Edward L. Keller

Colliculoreticular organization in primate oculomotor system

Publisher Summary This chapter summarizes saccadic eye movement-related discharge in superior colliculus (SC) neurons and in median pontomedullary reticular formation (RF) neurons and reviews the organization of colliculoreticular pathways, particularly with a view towards clarifying the mechanisms involved in controlling saccadic eye movements in primates. New data on the functional type of SC input to the RF are presented. A new interpretation is placed on the possible role played in saccadic generation by a class of neurons called quasi-visual cells. Saccade-related discharge of brain stem reticular formation neurons is discussed and comparisons are made between presaccadic activity in neurons in SC and RF. Studies showing the existence and nature of synaptic input from the SC to specific functional types of RF cells are reviewed and new preliminary results indicating the functionally identified type of SC neuron supplying at least a portion of these connections are shown. The possible role played by the neurons and synaptic connections described in these two anatomic structures is hypothesized in the form of saccadic control model.

Deficits in saccade target selection after inactivation of superior colliculus

Saccades are rapid eye movements that orient gaze toward areas of interest in the visual scene. Neural activity correlated with saccade target selection has been identified in several brain regions, including the superior colliculus (SC), but it is not known whether the SC is directly involved in target selection, or whether the SC merely receives selection-related signals from cortex in preparation for the execution of eye movements. In monkeys, we used focal reversible inactivation to test the functional contributions of the SC to target selection during visual search, and found that inactivation resulted in clear deficits. When a target appeared in the inactivated field, saccades were often misdirected to distractor stimuli. Control tasks showed that this deficit was not caused by low-level visual or motor impairments. Our results indicate that, in addition to its well-established involvement in movement execution, the SC has an important functional role in target selection.

Visual signals in the dorsolateral pontine nucleus of the alert monkey: Their relationship to smooth-pursuit eye movements

SummaryThe visual properties of 77 dorsolateral pontine nucleus (DLPN) cells were studied in two alert monkeys. In 41 cells, presentation of a moving random dot background pattern, while the monkeys fixated a stationary spot, elicited modulations in discharge rate that were related either to (i) the velocity of background motion in a specific direction or to (ii) only the direction of background movement. Thirty-six DLPN cells exhibited responses to small, 0.6–1.7 deg, visual stimuli. Nine such cells exhibited non-direction selective receptive fields that were eccentric from the fovea. During fixation of a stationary bluish spot, the visual responses of 27 DLPN cells to movement of a small, white “test” spot were characterized by two components: (1) as the test spot crossed the fovea in a specific direction, transient velocity-related increases in discharge rate occurred and (2) a maintained, smaller increase in activity was observed for the duration of test spot movement in the preferred direction. This DLPN activity associated with small visual stimuli was also observed during smooth-pursuit eye movements when, due to imperfect tracking, retinal image motion of the target produced slip in the same direction. These preliminary results suggest that the DLPN could supply the smooth-pursuit system with signals concerning the direction and velocity of target image motion on the retina.

Short-term priming, concurrent processing, and saccade curvature during a target selection task in the monkey.

In human subjects, two mechanisms for improving the efficiency of saccades in visual search have recently been described: color priming and concurrent processing of two saccades. Since the monkey provides an important model for understanding the neural underpinnings of target selection in visual search, we sought to explore the degree to which the saccadic system of monkeys uses these same mechanisms. Therefore, we recorded the eye movements of rhesus monkeys performing a simple color-oddity pop-out search task, similar to that used previously with human subjects. The monkeys were rewarded for making a saccade to the odd-colored target, which was presented with an array of three distractors. The target and distractors were randomly chosen to be red or green in each trial. Similar to what was previously observed for humans, we found that monkeys show the influence of a cumulative, short-term priming mechanism which facilitates saccades when the color of the search target happens to repeat from trial to trial. Furthermore, we found that like humans, when monkeys make an erroneous initial saccade to a distractor, they are capable of executing a second saccade to the target after a very brief inter-saccadic interval, suggesting that the two saccades have been programmed concurrently (i.e. in parallel). These results demonstrate a close similarity between human and monkey performance. We also made a new observation: we found that when monkeys make such two-saccade responses, the trajectory of the initial saccade tends to curve toward the goal of the subsequent saccade. This provides evidence that the two saccade goals are simultaneously represented on a common motor map, supporting the idea that the movements are processed concurrently. It also indicates that concurrent processing is not limited to brain areas involved in higher-level planning; rather, such parallel programming apparently occurs at a low enough level in the saccadic system that it can affect saccade trajectory.

Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey

Abstract The activity of single cells in the vestibular nuclei in alert, behaving monkey was studied by extracellular recording. A majority of the neurons found in the superior and the rostral medial vestibular nuclei can be divided into two classes on the basis of their discharge relationship to eye movements evoked during head rotation, visual target pursuit, or visual suppression of the vestibulo-ocular reflex. The firing rate of the first unit type is proportional to head rotational velocity (and the resulting compensatory eye velocity) but is not modulated during slow eye movements of pure visual origin. During visual suppression of the vestibulo-ocular reflex, the relationship of this type of unit discharge to head velocity remains unchanged, although the eye velocity is now zero. The second type of unit more closely resembles oculomotor neurons in that its discharge pattern is proportional to eye position and velocity during eye movements of both visual and vestibular origin. However during suppression of the vestibuloocular reflex this type of unit continues to show a greatly reduced but consistent modulation of discharge rate proportional to head velocity. Thus the direct projection of vestibular neurons to oculomotor neurons cannot by itself account for the ability of the monkey to completely suppress its vestibulo-ocular reflex.

1994 Special Issue: Two-dimensional neural network model of the primate saccadic system

The objective of this paper is to present a distributed model of the spatiotemporal neural processing that underlies the control of two-dimensional saccadic eye movements in the monkey. In this new model the superior colliculus (SC) is represented by two layers of cells. Simulated visual inputs activate the upper layer that is connected to the lower (motor) layer with feedforward projections. Extensive lateral interconnections exist in the motor layer. The weights assigned to these interconnections are established with a recurrent back propagation algorithm and by training on a set of activity patterns obtained from neurons recorded in the monkey SC. A distributed set of connections to horizontal and vertical brainstem saccadic burst generators is trained to allow the model to make accurate saccades to randomly selected target positions. Finally, the model is able to produce accurate eye movements and realistic neural discharge for saccades evoked with a variety of experimental conditions not included in the training set (for example, averaging and express saccades).

Smooth-pursuit initiation in the presence of a textured background in monkey

Smooth pursuit eye movements in the monkey were studied by measuring the average eye acceleration in the first 100 msec of the ocular response to suddenly moving constant velocity discrete visual targets. The tracking targets motion was initiated on or eccentric to the fovea against a very dimly lit homogeneous background or an illuminated, highly textured, large-field background. The effect of the textured background was always to reduce the initial eye acceleration as compared to that present in the homogeneous background case. Movement of the background in the opposite direction to target spot movement also reduced the initial eye acceleration. In contrast, steady-state tracking measured several hundred msec after the onset of pursuit under the same conditions was only marginally reduced by the presence of the textured background.

Gain of the vestibulo-ocular reflex in monkey at high rotational frequencies.

Abstract The gain of the vestibulo-ocular reflex (VOR) was measued in alert monkeys during sinusoidal oscillations of the animals over a frequency range extending from 0.5 to 6 Hz. In confirmation of the results of previous investigators the gain of the VOR was found to be consistently below unity in the dark at rotational frequencies up to 1 Hz. When visual information was present to augment the vestibular input the gain increased to a value of 1 over this same frequency range. In contrast, as the rotational frequency increased above 1 Hz, the gain in the dark increased steadily until it exceeded unity at about 2 Hz. Peak gain (mean = 1.3) was reached in the dark at about 4 Hz and declined sharply at higher frequencies to fall below one at 6 Hz. Gain in the presence of fixed visual images remained at one over this entire range of frequencies.

Behavior of horizontal semicircular canal afferents in alert monkey during vestibular and optokinetic stimulation

SummaryThe behavior of single vestibular nerve fibers from the lateral semicircular canal was recorded during sinusoidal oscillations of the head, during optokinetic stimulation with the head stationary, and during spontaneous oculomotor behavior in the alert monkey. The response of similar fibers to adequate vestibular stimulation was also studied in some of the animals under deeply anesthetized conditions. In the alert animals all units were spontaneously active and their discharge was modulated only by adequate vestibular stimulation. Ipsilateral horizontal rotations of the head were excitatory for all units. No modification of this basic vestibular response by visual stimulation including full-field striped drum rotation was observed. Furthermore no correlation of unit activity with oculomotor function including voluntary saccadic and pursuit eye movements was found in any of the units. The regularity of spontaneous discharge was the most consistent characteristic that differentiated the unit response into types. Most units were very regular in discharge, but a few were very irregular. The averaging of unit discharge over several cycles of oscillatory head rotation showed that the irregular type units were also consistently modulated by adequate vestibular stimulation. Both regular and irregular type units were found in the anesthetized animals. Unimodal distributions of the quantitative values for unit resting discharge rate, sensitivity, and phase relationship were found. The distributions for these three parameters were similar in the units recorded in the anesthetized animals. Thus at least these characteristics of semicircular canal response seem not to be affected by the vestibular efferent system which should be altered or eliminated in the case of the anesthetized animals.

Accommodative vergence in the alert monkey. Motor unit analysis

Abstract The behavior of both abducens nucleus and oculomotor nucleus motoneurons during accommodative vergence eye movements is examined in the alert monkey. This behavior is compared with that of the same neurons during versional eye movements. The behavior is found to be identical, which indicates that oculomotor unit discharge is determined by fixation angle without regard to the type of movement used to reach that angle. Detailed statistical analysis of unit firing rate also suggests that the separate inputs controlling vergence and version are probably combined at some supranuclear level before the motoneuron. The firing rates of motoneurons during the dynamic phase of a vergence movement is examined and compared to that during pursuit movements in an attempt to correlate neuron discharge with the mechanical dynamics of the orbit.