferraina ◽  
Takashi Mitsuda ◽  
Barbara Marconi ◽  
Aldo Genovesio ◽  
...  

Neural activity was recorded in the parietooccipital cortex while monkeys performed different tasks aimed at investigating visuomotor interactions of retinal, eye, and arm-related signals on neural activity. The tasks were arm reaching 1) to foveated targets; 2) to extrafoveal targets, with constant eye position; 3) within an instructed-delayed paradigm, under both light and darkness; 4) saccadic eye movements toward, and static eye holding on peripheral targets; and 5) visual fixation and stimulation. The activity of many cells was modulated during arm reaction (68%) and movement time (58%), and during static holding of the arm in space (64%), when eye position was kept constant. Eye position influenced the activity of many cells during hand reaction (45%) and movement time (51%) and holding of hand static position (69%). Many cells (56%) were also modulated during preparation for hand movement, in the delayed reach task. Modulation was present also in the dark in 59% of cells during this epoch, 51% during reaction and movement time, and 48% during eye/hand holding on the target. Cells (50%) displaying light-dark differences of activity were considered as related to the sight and monitoring of hand motion and/or position in the visual field. Saccadic eye movements modulated a smaller percentage (25%) of cells than eye position (68%). Visual receptive fields were mapped in 44% of the cells studied. They were generally large and extended to the periphery of the tested (30°) visual field. Sixty-six percent of cells were motion sensitive. Therefore the activity of many neurons in this area reflects the combined influence of visual, eye, and arm movement–related signals. For most neurons, the orientation of the preferred directions computed across different epochs and tasks, therefore expression of all different eye- and hand-related activity types, clustered within a limited sector of space, the field of global tuning. These spatial fields might be an ideal frame to combine eye and hand signals, thanks to the congruence of their tuning properties. The relationships between cell activity and oculomotor and visuomanual behavior were task dependent. During saccades, most cells were recruited when the eye moved to a spatial location that was also target for hand movement, whereas during hand movement most cells fired depending on whether or not the animal had prior knowledge about the location of the visual targets.


1991 ◽  
Vol 65 (6) ◽  
pp. 1464-1483 ◽  
Author(s):  
S. Funahashi ◽  
C. J. Bruce ◽  
P. S. Goldman-Rakic

1. Single-neuron activity was recorded from the prefrontal cortex of monkeys performing saccadic eye movements in oculomotor delayed-response (ODR) and visually guided saccade (VGS) tasks. In the ODR task the monkey was required to maintain fixation of a central spot throughout the 0.5-s cue and 3.0-s delay before making a saccadic eye movement in the dark to one of four or eight locations where the visual cue had been presented. The same locations were used for targets in the VGS tasks; however, unlike the ODR task, saccades in the VGS tasks were visually guided. 2. Among 434 neurons recorded from prefrontal cortex within and surrounding the principal sulcus (PS), 147 changed their discharge rates in relation to saccadic eye movements in the ODR task. Their response latencies relative to saccade initiation were distributed between -192 and 460-ms, with 22% exhibiting presaccadic activity and 78% exhibiting only postsaccadic activity. Among PS neurons with presaccadic activity, 53% also had postsaccadic activity when the monkey made saccadic eye movements opposite to the directions for which the presaccadic activity was observed. 3. Almost all (97%) PS neurons with presaccadic activity were directionally selective. The best direction and tuning specificity of each neuron were estimated from parameters used to fit a Gaussian tuning curve function. The best direction for 62% of the neurons with presaccadic activity was toward the contralateral visual field, with the remaining neurons having best directions toward the ipsilateral field (23%) or along the vertical meridian (15%). 4. Most postsaccadic activity of PS neurons (92%) was also directionally selective. The best direction for 48% of these neurons was toward the contralateral visual field, with the remaining neurons having best directions toward the ipsilateral field (36%) or along the vertical meridian (16%). Eighteen percent of the neurons with postsaccadic activity showed a reciprocal response pattern: excitatory responses occurred for one set of saccade directions, whereas inhibitory responses occurred for roughly the opposite set of directions. 5. Sixty PS neurons with saccade-related activity in the ODR task were also examined in a VGS task. Forty of these neurons showed highly similar profiles of directional specificity and response magnitude in both tasks, 13 showed saccade-related activity only in the ODR task, and 7 changed their response characteristics between the ODR and VGS tasks.(ABSTRACT TRUNCATED AT 400 WORDS)


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