Two types of eye movements during electrical stimulation of the rostral and caudal parts of the medial frontal "oculomotor" area in cats

The character of eye movements during electrical stimulation of the medial wall of the brain beneath the cruciate sulcus and of the inferior wall of the cruciate sulcus itself in the frontal cortex was investigated in waking cats. Stimulation of this part of the brain evoked two types of eye movements: unidirectional concomitant saccades, whose direction and amplitude were independent of the original position of the eyes in the orbits, and saccades into the central position (so-called centering saccades). Unidirectional saccades appeared in response to stimulation of the caudal part of the investigated zone, centering saccades in response to stimulation of its rostral part. Analysis of the directions and amplitudes of unidirectional saccades suggested the retinotopic organization of the caudal zone. Systematic changes in the magnitude and direction of vertical saccades during stimulation of the deep parts of the cruciate sulcus indicated previsely the projection of the vertical meridian of the retina. Reappearance of vertical saccades evoked by stimulation of certain parts of the medial wall of the brain suggests the existence of more than one retinotopically organized zone in this region. Inconstancy of stereotaxic coordinates of the oculomotor area, studied in different animals, was noted.Institute for Problems in Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 16, No. 6, pp. 761–766, November–December, 1984.     

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     

Blink Perturbation Effects on Saccades Evoked by Microstimulation of the Superior Colliculus

Current knowledge of saccade-blink interactions suggests that blinks have paradoxical effects on saccade generation. Blinks suppress saccade generation by attenuating the oculomotor drive command in structures like the superior colliculus (SC), but they also disinhibit the saccadic system by removing the potent inhibition of pontine omnipause neurons (OPNs). To better characterize these effects, we evoked the trigeminal blink reflex by delivering an air puff to one eye as saccades were evoked by sub-optimal stimulation of the SC. For every stimulation site, the peak and average velocities of stimulation with blink movements (SwBMs) were lower than stimulation-only saccades (SoMs), supporting the notion that the oculomotor drive is weakened in the presence of a blink. In contrast, the duration of the SwBMs was longer, consistent with the hypothesis that the blink-induced inhibition of the OPNs could prolong the window of time available for oculomotor commands to drive an eye movement. The amplitude of the SwBM could also be larger than the SoM amplitude obtained from the same site, particularly for cases in which blink-associated eye movements exhibited the slowest kinematics. The results are interpreted in terms of neural signatures of saccade-blink interactions.     

A competitive integration model of exogenous and endogenous eye movements

We present a model of the eye movement system in which the programming of an eye movement is the result of the competitive integration of information in the superior colliculi (SC). This brain area receives input from occipital cortex, the frontal eye fields, and the dorsolateral prefrontal cortex, on the basis of which it computes the location of the next saccadic target. Two critical assumptions in the model are that cortical inputs are not only excitatory, but can also inhibit saccades to specific locations, and that the SC continue to influence the trajectory of a saccade while it is being executed. With these assumptions, we account for many neurophysiological and behavioral findings from eye movement research. Interactions within the saccade map are shown to account for effects of distractors on saccadic reaction time (SRT) and saccade trajectory, including the global effect and oculomotor capture. In addition, the model accounts for express saccades, the gap effect, saccadic reaction times for antisaccades, and recorded responses from neurons in the SC and frontal eye fields in these tasks.     

Optimal control of saccades by spatial-temporal activity patterns in the monkey superior colliculus

A major challenge in computational neurobiology is to understand how populations of noisy, broadly-tuned neurons produce accurate goal-directed actions such as saccades. Saccades are high-velocity eye movements that have stereotyped, nonlinear kinematics; their duration increases with amplitude, while peak eye-velocity saturates for large saccades. Recent theories suggest that these characteristics reflect a deliberate strategy that optimizes a speed-accuracy tradeoff in the presence of signal-dependent noise in the neural control signals. Here we argue that the midbrain superior colliculus (SC), a key sensorimotor interface that contains a topographically-organized map of saccade vectors, is in an ideal position to implement such an optimization principle. Most models attribute the nonlinear saccade kinematics to saturation in the brainstem pulse generator downstream from the SC. However, there is little data to support this assumption. We now present new neurophysiological evidence for an alternative scheme, which proposes that these properties reside in the spatial-temporal dynamics of SC activity. As predicted by this scheme, we found a remarkably systematic organization in the burst properties of saccade-related neurons along the rostral-to-caudal (i.e., amplitude-coding) dimension of the SC motor map: peak firing-rates systematically decrease for cells encoding larger saccades, while burst durations and skewness increase, suggesting that this spatial gradient underlies the increase in duration and skewness of the eye velocity profiles with amplitude. We also show that all neurons in the recruited population synchronize their burst profiles, indicating that the burst-timing of each cell is determined by the planned saccade vector in which it participates, rather than by its anatomical location. Together with the observation that saccade-related SC cells indeed show signal-dependent noise, this precisely tuned organization of SC burst activity strongly supports the notion of an optimal motor-control principle embedded in the SC motor map as it fully accounts for the straight trajectories and kinematic nonlinearity of saccades.     

Manipulating intent: evidence for a causal role of the superior colliculus in target selection

The superior colliculus (SC) is well known for its role in the motor control of saccades. Recent work has shown that it also plays a role in the selection of saccades, but a causal role in the process of target selection has not been demonstrated. We applied subthreshold microstimulation to the SC while monkeys performed a task requiring them to select a stimulus as the target for a pursuit or saccade movement. Stimulation increased the proportion of selections toward the stimulus that appeared contralateral to the site of stimulation and also decreased their latencies. For pursuit, this stimulation-induced contralateral response bias was with respect to the initial target location and not the direction of eye movement, demonstrating a causal effect on target choice distinct from any effect on motor preparation. These results show that the SC helps decide the object of the next movement, beyond its traditional responsibility of saccade production.     

Neural network simulations of the primate oculomotor system

The performance of a neural network that simulates the vertical saccade-generating portion of the primate brain is evaluated. Consistent with presently available anatomical evidence, the model makes use of an eye displacement signal for its feedback. Its major features include a simple mechanism for resetting its integrator at the end of each saccade, the ability to generate staircases of saccades in response to stimulation of the superior colliculus, and the ability to account for the monotonic relation between motor error and the instantaneous discharge of presaccadic neurons of the superior colliculus without placing the latter within the local feedback loop. Several experimentally testable predictions about the effects of stimulation or lesion of saccaderelated areas of the primate brain are made on the basis of model output in response to “stimulation” or “lesion” of model elements.     

Neural network simulations of the primate oculomotor system. V. Eye–head gaze shifts

We examined the performance of a dynamic neural network that replicates much of the psychophysics and neurophysiology of eye–head gaze shifts without relying on gaze feedback control. For example, our model generates gaze shifts with ocular components that do not exceed 35° in amplitude, whatever the size of the gaze shifts (up to 75° in our simulations), without relying on a saturating nonlinearity to accomplish this. It reproduces the natural patterns of eye–head coordination in that head contributions increase and ocular contributions decrease together with the size of gaze shifts and this without compromising the accuracy of gaze realignment. It also accounts for the dependence of the relative contributions of the eyes and the head on the initial positions of the eyes, as well as for the position sensitivity of saccades evoked by electrical stimulation of the superior colliculus. Finally, it shows why units of the saccadic system could appear to carry gaze-related signals even if they do not operate within a gaze control loop and do not receive head-related information.     

A two dimensional model for saccade generation

A model for the generation of oblique saccades is constructed by extending and modifying the one dimensional local feedback model. It is proposed that the visual system stores target location in inertial coordinates, but that the feedback loop which guides saccades works in retinotopic coordinates. To achieve straight trajectories for centripetal and centrifugal saccades in all meridians, a comparator computes motor error as a vector and uses the vectorial error signal to drive two orthogonally-acting burst generators. The generation of straight saccade trajectories when the extraocular muscles are of unequal strengths requires the introduction of a burst-tonic cell input to motor neurons. The model accounts for the results of two-site stimulation of the superior colliculus and frontal eye fields by allowing simultaneous activation of more than one comparator. The postulated existence of multiple comparators suggests that motor error may be computed topographically.     

Analysis of the middle latency evoked potentials to angular acceleration impulses in man

The middle latency vestibular evoked potential (ML-VsEP) recorded with scalp electrodes in man in response to impulses of angular acceleration is dominated by a forehead positive peak at about 15 ms and a negative peak at about 20 ms; the peak amplitude of this component is about 30 μV. This is followed by slower, smaller amplitude activity. The latency of this initial peak is similar to the latency of the vestibulo-ocular reflex (VOR) in monkeys. The present study was undertaken to elucidate the possible relation between the ML-VsEPs and VOR. This included recordings from forehead-mastoid electrodes (sites used to record VsEP) and other scalp electrodes and the recording of potentials due to eye movement: the electro-oculogram. Direct recording of eye movements was also conducted using an infra-red reflection device in those experiments in which the head was not moved. The recordings were conducted in man during vestibular stimulation eliciting VsEPs, during voluntary eye movements and during caloric and optokinetic stimulation. These experiments indicated that the 15–20 ms component of the ML-VsEP was not due to movements of the eye (corneoretinal dipole). The large amplitude 15–20 ms component of the ML-VsEP was similar in general magnitude, waveform, polarity, duration and rise time to the highly synchronous pre-saccadic spike (neural and/or myogenic) which precedes nystagnys and voluntary saccades. It therefore probably represents vestibular-initiated electrical activity in motor units of the extra-ocular muscles which then produce anti-compensatory saccades.     

A model of visually-guided smooth pursuit eye movements based on behavioral observations

We report a model that reproduces many of the behavioral properties of smooth pursuit eye movements. The model is a negative-feedback system that uses three parallel visual motion pathways to drive pursuit. The three visual pathways process image motion, defined as target motion with respect to the moving eye, and provide signals related to image velocity, image acceleration, and a transient that occurs at the onset of target motion. The three visual motion signals are summed and integrated to produce the eye velocity output of the model. The model reproduces the average eye velocity evoked by steps of target velocity in monkeys and humans and accounts for the variation among individual responses and subjects. When its motor pathways are expanded to include positive feedback of eye velocity and a switch, the model reproduces the exponential decay in eye velocity observed when a moving target stops. Manipulation of this expanded model can mimic the effects of stimulation and lesions in the arcuate pursuit area, the middle temporal visual area (MT), and the medial superior temporal visual area (MST).     

Encoding of Time-varying Stimuli in Populations of Cultured Neurons

We wondered whether random populations of dissociated cultured cortical neurons, despite of their lack of structure and/or regional specialization, are capable of modulating their neural activity as the effect of a time-varying stimulation – a simulated ‘sensory’ afference. More specifically, we used localized low-frequency, non-periodic trains of stimuli to simulate sensory afferences, and asked how much information about the original trains of stimuli could be extracted from the neural activity recorded at the different sites. Furthermore, motivated by the results of studies performed both in vivo and in vitro on different preparations, which suggested that isolated spikes and bursts may play different roles in coding time-varying signals, we explored the amount of such ‘sensory’ information that could be associated to these different firing modes. Finally, we asked whether and how such ‘sensory’ information is transferred from the sites of stimulation (i.e., the ‘sensory’ areas), to the other regions of the neural populations. To do this we applied stimulus reconstruction techniques and information theoretic concepts that are typically used to investigate neural coding in sensory systems. Our main results are that (1) slow variations of the rate of stimulation are coded into isolated spikes and in the time of occurrence of bursts (but not in the bursts’ temporal structure); (2) increasing the rate of stimulation has the effect of increasing the proportion of isolated spikes in the average evoked response and their importance in coding for the stimuli; and, (3) the ability to recover the time course of the pattern of stimulation is strongly related to the degree of functional connectivity between stimulation and recording sites. These observations parallel similar findings in intact nervous systems regarding the complementary roles of bursts and tonic spikes in encoding sensory information. Our results also have interesting implications in the field of neuro-robotic interfaces. In fact, the ability of populations of neurons to code information is a prerequisite for obtaining hybrid systems, in which neuronal populations are used to control external devices.     

A model that integrates eye velocity commands to keep track of smooth eye displacements

Past results have reported conflicting findings on the oculomotor system’s ability to keep track of smooth eye movements in darkness. Whereas some results indicate that saccades cannot compensate for smooth eye displacements, others report that memory-guided saccades during smooth pursuit are spatially correct. Recently, it was shown that the amount of time before the saccade made a difference: short-latency saccades were retinotopically coded, whereas long-latency saccades were spatially coded. Here, we propose a model of the saccadic system that can explain the available experimental data. The novel part of this model consists of a delayed integration of efferent smooth eye velocity commands. Two alternative physiologically realistic neural mechanisms for this integration stage are proposed. Model simulations accurately reproduced prior findings. Thus, this model reconciles the earlier contradictory reports from the literature about compensation for smooth eye movements before saccades because it involves a slow integration process. Action Editor: Jonathan D. Victor     

A model of the saccade-generating system that accounts for trajectory variations produced by competing visual stimuli

Variable saccade trajectories are produced in visual search paradigms in which multiple potential target stimuli are present. These variable trajectories provide a rich source of information that may lead to a deeper understanding of the basic control mechanisms of the saccadic system. We have used published behavioral observations and neural recordings in the superior colliculus (SC), gathered in monkeys performing visual search paradigms, to guide the construction of a new distributed model of the saccadic system. The new model can account for many of the variations in saccade trajectory produced by the appearance of multiple visual stimuli in a search paradigm. The model uses distributed feedback about current eye motion from the brainstem to the SC to reduce activity there at physiologically realistic rates during saccades. The long-range lateral inhibitory connections between SC cells used in previous models have been eliminated to match recent physiological evidence. The model features interactions between visually activated multiple populations of cells in the SC and distributed and topologically organized inhibitory input to the SC from the SNr to produce some of the types of variable saccadic trajectories, including slightly curved and averaging saccades, observed in visual search tasks. The distributed perisaccadic disinhibition of SC from the substantia nigra (SNr) is assumed to have broad spatial tuning. In order to produce the strongly curved saccades occasionally recorded in visual search, the existence of a parallel input to the saccadic burst generators in addition to that provided by the distributed input from the SC is required. The spatiotemporal form of this additional parallel input is computed based on the assumption that the input from the model SC is realistic. In accordance with other recent models, it is assumed that the parallel input comes from the cerebellum, but our model predicts that the parallel input is delayed during highly curved saccadic trajectories.     

Mathematical models of eye movements in reading: a possible role for autonomous saccades

 An efficient method for the exact numerical simulation of semi-Markov processes is used to study minimal models of the control of eye movements in reading. When we read a text, typical sequences of fixations form a rather complicated trajectory – almost like a random walk. Mathematical models of eye movement control can account for this behavior using stochastic transition rules between few discrete internal states, which represent combinations of certain stages of lexical access and saccade programs. We show that experimentally observed fixation durations can be explained by residence-time-dependent transition probabilities. Stochastic processes with this property are known as semi-Markov processes. For our numerical simulations we use the minimal process method (Gillespie algorithm), which is an exact and efficient simulation algorithm for this class of stochastic processes. Within this mathematical framework, we study different forms of coupling between eye movements and shifts of covert attention in reading. Our model lends support to the existence of autonomous saccades, i.e., the hypothesis that initiations of saccades are not completely determined by lexical access processes. Received: 21 March 2000 / Accepted in revised form: 10 January 2001     

A new visual area on the inferior wall of the cat cruciate sulcus

Properties of 187 neurons in the inferior wall of the cruciate sulcus, in an area where electrical stimulation evoked unidirectional saccadic eye movements, were investigated in waking cats. Of the total number 172 responded to visual stimulation. Neurons in the surface layers of the cortex responded to simple visual stimuli: light or dark spots or bars, both stationary and moving at speeds of around 30 deg/sec. These neurons showed no selectivity as regards stimulus orientation but sometimes behaved selectively toward the direction of their movements. In the intermediate layers the maximal neuronal response was obtained to a model of a bird flaping its wings. Neuronal responses in the depth of the cortex were characterized by selectivity to movement of stimuli toward or away from the animal in a certain part of the visual field, irrespective of whether a light stimulus was presented against a dark background or a dark stimulus against the light background. Responses to visual stimulation were exhibited only if the animal was in a state of activation, when the EEG showed desynchronization, and they were absent in a state of quite wakefulness. No responses were obtained to auditory or somatic stimulation. Responses to visual stimulation were not found in neurons of the medial wall of the brain beneath the cruciate sulcus, but responses were recorded to eye movements of definite size or orientation. It is postulated that at least two contiguous retinotopically organized zones exist in this part of the brain. Activity of one of them is connected with visual function, that of the other with eye movements.Institute for Problems in Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 16, No. 6, pp. 766–773, November–December, 1984.     

Linear ensemble-coding in midbrain superior colliculus specifies the saccade kinematics

Recently, we proposed an ensemble-coding scheme of the midbrain superior colliculus (SC) in which, during a saccade, each spike emitted by each recruited SC neuron contributes a fixed minivector to the gaze-control motor output. The size and direction of this 'spike vector' depend exclusively on a cell's location within the SC motor map (Goossens and Van Opstal, in J Neurophysiol 95: 2326-2341, 2006). According to this simple scheme, the planned saccade trajectory results from instantaneous linear summation of all spike vectors across the motor map. In our simulations with this model, the brainstem saccade generator was simplified by a linear feedback system, rendering the total model (which has only three free parameters) essentially linear. Interestingly, when this scheme was applied to actually recorded spike trains from 139 saccade-related SC neurons, measured during thousands of eye movements to single visual targets, straight saccades resulted with the correct velocity profiles and nonlinear kinematic relations ('main sequence properties' and 'component stretching'). Hence, we concluded that the kinematic nonlinearity of saccades resides in the spatial-temporal distribution of SC activity, rather than in the brainstem burst generator. The latter is generally assumed in models of the saccadic system. Here we analyze how this behaviour might emerge from this simple scheme. In addition, we will show new experimental evidence in support of the proposed mechanism.     

Influence of the motor cortex on lateral geniculate responses evoked in the cat by contralateral superior colliculus stimulation

It is shown that in nembutal anesthetized cats, a single stimulation of motor cortex (MC) causes a response in lateral geniculate nucleus (LGN). The development of this response had a conditioning effect on the LGN response evoked by stimulation of the contralateral superior colliculus (SC), markedly inhibiting it. The degree of this inhibition depended on the time interval between the cortical conditioning stimulation and the tectal test stimulation. A single conditioning MC stimulation did not noticeably change the LGN responses evoked by a light stimulus, but markedly inhibited visual responses from deep SC layers (those regions which on stimulation gave rise to LGN responses). From the results, it is suggested that the MC monitors the execution of tectal influences on LGN function at the tectal level rather than the geniculate level, and it is precisely by this means that it regulates saccadic suppression of LGN function, in the realization of which, as presumed earlier, the SC takes part.A. I. Karaev Institute of Physiology, Azerbaijan Academy of Sciences, Baku. Translated from Neirofiziologiya, Vol. 24, No. 4, July–August 1992.     

Attention governs action in the primate frontal eye field

While the motor and attentional roles of the frontal eye field (FEF) are well documented, the relationship between them is unknown. We exploited the known influence of visual motion on the apparent positions of targets, and measured how this illusion affects saccadic eye movements during FEF microstimulation. Without microstimulation, saccades to a moving grating are biased in the direction of motion, consistent with the apparent position illusion. Here we show that microstimulation of spatially aligned FEF representations increases the influence of this illusion on saccades. Rather than simply impose a fixed-vector signal, subthreshold stimulation directed saccades away from the FEF movement field, and instead more strongly in the direction of visual motion. These results demonstrate that the attentional effects of FEF stimulation govern visually guided saccades, and suggest that the two roles of the FEF work together to select both the features of a target and the appropriate movement to foveate it.