Functional imaging of the primate superior colliculus during saccades to visual targets

The primate superior colliculus (SC) is a midbrain nucleus crucial for the control of rapid eye movements (saccades). Its neurons are topographically arranged over the rostrocaudal and mediolateral extent of its deeper layers so that saccade metrics (amplitude and direction) are coded in terms of the location of active neurons. We used the quantitative [14C]-deoxyglucose method to obtain a map of the two-dimensional pattern of activity throughout the SC of rhesus monkeys repeatedly executing visually guided saccades of the same amplitude and direction for the duration of the experiment. Increased metabolic activity was confined to a circumscribed region of the two-dimensional reconstructed map of the SC contralateral to the direction of the movement. The precise rostrocaudal and mediolateral location of the area activated depended on saccade metrics. Our data support the notion that the population of active SC cells remains stationary in collicular space during saccades.     

Superior colliculus encodes distance to target,not saccade amplitude,in multi-step gaze shifts

The superior colliculus (SC) is important for generating coordinated eye-head gaze saccades. Its deeper layers contain a retinotopically organized motor map in which each site is thought to encode a specific gaze saccade vector. Here we show that this fundamental assumption in current models of collicular function does not hold true during horizontal multi-step gaze shifts in darkness that are directed to a goal and composed of a sequence of gaze saccades separated by periods of steady fixation. At the start of a multi-step gaze shift in cats, neural activity on the SC's map was located caudally to encode the overall amplitude of the gaze displacement, not the first saccade in the sequence. As the gaze shift progressed, the locus of activity moved to encode the error between the goal and the current gaze position. Contrary to common belief, the locus of activity never encoded gaze saccade amplitude, except for the last saccade in the sequence.     

Activity in deep intermediate layer collicular neurons during interrupted saccades

The activity of neurons located in the deep intermediate and adjacent deep layers (hereafter called just deep intermediate layer neurons) of the superior colliculus (SC) in monkeys was recorded during saccades interrupted by electrical stimulation of the brainstem omnipause neuron (OPN) region. The goal of the experiment was to determine if these neurons maintained their discharge during the saccadic interruption, and thus, could potentially provide a memory trace for the intended movement which ends accurately on target in spite of the perturbation. The collicular neurons recorded in the present study were located in the rostral three-fifths of the colliculus. Most of these cells tended to show considerable presaccadic activity during a delayed saccade paradigm, and, therefore, probably overlap with the population of SC cells called buildup neurons or prelude bursters in previous studies. The effect of electrical stimulation in the OPN region (which interrupted ongoing saccades) on the discharge of these neurons was measured by computing the percentage reduction in a cell's activity compared to that present during non-interrupted saccades. During saccade interruption about 70% of deep intermediate layer neurons experienced a major reduction (30% or greater) in their activity, but discharge recovered quickly after the termination of the stimulation as the eyes resumed their movement to finish the saccade on the target. Therefore, the pattern of activity recorded in most of the deep intermediate layer neurons during interrupted saccades qualitatively resembled that previously reported for the saccade-related burst neurons which tend to be located more dorsally in the intermediate layer. In contrast, some of our cells (30%) showed little or no perturbation in their activity caused by the saccade interrupting stimulation. Because all the more dorsally located burst neurons and the majority of our deep intermediate layer neurons show a total or major suppression in their discharge during interrupted saccades, it seems unlikely that the colliculus by itself could maintain an accurate memory of the desired saccadic goal or the remaining dynamic motor error required to account for the accuracy of the resumed movement which occurs following the interruption. However, it remains possible that the smaller proportion of our neurons whose activity was not perturbed during interrupted movements could play a role in the mechanisms underlying saccade accuracy in the interrupted saccade paradigm. Interrupted saccades have longer durations than normal saccades to the same target. Therefore, we investigated whether the discharge of our deeper collicular cells was also necessarily prolonged during interrupted saccades, and, if so, how the prolongation compared to the prolongation of the saccade. Sixty percent of our sample neurons showed a prolongation in discharge that was approximately the same as the prolongation in saccade duration (difference < 15 ms in magnitude). The, observation that temporal discharge in our neurons was perturbed to roughly match saccadic temporal perturbation suggests that dynamic feedback about ongoing saccadic motion is provided to the colliculus, but does not necessarily imply that this structure is the site responsible for the computation of dynamic motor error.     

Influence of the superior colliculus on visual responses of cells in the rabbit's lateral posterior nucleus

Summary The lateral posterior-pulvinar (LP-P) complex of mammals receives a major input from the superior colliculus (SC). We have studied the response properties of LP cells and investigated the effects of reversible inactivation of the colliculus on the visual responses of LP units in anesthetized and paralyzed rabbits. Cells in LP had large receptive fields responsive to either stationary or moving stimuli. One third of the motion-sensitive cells were direction selective. The size of the receptive fields increased with eccentricity and there was a retinotopic organization along the dorso-ventral axis. Comparison of the LP and superior colliculus properties revealed substantial differences in visual response characteristics of these two structures such as the size of the receptive fields and the number of direction-selective cells. Electrical stimulation of the LP evoked antidromic action potentials in tectal cells that were motion sensitive. We found a dorsoventral gradient in the projections of collicular cells. Units located more dorsally in the colliculus sent their axons to LP while cells lying more ventrally sent axons toward the region lying posterior to LP. A micropipette filled with lidocaine hydrochloride was lowered into the superficial layers of the superior colliculus in order to reversibly inactivate a small population of collicular cells. Rendering the superior colliculus inactive produced a sharp attenuation of visual responses in the majority of LP cells. Some neurons ceased all stimulus-driven activity after collicular blockade while a few cells exhibited increased excitability following collicular inactivation. These experiments also indicate that the tecto-LP path is topographically organized. An injection in the colliculus failed to influence the thalamic response when it was not in retinotopic register with the LP cells being recorded. Our results demonstrate that the superior colliculus input to LP is mainly excitatory in nature.     

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

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 between E-saccade amplitude and current strength, E-saccade direction is remarkably independent of electrical stimulation parameters. At sufficiently high current strengths (about 20 microA), 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 in E-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 with V-saccade scatter data, recently obtained in the human (Van Opstal and Van Gisbergen 1989c). Finally, an analysis of saccade dynamics shows that E-saccades can reach V-saccadic velocities at higher current strengths. However, at near-threshold current strengths, where E-saccade amplitude decreases, we found at most stimulation sites (22/37) that E-saccades are consistently slower than V-saccades of the same amplitude. Possible mechanisms underlying the collicular role in saccade generation are discussed.     

Interactions between natural and electrically evoked saccades

Electrical microstimulation was applied at brain sites (thalamic internal medullary lamina complex and superficial layers of superior colliculus) of alert, trained monkeys to evoke fixed-vector saccades. When the stimulation was timed to occur during or after an eye movement, the evoked saccade had a modified trajectory, compensating for, at least, the last portion of the ongoing eye movement. The hypothesis proposed to explain this compensatory effect (Schlag-Rey et al. 1989) is that the electrical stimulation produces a saccade by generating a signal, equivalent to a retinal error, specifying the saccade goal at a fixed location with respect to some eye position (called reference eye position). If the eyes are moving at the time of stimulation, the reference eye position lies somewhere along the trajectory of the ongoing movement. In the present study, we tried to determine this reference eye position, and deduce from it the instant at which the goal was specified. A significant timing difference was observed between thalamic and collicular stimulations. The goal appeared to be referred to an eye position existing at stimulation onset in superior colliculus (SC), and 35-65 ms before stimulation onset in central thalamus. In the latter case, the results suggest that the evoked saccade was aimed at the spatial location that the brain computed by summing a retinal error signal (evoked by stimulation) with the eye position at the time such a signal would have been elicited by a real target. In contrast, the collicular results suggest that the evoked saccade was directed to the retinal location specified by the retinal error signal. The findings imply that if the eyes are not steady while the target position is calculated, signals conveyed in the superficial layers of SC (in contrast to the thalamus) cannot direct the eyes correctly to a visual target.     

Effects of eye position on saccades evoked electrically from superior colliculus of alert cats

Electrical stimulation was carried out in the intermediate and deep gray layers of the superior colliculus in alert cats. The heads of the animals were fixed, and their eye movements were recorded with the scleral search coil method. Stimulation in the anterior two-thirds of the colliculus with long-duration pulse trains produced multiple saccades, as in the primate (45, 51), but their directions and amplitudes were influenced significantly by the initial position of the eye. Stimulation in the posterior part of the colliculus evoked saccades that appeared to be "goal-directed," whereas stimulation at the extreme caudal edge of the colliculus yielded centering saccades. These observations confirm previous reports of Roucoux and Crommelinck (48) and Guitton et al. (24). Saccades evoked during bilateral simultaneous stimulation of the superior colliculi were also dependent on the initial position of the eye. At certain relative intensities of stimulation on the two sides, saccades failed to occur when the eye was within a particular part of the oculomotor range. When the eye was outside this region, the same stimuli triggered an eye movement that drove the eye toward the zone of saccade failure. These findings indicate that saccadic commands resulting from focal collicular stimulation in the cat can be modified by information about current eye position. It is not certain where in the brain this occurs or by what neural mechanisms, but a local feedback model of the saccadic control system (46) can account for the main observations. The functional significance of these findings depends in large measure on the degree to which focal collicular stimulation reproduces naturally occurring patterns of neural activity.     

Interactions between natural and electrically evoked saccades

Summary Fixed-vector saccades evoked by electrical stimulation may result from the elicitation of a retinal error signal directing the eyes toward a goal, or from the elicitation of a motor error signal determining the vector itself. Theoretically, the two mechanisms can be differentiated by delivering the stimulation while the eyes are already in motion (colliding saccade paradigm), thereby changing the eye position from which the evoked saccade starts. Only in the first case is the trajectory of the evoked saccade expected to be modified to compensate for part of the ongoing eye movement. An attempt was made to distinguish retinal vs. motor error mechanisms by applying the colliding saccade paradigm of stimulation to 29 sites throughout the superior colliculus (SC) of two trained monkeys. Compensatory evoked saccades, as predicted by the retinal error hypothesis, were obtained consistently in the superficial layers and at deeper sites where visual unit responses could be recorded. Conversely, in deep layers where only presaccadic activity was found, evoked saccades either were not affected by collision or summed their vectors with that of the ongoing movement. These last observations are both consistent with the hypothesis that the signal produced from deep sites was an initial motor error. A second observation was incidentally made: when stimulation was applied to the most superficial SC region, it definitively erased the goal of the ongoing saccade, and the latter did not resume its interrupted course. The colliding saccade paradigm may be useful in clarifying the role of structures involved in oculomotor function.     

Perturbation of combined saccade-vergence movements by microstimulation in monkey superior colliculus.

Perturbation of combined saccade-vergence movements by microstimulation in monkey superior colliculus. This study investigated the role of the monkey superior colliculus (SC) in the control of visually (V)-guided combined saccade-vergence movements by assessing the perturbing effects of microstimulation. We elicited an electrical saccade (E) by stimulation (in 20% of trials) in the SC while the monkey was preparing a V-guided movement to a near target. The target was aligned such that E- and V-induced saccades had similar amplitudes but different directions and such that V-induced saccades had a significant vergence component (saccades to a near target). The onset of the E-stimulus was varied from immediately after V-target onset to after V-saccade onset. E-control trials, where stimulation was applied during fixation of a V-target, yielded the expected saccade but no vergence. By contrast, early perturbation trials, where the E-stimulus was applied soon after the onset of the V-target, caused an E-triggered response with a clear vergence component toward the V-target. Midflight perturbation, timed to occur just after the monkey initiated the movement toward the target, markedly curtailed the ongoing vergence component during the saccade. Examination of pooled responses from both types of perturbation trials showed weighted-averaging effects between E- and V-stimuli in both saccade and fast vergence components. Both components exhibited a progression from E- to V-dominance as the E-stimulus was delayed further. This study shows that artificial intervention in the SC, while a three-dimensional (3D) refixation is being prepared or is ongoing, can affect the timing (WHEN) and the metric specification (WHERE) of both saccades and vergence. To explain this we interpret the absence of overt vergence in the E-controls as being caused by a zero-vergence change command rather than reflecting the mere absence of a collicular vergence signal. In the perturbation trials, the E-evoked zero-vergence signal competes with the V-initiated saccade-vergence signal, thereby giving rise to a compromised 3D response. This effect would be expected if the population of movement cells at each SC site is tuned in 3D, combining the well-known topographical code for direction and amplitude with a nontopographical depth representation. On E-stimulation, the local population would yield a net saccade signal caused by the topography, but the cells coding for different depths would be excited equally, causing the vergence change to be zero.     

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.     

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.     

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.     

The direct visuo-motor pathway in mammalian superior colliculus; novel perspective on the interlaminar connection

The mammalian superior colliculus (SC) is a center controlling the orienting behaviors such as saccadic eye movements. The superficial layers receive visual inputs and the deeper layers send descending motor command to the brainstem and spinal cord. Existence of the interlaminar connection from the superficial to the deeper layers has been an issue of debate during the last two decades. Recent studies have proved the existence of the interlaminar connection by introducing the in vitro slice preparations. When the collicular circuit is disinhibited from gamma-amino butyric acid A (GABA(A)) receptor-mediated inhibition, the signal transmission through the interlaminar connection is enormously facilitated and neurons in the deeper layers exhibit bursting response to stimulation of the superficial layer with non-linear amplification mechanism that depends on the activation of NMDA-type glutamate receptors. In addition, the cholinergic input to the intermediate layer lowers the threshold for the bursting response and facilitates the transmission through the interlaminar connection via activation of nicotinic receptors. The signal transmission through the interlaminar connection may lead to execution of extremely short latency saccades called express saccades.     

Responses resembling defensive behaviour produced by microinjection of glutamate into superior colliculus of rats

Electrical stimulation of the superior colliculus in rats elicits not only orienting movements, as it does in other mammals, but also behaviours resembling such natural defensive responses as prolonged freezing, cringing, shying, and fast running and jumping. To investigate the location of the cells mediating these behaviours, the superior colliculus was systematically mapped with microinjections of sodium L-glutamate (50 mM, 200 nl), and the resultant behavioural changes as assessed in an open field were analysed for defence-like responses. The main regions that gave defensive behaviour were (i) rostromedial superior colliculus (all layers), and (ii) both medial and lateral parts of the caudal deep layers. Cells in these areas project into the ipsilateral descending pathway. However, the cells of origin of this pathway are also found in collicular regions, such as rostral intermediate gray and parts of far caudal colliculus, that did not give defensive movements in response to glutamate stimulation. It is unclear whether this is because only parts of the ipsilateral pathway mediate defensive behaviours, or because glutamate is a relatively inefficient stimulating agent for these systems. An unexpected feature of the results was that at a number of collicular sites the nature of the defensive response changed with successive (up to three) injections of glutamate, often appearing to become more intense. Whether the mechanism underlying this potentiation is related to the conditioning of natural defensive behaviour is unknown.     

Sensori-motor integration in the primate superior colliculus

The sudden onset of a novel stimulus usually triggers orienting responses of the eyes, head and external ears (pinnae). These responses facilitate the reception of additional signals originating from the source of the stimulus and assist in the sensory guidance of appropriate limb and body movements. A midbrain structure, the superior colliculus, plays a critical role in triggering and organizing orienting movements and is a particularly interesting structure for studying the neural computations involved in the translation of sensory signals into motor commands. Auditory, somatosensory and visual signals converge in its deep layers, where neurons are found that generate motor commands for eye, head and pinna movements. This article focuses on the role of the superior colliculus in the control of saccadic (quick, high-velocity) eye movements with particular regard to three issues related to the functional properties of collicular neurons. First, how do neurons with large movement fields specify accurately the direction and amplitude of an eye movement? Second, how are signals converted from different sensory modalities into commands in a common motor frame of reference? Last, how are the motor command signals found in the superior colliculus transformed into those needed by the motor neuron pools innervating the extraocular muscles?     

Supplementary eye field: representation of saccades and relationship between neural response fields and elicited eye movements

The functional organization of the low-threshold supplementary eye field (SEF) was studied by analyzing presaccadic activity, electrically elicited saccades, and the relationship between them. Response-field optimal vectors, defined as the visual field coordinates or saccadic eye-movement dimensions evoking the highest neural discharge, were quantitatively estimated for 160 SEF neurons by systematically varying peripheral target location relative to a central fixation point and then fitting the responses to Gaussian functions. Saccades were electrically elicited at 109 SEF sites by microstimulation (70 ms, 10-100 microA) during central fixation. The distribution of response fields and elicited saccades indicated a complete representation of all contralateral saccades in SEF. Elicited saccade polar directions ranged between 97 and 262 degrees (data from left hemispheres were transformed to a right-hemisphere convention), and amplitudes ranged between 1.8 and 26.9 degrees. Response-field optimal vectors (right hemisphere transformed) were nearly all contralateral as well; the directions of 115/119 visual response fields and 80/84 movement response fields ranged between 90 and 279 degrees, and response-field eccentricities ranged between 5 and 50 degrees. Response-field directions for the visual and movement activity of visuomovement neurons were strongly correlated (r = 0.95). When neural activity and elicited saccades obtained at exactly the same sites were compared, response fields were highly predictive of elicited saccade dimensions. Response-field direction was highly correlated with the direction of saccades elicited at the recording site (r = 0.92, n = 77). Similarly, response-field eccentricity predicted the size of subsequent electrically elicited saccades (r = 0.49, n = 60). However, elicited saccades were generally smaller than response-field eccentricities and consistently more horizontal when response fields were nearly vertical. The polar direction of response fields and elicited saccades remained constant perpendicular to the cortical surface, indicating a columnar organization of saccade direction. Saccade direction progressively shifted across SEF; however, these orderly shifts were more indicative of a hypercolumnar organization rather than a single global topography. No systematic organization for saccade amplitude was evident. We conclude that saccades are represented in SEF by congruent visual receptive fields, presaccadic movement fields, and efferent mappings. Thus SEF specifies saccade vectors as bursts of activity by local groups of neurons with appropriate projections to downstream oculomotor structures. In this respect, SEF is organized like the superior colliculus and the frontal eye field even though SEF lacks an overall global saccade topography. We contend that all specialized oculomotor functions of SEF must operate within the context of this fundamental organization.     

Analysis of the step response of the saccadic feedback: system behavior

We used prolonged stimulation of the monkey superior colliculus to elicit staircase eye movements. By changing the parameters of the stimulating current we were able to obtain movements with different dynamics. An increase in the current frequency resulted in the shortening of the intersaccadic interval and a decrease of the amplitudes in the staircase. In cases of high stimulation, after an initial saccade of fixed metrics, the eyes moved in an apparently smooth fashion. The movement was conjugate and in the same direction as the first saccade. By analyzing the velocity trace we found that the movement consisted of a chain of small saccades, each of which started before the previous one ended. We conducted a quantitative analysis of the staircase movements including the cases of apparently smooth movement of the eyes. We conclude that all of the movements elicited by prolonged SC stimulation were generated by the saccadic feedback circuitry. The dynamic profiles of the elicited movements changed continuously with the stimulating current parameters. On one end of the continuum we observed the classically described staircase movements with individual movements separated in time. On the other end of the continuum we saw the apparent smooth movement as the limit case produced by high stimulation of the SC.     

Convergence of afferents from frontal cortex and substantia nigra onto acetylcholinesterase-rich patches of the cat's superior colliculus

The patterns of distribution of frontotectal and nigrotectal fibers were studied with the anterograde horseradish peroxidase method in the cat. Direct serial-section comparisons were made between the afferent-fiber patterns and the compartmentalized arrangements of acetylcholinesterase staining within the intermediate and deep collicular layers. Many of the patches of high acetylcholinesterase activity in the intermediate gray layer proved to be zones in which labeled frontotectal and nigrotectal fibers converged. These acetylcholinesterase-rich patches may thus represent sites at which functional influences from the basal ganglia and frontal cortex are coordinated. In the deeper tiers of the intermediate gray layer and layers ventral to it, there were also zones of heightened and diminished acetylcholinesterase staining. Much of this histochemical patterning was reflected in the arrangement of fibers labeled by large rostromedial frontal injections, but these deeper tiers were not strongly labeled after more lateral frontal injections or after injections placed in the substantia nigra. The deeper parts of the acetylcholinesterase-positive gridwork in the superior colliculus are thus distinct from its upper tier of acetylcholinesterase-positive patches. We conclude that the compartmentalized patterning of dense acetylcholinesterase staining in the intermediate and deep collicular layers represents a mosaic architecture to which collicular afferent circuitry is tightly related. This gridwork may serve to set up functional domains within which different aspects of collicular processing are accommodated.