Activity of premotor vestibular neurons in the alert cat

The activity of medial vestibular nucleus neurons projecting to the contralateral abducens nucleus (premotor vestibular neurons) has been recorded during spontaneous and vestibular induced eye movements in the alert cat. Recorded neurons were identified by their antidromic activation from the abducens nucleus and by the post-synaptic field potential induced in this nucleus. The activity of identified medial vestibular neurons increased significantly with horizontal eye position and velocity toward the contralateral side, and decreased abruptly during ipsilateral saccades. The activity of these neurons was also related to head velocity toward the ipsilateral side. The functional role and origin of eye position and velocity signals present in these vestibular neurons are discussed.     

On the predominance of anti-compensatory eye movements in vestibular nystagmus

The predominance of anti-compensatory eye movements in vestibular nystagmus recorded during sinusoidal and post-rotational tests is interpreted in terms of a mathematical model of the vestibulo-ocular system. Namely, a direct pathway between the vestibular nuclei and the saccadic mechanism is assumed. In the range of frequencies of natural head movements this pathway carries on a signal proportional to head angular velocity. Therefore, during active head movements the saccadic mechanism is forced to produce quick eye rotations in the direction of head movement and, thus, to cooperate in the task of picking up visual targets outside the visual field. During passive head movements giving rise to nystagmus the assumed pathway contributes to reduce the error in eye resetting due to the saccadic delay. Analytical considerations and simulation results seem to prove the adequacy of the proposed model.Work supported by the National Research Council (C.N.R.), Rome, Italy     

Tests of Models for Saccade–Vergence Interaction using Novel Stimulus Conditions

During natural activities, two types of eye movements - saccades and vergence - are used in concert to point the fovea of each eye at features of interest. Some electrophysiological studies support the concept of independent neurobiological substrates for saccades and vergence, namely saccadic and vergence burst neurons. Discerning the interaction of these two components is complicated by the near-synchronous occurrence of saccadic and vergence components. However, by positioning the far target below the near target, it is possible to induce responses in which the peak velocity of the vertical saccadic component precedes the peak velocity of the horizontal vergence component by approximately 75 ms. When saccade-vergence responses are temporally dissociated in this way, the vergence velocity waveform changes, becoming less skewed. We excluded the possibility that such change in skewing was due to visual feedback by showing that similar behavior occurred in darkness. We then tested a saccade-related vergence burst neuron (SVBN) model proposed by Zee et al. in J Neurophysiol 68:1624-1641 (1992), in which omnipause neurons remove inhibition from both saccadic and vergence burst neurons. The technique of parameter estimation was used to calculate optimal values for responses from human subjects in which saccadic and convergence components of response were either nearly synchronized or temporally dissociated. Although the SVBN model could account for convergence waveforms when saccadic and vergence components were nearly synchronized, it could not when the components were temporally dissociated. We modified the model so that the saccadic pulse changed the parameter values of the convergence burst units if both components were synchronized. The modified model accounted for velocity waveforms of both synchronous and dissociated convergence movements. We conclude that both the saccadic pulse and omnipause neuron inhibition influence the generation of vergence movements when they are made synchronously with saccades.     

Neurophysiology of the motoneurons of the external oculomotor nucleus in the waking cat

The spontaneous and visually induced activity of abducens motoneurons has been recorded in the alert cat. Motoneurons were identified by their antidromic activation from the ipsilateral abducens nerve. All identified motoneurons appeared related to both the position and velocity of the eye in the horizontal plane, although distributed in a wide range. Neural time constants were also measured, showing a mean value similar to that of the mechanical time constant of the oculomotor plant. According to present results, abducens motoneurons of cats and monkeys are very similar, notwithstanding some differences in their activities during saccadic movements.     

Eye movements modulate visual receptive fields of V4 neurons

The receptive field, defined as the spatiotemporal selectivity of neurons to sensory stimuli, is central to our understanding of the neuronal mechanisms of perception. However, despite the fact that eye movements are critical during normal vision, the influence of eye movements on the structure of receptive fields has never been characterized. Here, we map the receptive fields of macaque area V4 neurons during saccadic eye movements and find that receptive fields are remarkably dynamic. Specifically, before the initiation of a saccadic eye movement, receptive fields shrink and shift towards the saccade target. These spatiotemporal dynamics may enhance information processing of relevant stimuli during the scanning of a visual scene, thereby assisting the selection of saccade targets and accelerating the analysis of the visual scene during free viewing.     

The interstitial nucleus of Cajal of the cat. I. Neurons activity related to vertical eye movements

Interstitial nucleus of Cajal (INC) neurons activity was studied during vertical optokinetic nystagmus (OKN) and after-nystagmus (OKAN) in awake cats lying on their right side. The activity of one hundred neurons was recorded in the left INC and analysed in relation with the vertical component of OKN and OKAN. The activity of 27 neurons was correlated either to eye position or to both eye velocity and eye position; 18 of these neurons were recorded in their on-direction and their off-direction. The analysis of the 18 neurons showed that the activity of 8 of them was correlated to eye position in the on-direction and in the off-direction and the correlation to eye position was higher than to eye velocity; these neurons are considered as position neurons. Seven other neurons had a higher correlation to eye position that to eye velocity in the on-direction and this relation reversed in the off-direction, these neurons are considered as position-velocity neurons. Thirty two burst-neurons were activated only during quick phases of OKN and OKAN and they were silent during slow phases and periods of fixation. Nine burst neurons had an upward on-direction and 23 neurons a downward on-direction. The eye velocity-average burst frequency (ABF) and quick phase duration-burst duration relationships had low correlations and suggested that INC burst neurons were excitatory premotor neurons. Statistical analysis showed that downward on-direction burst neurons had a higher ABF that upward on-direction burst neurons. Moreover, during OKN and OKAN, the velocity sensitivity of INC burst neurons was the same. The activity of the remaining neurons (41 neurons) was not quantitatively correlated to vertical and horizontal eye movements; they were classified as irregular tonic neurons. This study shows that INC neurons carry an eye position signal which was never reported before. This supports the results of INC lesion studies which showed that INC is involved in the vertical velocity to position integration. Moreover, there is an up versus down asymmetry in the frequency of INC burst neurons.     

Unit activity in the superior colliculus of the cat following passive eye movements.

Unit response in the superior colliculus and underlying structures has been examined in the choralose-anaesthetized cat following passive movement of an occluded eye. One group of units was sensitive to small saccadic movements, responded regardless of the initial postion of the eye, and in most instances responded to movements in opposit directions. A second numerically smaller group also responded when they eye was moved at saccadic velocity but only when the eye passed a fixed point. Such units with fixed positional thresholds were found following movements in both nasal and temporal directions as well as to both upward and downward movement. Both types of unit response were found after transection of the optic nerve and were also recorded when individual extraocular muscles were subjected to controlled stretch. It is assumed that most unit activity seen after passive movement of the occluded eye is due to activity in extraocular muscle receptors. In the deep layers of the superior colliculus responses to small eye movements were found to be due to the activation of very low threshold receptors sensitive to vibration in the facial area.     

Effects of axotomy on the activity of the motor neurons of the external ocular motor nucleus during saccadic movements

The instantaneous firing frequency of cat abducens nucleus motoneurons (Mns) during spontaneous saccadic eye movements has been analyzed. Recordings were carried out from both control and axotomized Mns. Firing frequency of control Mns increased gradually during the first four to five interspike intervals, at which point maximum firing frequency was reached. Axotomized Mns showed an increase in firing frequency only up to the second or third interval, decreasing rapidly then. Linear relationships, with high correlation coefficients, were established between the first five intervals versus maximum frequency or peak eye velocity during saccades, in both control and axotomized Mns. However, the latter showed a decrease in the linear correlation from the third interval because of the decrease in the slope of the relationship. Functional implications of these results are discussed according to the present hypothesis on the effects of axotomy upon oculomotor neurons.     

Different programming modes of human saccadic eye movements as a function of stimulus eccentricity: Indications of a functional subdivision of the visual field

1. Voluntary saccadic eye movements were made toward flashes of light on the horizontal meridian, whose duration and distance from the point of fixation were varied; eye movements were measured using d.c.-electrooculography.—2. Targets within 10°–15° eccentricity are usually reached by one saccadic eye movement. When the eyes turn toward targets of more than 10°–15° eccentricity, the first saccadic eye movement falls short of the target by an angle usually not exceeding 10°. The presence of the image of the target off the fovea (visual error signal) subsequent to such an undershoot elicits, after a short interval, corrective saccades (usually one) which place the image of the target on the fovea. In the absence of a visual error signal, the probability of occurrence of corrective saccades is low, but it increases with greater target eccentricities. These observations suggest that there are different, eccentricity-dependent modes of programming saccadic eye movements.—3. Saccadic eye movements appear to be programmed in retinal coordinates. This conclusion is based on the observations that, irrespective of the initial position of the eyes in the orbit, a) there are different programming modes for eye movements to targets within and beyond 10°–15° from the fixation point, and b_ the maximum velocity of saccadic eye movements is always reached at 25° to 30° target eccentricity. —4. Distributions of latency and intersaccadic interval (ISI) are frequently multimodal, with a separation between modes of 30 to 40 msec. These observations suggest that saccadic eye movements are produced by mechanisms which, at a frequency of 30 Hz, process visual information. —5. Corrective saccades may occur after extremely short intervals (30 to 60 msec) regardless of whether or not a visual error signal is present; the eyes may not even come to a complete stop during these very short intersaccadic intervals. It is suggested that these corrective saccades are triggered by errors in the programming of the initial saccadic eye movements, and not by a visual error signal. —6. The exitence of different, eccentricity-dependent programming modes of saccadic eye movements, is further supported by anatomical, physiological, psychophysical, and neuropathological observations that suggest a dissociation of visual functions dependent on retinal eccentricity. Saccadic eye movements to targets more eccentric than 10°–15° appear to be executed by a mechanism involving the superior colliculus (perhaps independent of the visual cortex), whereas saccadic eye movements to less eccentric targets appear to depend on a mechanism involving the geniculo-cortical pathway (perhaps in collaboration with the superior colliculus).     

The composition of central programs subserving horizontal eye movements in man

A hypothesis is presented which describes, in biomechanical terms, the central programs underlying horizontal eye movements in man. It is suggested that eye movements are produced by means of programmed shifts of the so-called invariant muscle characteristics (static force vs angle of gaze). These shifts lead to a change of the equilibrium point resulting from the interaction of agnnist and antagonist muscles and, as a consequence, to movement and the attainment of a new position of gaze. A reciprocal or a coactivation command to agonist and antagonist muscles occurs when their characteristics shift with respect to the coordinate in the same or opposite directions, respectively. It is proposed that during pursuit and saccadic eye movements a supperposition of the both central commands occurs. During a saccade, the reciprocal command develops evenly up to a certain level. The initial and final levels of the reciprocal command dictate the respective position of gaze and therefore the size of the saccade. The coactivation command develops to a maximum level and is slowly switched off when the new position of gaze has been achieved. The magnitude of the coactivation command seems to be not connected with an absolute position of gaze. It provides probably a stability of the movement and, in particular, prevents overshoot and oscillation during the saccade. The same timing of these commands occurs during pursuit movements, but the magnitude of the coactivation command and the rates of the development of the both commands are less in this case and correlate with the velocity of the movement. This hypothesis enables the tension changes in the muscle during saccadic and pursuit movements to be simulated in qualitative accordance with unique experimental data obtained by Collins et al. (1975). The functional significance of superposition of these motor commands and similarity in the efferent organization of eye and limb movements are discussed.     

Sensory and behavioral properties of neurons in posterior parietal cortex of the awake, trained monkey.

Neurons in posterior parietal cortex of the awake, trained monkey respond to passive visual and/or somatosensory stimuli. In general, the receptive fields of these cells are large and nonspecific. When these neurons are studied during visually guided hand movements and eye movements, most of their activity can be accounted for by passive sensory stimulation. However, for some visual cells, the response to a stimulus is enhanced when it is to be the target for a saccadic eye movement. This enhancement is selective for eye movements into the visual receptive field since it does not occur with eye movements to other parts of the visual field. Cells that discharge in association with a visual fixation task have foveal receptive fields and respond to the spots of light used as fixation targets. Cells discharging selectively in association with different directions of tracking eye movements have directionally selective responses to moving visual stimuli. Every cell in our sample discharging in association with movement could be driven by passive sensory stimuli. We conclude that the activity of neurons in posterior parietal cortex is dependent on and indicative of external stimuli but not predictive of movement.     

Open-loop simulations of the primate saccadic system using burst cell discharge from the superior colliculus

 Saccade-related burst neurons (SRBNs) in the monkey superior colliculus (SC) have been hypothesized to provide the brainstem saccadic burst generator with the dynamic error signal and the movement initiating trigger signal. To test this claim, we performed two sets of open-loop simulations on a burst generator model with the local feedback disconnected using experimentally obtained SRBN activity as both the driving and trigger signal inputs to the model. First, using neural data obtained from cells located near the middle of the rostral to caudal extent of the SC, the internal parameters of the model were optimized by means of a stochastic hill-climbing algorithm to produce an intermediate-sized saccade. The parameter values obtained from the optimization were then fixed and additional simulations were done using the experimental data from rostral collicular neurons (small saccades) and from more caudal neurons (large saccades); the model generated realistic saccades, matching both position and velocity profiles of real saccades to the centers of the movement fields of all these cells. Second, the model was driven by SRBN activity affiliated with interrupted saccades, the resumed eye movements observed following electrical stimulation of the omnipause region. Once again, the model produced eye movements that closely resembled the interrupted saccades produced by such simulations, but minor readjustment of parameters reflecting the weight of the projection of the trigger signal was required. Our study demonstrates that a model of the burst generator produces reasonably realistic saccades when driven with actual samples of SRBN discharges. Received: 25 October 1994/Accepted in revised form: 20 June 1995     

The Mechanism of Saccade Motor Pattern Generation Investigated by a Large-Scale Spiking Neuron Model of the Superior Colliculus

The subcortical saccade-generating system consists of the retina, superior colliculus, cerebellum and brainstem motoneuron areas. The superior colliculus is the site of sensory-motor convergence within this basic visuomotor loop preserved throughout the vertebrates. While the system has been extensively studied, there are still several outstanding questions regarding how and where the saccade eye movement profile is generated and the contribution of respective parts within this system. Here we construct a spiking neuron model of the whole intermediate layer of the superior colliculus based on the latest anatomy and physiology data. The model consists of conductance-based spiking neurons with quasi-visual, burst, buildup, local inhibitory, and deep layer inhibitory neurons. The visual input is given from the superficial superior colliculus and the burst neurons send the output to the brainstem oculomotor nuclei. Gating input from the basal ganglia and an integral feedback from the reticular formation are also included.We implement the model in the NEST simulator and show that the activity profile of bursting neurons can be reproduced by a combination of NMDA-type and cholinergic excitatory synaptic inputs and integrative inhibitory feedback. The model shows that the spreading neural activity observed in vivo can keep track of the collicular output over time and reset the system at the end of a saccade through activation of deep layer inhibitory neurons. We identify the model parameters according to neural recording data and show that the resulting model recreates the saccade size-velocity curves known as the saccadic main sequence in behavioral studies. The present model is consistent with theories that the superior colliculus takes a principal role in generating the temporal profiles of saccadic eye movements, rather than just specifying the end points of eye movements.     

Neural Activity in the Macaque Putamen Associated with Saccades and Behavioral Outcome

It is now widely accepted that the basal ganglia nuclei form segregated, parallel loops with neocortical areas. The prevalent view is that the putamen is part of the motor loop, which receives inputs from sensorimotor areas, whereas the caudate, which receives inputs from frontal cortical eye fields and projects via the substantia nigra pars reticulata to the superior colliculus, belongs to the oculomotor loop. Tracer studies in monkeys and functional neuroimaging studies in human subjects, however, also suggest a potential role for the putamen in oculomotor control. To investigate the role of the putamen in saccadic eye movements, we recorded single neuron activity in the caudal putamen of two rhesus monkeys while they alternated between short blocks of pro- and anti-saccades. In each trial, the instruction cue was provided after the onset of the peripheral stimulus, thus the monkeys could either generate an immediate response to the stimulus based on the internal representation of the rule from the previous trial, or alternatively, could await the visual rule-instruction cue to guide their saccadic response. We found that a subset of putamen neurons showed saccade-related activity, that the preparatory mode (internally- versus externally-cued) influenced the expression of task-selectivity in roughly one third of the task-modulated neurons, and further that a large proportion of neurons encoded the outcome of the saccade. These results suggest that the caudal putamen may be part of the neural network for goal-directed saccades, wherein the monitoring of saccadic eye movements, context and performance feedback may be processed together to ensure optimal behavioural performance and outcomes are achieved during ongoing behaviour.     

Neural correlates of saccadic suppression in humans

When you look into a mirror and move your eyes left to right, you will see that you cannot observe your own eye movements. This demonstrates the phenomenon of saccadic suppression: during saccadic eye movements, visual sensitivity is much reduced. Given that humans make more than 100,000 eye movements each day, it is clear why suppression is needed: without it, the motion on the retina would prevent us from seeing anything at all. Psychophysical data show that suppression is stimulus selective: it is strongest for the kind of stimuli that preferentially activate magnocellular thalamic neurons. This has led to the hypothesis that saccadic suppression selectively targets the magnocellular stream. We used fMRI to find brain areas with a stimulus-selective suppression of the BOLD signal that matches the psychophysical data. We found such a neural correlate of saccadic suppression in the dorsal stream (hMT+, V7) and in ventral area V4. These areas receive magnocellular input; hence our findings are consistent with the magnocellular hypothesis. The range of effects in our data and in single cell data, however, argues against a single thalamic mechanism that suppresses all cortical input. Instead, we speculate that saccadic suppression relies on multiple mechanisms operating in different cortical areas.     

Effect of fast moving stimuli and saccadic eye movements on cell activity in visual areas V1 and V2 of behaving monkeys

Extracellular recordings were carried out in the visual cortex of behaving monkeys trained on a fixation/detection task, during which a target light was displayed stationary or suddenly moving on a tangent translucent screen. The responses of visual cortical cells to fast moving stimuli during steady fixation and those obtained during rapid eye movements (saccades) which moved their receptive field across a stationary stimulus, were studied. Areas V1 and V2 were explored. When tested with rapidly moving stimuli (500 deg/sec) during steady fixation, neurons in each area behaved in almost the same way. About one fourth of them were activated, the remainder showing either no response (little more than a half of them) or a reduction of the spontaneous firing rate. In both areas, some of the neurons activated during steady fixation did not respond or responded very weakly during eye motion at saccadic velocity (500 +/- 50 deg/sec). Neurons of this type, which we refer to as 'real motion' cells, could somehow contribute to the maintenance of visual stability during the execution of large eye movements.     

Evidence for the lateral intraparietal area as the parietal eye field.

It has long been appreciated that the posterior parietal cortex plays a role in the processing of saccadic eye movements. Only recently has it been discovered that a small cortical area, the lateral intraparietal area, within this much larger area appears to be specialized for saccadic eye movements. Unlike other cortical areas in the posterior parietal cortex, the lateral intraparietal area has strong anatomical connections to other saccade centers, and its cells have saccade-related responses that begin before the saccades. The lateral intraparietal area appears to be neither a strictly visual nor strictly motor structure; rather it performs visuomotor integration functions including determining the spatial location of saccade targets and forming plans to make eye movements.     

Interocular yoking in human saccades examined by mutual information analysis

Background

Saccadic eye movements align the two eyes precisely to foveate a target. Trial-by-trial variance of eye movement is always observed within an identical experimental condition. This has often been treated as experimental error without addressing its significance. The present study examined statistical linkages between the two eyes’ movements, namely interocular yoking, for the variance of eye position and velocity.

Methods

Horizontal saccadic movements were recorded from twelve right-eye-dominant subjects while they decided on saccade direction in Go-Only sessions and on both saccade execution and direction in Go/NoGo sessions. We used infrared corneal reflection to record simultaneously and independently the movement of each eye. Quantitative measures of yoking were provided by mutual information analysis of eye position or velocity, which is sensitive to both linear and non-linear relationships between the eyes’ movements. Our mutual information analysis relied on the variance of the eyes movements in each experimental condition. The range of movements for each eye varies for different conditions so yoking was further studied by comparing GO-Only vs. Go/NoGo sessions, leftward vs. rightward saccades.

Results

Mutual information analysis showed that velocity yoking preceded positional yoking. Cognitive load increased trial variances of velocity with no increase in velocity yoking, suggesting that cognitive load may alter neural processes in areas to which oculomotor control is not tightly linked. The comparison between experimental conditions showed that interocular linkage in velocity variance of the right eye lagged that of the left eye during saccades.

Conclusions

We conclude quantitative measure of interocular yoking based on trial-to-trial variance within a condition, as well as variance between conditions, provides a powerful tool for studying the binocular movement mechanism.

     

A novel interpretation for the collicular role in saccade generation

Recently, we found evidence that the activity of neurons in the deep layers of the monkey superior colliculus (SC) is modulated by initial eye position (gain fields). In this paper, we propose a quantitative model of the motor SC which incorporates these new findings. Inputs to the motor map represent the desired eye displacement vector (motor error), as well as initial eye position. A unit's activity in the motor map is described by multiplying a weak linear eye position sensitivity with a gaussian tuning to motor error. The motor map projects to several sets of output neurons, representing the coordinates of the desired eye displacement vector, the desired eye position in the head, and the three-dimensional ocular rotation axis for saccades in Listing's plane, respectively. All these signals have been hypothesized in the literature to drive the saccade burst generator. We show that these signals can be extracted from the motor map by a linear weighting of the population activity. The saccadic system may employ all coding strategies in parallel to ensure high spatial accuracy in many complex sensorimotor tasks, such as orienting to multimodal stimuli.     

Dorsal premotor neurons encode the relative position of the hand, eye, and goal during reach planning

When reaching to grasp an object, we often move our arm and orient our gaze together. How are these movements coordinated? To investigate this question, we studied neuronal activity in the dorsal premotor area (PMd) and the medial intraparietal area (area MIP) of two monkeys while systematically varying the starting position of the hand and eye during reaching. PMd neurons encoded the relative position of the target, hand, and eye. MIP neurons encoded target location with respect to the eye only. These results indicate that whereas MIP encodes target locations in an eye-centered reference frame, PMd uses a relative position code that specifies the differences in locations between all three variables. Such a relative position code may play an important role in coordinating hand and eye movements by computing their relative position.