Chapter 10 Roles of the lateral suprasylvian cortex in convergence eye movement in cats

1643 Regional differences in the lateral suprasylvian area and the evoked potentiation of ocular convergence in cats

Functional roles of the lateral suprasylvian cortex in ocular near response in the cat

Ocular convergence-related neuronal responses in the lateral suprasylvian area of alert cats

RECENT SINGLE-UNIT recording studies of the alert rhesus monkey superior colliculus have disclosed that the deeper layers of this structure contain cells which discharge in association with eye movement (15-17, 23, 24). Such units fire selectively prior to saccades of a specific direction and size, irrespective of the position of the eye in orbit. Stimulation studies of the superior colliculus have so far produced conflicting results. Some reports suggest that in the alert cat stimulation brings the eye to a certain position in orbit irrespective of eye position prior to stimulation (1, 9, 19). Thus, the size and direction of elicited saccades is reported to vary as a function of initial eye position. By contrast, in the alert monkey it has recently been reported that stimulation produces conjugate saccades of a specific size and direction; these parameters are the same no matter where the eye is in the orbit prior to stimulation (12, 15, 16). The stimulation map of Robinson (12) shows a reasonable correspondence with the receptive-field map of the superior colliculus reported by Cynader and Berman (5). The aim of this study was to clarify the relationship between recording and stimulation data by using methods which allow a direct comparison. We used alert rhesus monkeys which had one eye immobilized for the mapping of visual receptive fields. The other eye was normal, thus permitting the study of eye movement. Stimulation and recording were carried out using the same low-resistance microelectrode; for each site sampled, records were obtained for both single-unit activity and for electrical stimulation.

Converging lines of evidence support a role for the intermediate and deep layers of the superior colliculus (SC) and the mesencephalic reticular formation (MRF) in the control of combined head and eye movements (i.e., gaze). Recent microstimulation, single-cell recording, and lesion experiments are reviewed in which monkeys are free to move their heads. Cells in the SC discharge in advance of combined head and eye movements and most likely provide a gaze error signal to downstream structures. In contrast, the neurons in the MRF are of at least two types. Eye cells have features that are similar to neurons in the rostral portion of the SC, but fire before the onset of horizontal eye movments. A second group of MRF neurons begin to fire after the onset of the gaze shift and are most closely associated with movements of the head. The peak discharge of these late-onset MRF neurons occurs near the peak head velocity. Stimulation in the rostral SC generates eye movements with fixed amplitude and direction. A similar response is noted after stimulation of the more dorsal portion of the caudal MRF. Stimulation in the caudal portion of the SC produces combined head and eye movements of fixed amplitude. Electrical activation of the more ventral portions of the caudal MRF generates goal-directed and centering eye movements. Temporary inactivation of the SC with the GABA agonist muscimol generated hypometria and curved trajectories of contralateral eye movements. Inactivation of the caudal MRF produced contralateral hypermetria and ipsilateral hypometria of saccades. Release of the monkey's head demonstrated a profound contralateral head tilt. Taken together, these data suggest that the gaze signal generated in the SC is filtered by neurons in the MRF to generate a feedback signal of eye motor error. The head signal found in the MRF could cancel a portion of the gaze signal coming from the SC in the form of head velocity feedback.

ACCUMULATING EVIDENCE suggests that the superior colliculus plays an important role in orientation and eye movement. Ablation studies have shown that destruction of superior colliculi interferes with spatial orientation and eye movement (Z-29), although the evidence regarding the effects of such lesions in primates is conflicting (1, 7, 17, 18; and unpublished observations). Stimulation studies have disclosed that electrical or chemical stimulation of the superior colliculus elicits eye and head movement in several species (4, 1 I, 20, 22). While most single-unit studies centered on the visual information-processing role of the mammalian superior colliculi (12-16, 30, 32, 33; M. Cynader and N. Berman, unpublished observations), a few studies have recently appeared that demonstrate eye-movement related unit activity (22, 31, 35) The aim of the present study was to investigate the discharge characteristics of single units in the superior colliculus of the alert, unanesthe tized monkey. We wished to assess both the visual receptivefield characteristics of units and the possible relation of unit discharges to eye movement. To carry out this plan one eye of each monkey was immobilized prior to the experiment by transection of the 3rd, 4th, and 6th cranial nerves. This made it possible to study in the monkey, whose head was restrained, receptive fields of units of the immobilized eye, and to relate the discharge characteristics of collicular units to the movement of the normal eye during both saccadic and smooth pursuit eye movements. M. Cynader and N. Berman (unpublished data) recently have shown that nearly all units in the monkey

Effects of Superior Colliculus Inhibition on Three-Dimensional Visual Motion Processing in the Lateral Suprasylvian Visual Area of the Cat

Colliculoreticular organization in primate oculomotor system

Eye movements evoked by cerebellar stimulation in the alert monkey.

One of the most important functions of the brain is to guide our behavior through an ever-changing environment as our goals and desires fluctuate. One simple, yet elegant system for investigating how sensory information and goal-related information combine to control and coordinate efficient behavior is the guidance of saccadic eye movements. The brain relies heavily on visual input to guide and coordinate our complex actions, but it is impossible for our brain to simultaneously process every aspect of visual information present in real world scenes at any given moment. Instead, the retina has evolved a highly specialized fovea in the center where we have the highest visual acuity. Therefore, to analyze a visual scene optimally, the eyes reorient in complex sequences so that the high acuity fovea of the retina can be directed to specific objects of interest. These saccadic eye movements are interspersed with periods of active fixation during which the visual system performs a detailed analysis of an object that may pertain to our current goals. Alternating between the serial process of making saccades and the analytical process of active fixation is repeated several hundred thousand times per day and is critical for numerous behaviors like reading this issue of EJN, driving an automobile or negotiating a busy sidewalk. In the laboratory, saccadic behavior can be measured easily and accurately. Quantitative analysis of saccade behavior can also serve as an important tool to investigate brain disorders in a host of neurological and psychiatric disorders (Leigh & Zee, 2006). Over the past few decades, there has been a tremendous increase in our knowledge of the systems that contribute to the control of saccadic eye movements. There have been many recent and exciting advances. Anatomical, physiological, clinical and imaging studies have contributed to our extensive knowledge of the saccade control circuit (Fig. 1), which includes regions of the occipital, parietal and frontal cortex, basal ganglia, thalamus, superior colliculus, cerebellum, and brainstem reticular formation. Within each of these brain regions are multiple populations of neurons and subnuclei that perform critical operations to coordinate behavior. In addition to overt eye movements that explicitly orient the visual system, visual selection may also be directed covertly to different locations or objects without any movement of the eyes. For example, we have the ability to shift attention away from where we look without initiating a saccade. Both overt (move the eyes) and covert (only shift attention) orienting can be directed voluntarily to a specific location or object, or involuntarily ‘captured’ by an abrupt change in the visual environment (Posner, 1980; Theeuwes, 1991; Fecteau & Munoz, 2006). There is significant overlap in the brain areas that participate in overt and covert orienting, which include several components of the frontoparietal network and the superior colliculus. This special issue of EJN contains reviews and original articles by some of the leading experts in the fields of saccades and visual search. There have been many recent exciting advances in these fields that are captured in the contributions in this issue. The contributions focus on different brain areas but the content ranges from the sensory input to the motor output and everything in between (Fig. 1). There are several different state-of-the-art technologies employed including quantitative behavioral analysis, neurophysiology, neuroimaging, clinical investigation, transcranial magnetic stimulation and modeling.

Activity of superior colliculus in behaving monkey. IV. Effects of lesions on eye movements.

1642 Changes in ocular convergence during 3-d task using a hmd in humans

The superior colliculus (SC) has long been recognized as an important structure in the generation of saccadic eye movements. The SC of the cat and the monkey has recently been shown to be involved in the control of visual fixation. A subpopulation of collicular cells exhibits tonic discharge when the animal fixates on a target of interest. These cells are located in the rostral SC where the central visual field is represented. Active fixation is thought to be important for the ocular near response; accommodation, vergence and pupillo-constriction, and these systems are functionally linked. Therefore, it is possible that the rostral SC is also involved in the control of accommodation or vergence. The results of several recent studies have suggested that the rostral SC is also involved in the control of accommodation. The accommodation-related area in the rostral SC also corresponds to the area of representation of the central visual field. The accommodation-related area in the SC receives heavy projections from the accommodation area in the lateral suprasylvian (LS) area of the cat cortex. It is well known that the LS area is also involved in the control of vergence and pupillo-constriction. The rostral SC projects to the pretectal nuclei (PT) where accommodative responses are evoked by microstimulation, the raphe interpositus (RIP), in which omnipause neurons are located, and the dorsomedial portion of the nucleus reticularis tegmenti pontis. Many neurons in the intermediate layers of the rostral SC have divergent axon collaterals to the PT and the RIP. The rostral SC is likely a key structure involved in the near response and visual fixation.

Convergence eye movements evoked by microstimulation of the rostral superior colliculus in the cat.

Responses of Collicular Fixation Neurons to Gaze Shift Perturbations in Head-Unrestrained Monkey Reveal Gaze Feedback Control