A random walk model of fast-phase timing during optokinetic nystagmus

 Most vertebrate animals produce optokinetic nystagmus in response to rotation of their visual surround. Nystagmus consists of an alternation of slow-phase eye rotations, which follow the surround, and fast-phase eye rotations, which quickly reset eye position. The time intervals between fast phases vary stochastically, even during optokinetic nystagmus produced by constant velocity rotation of a uniform surround. The inter-fast-phase interval distribution has a long tail, and intervals that are long relative to the mode become even more likely as constant surround velocity is decreased. This paper provides insight into fast-phase timing by showing that the process of fast-phase generation during constant velocity optokinetic nystagmus is analogous to a random walk with drift toward a threshold. Neurophysiologically, the output of vestibular nucleus neurons, which drive the slow phase, would approximate a random walk with drift because they integrate the noisy, constant surround velocity signal they receive from the visual system. Burst neurons, which fire a burst to drive the fast phase and reset the slow phase, are brought to threshold by the vestibular nucleus neurons. Such a nystagmic process produces stochastically varying inter-fast-phase intervals, and long intervals emerge naturally because, as drift rate (related to surround velocity) decreases, it becomes more likely that any random walk can meander for a long time before it crosses the threshold. The theoretical probability density function of the first threshold crossing times of random walks with drift is known to be that of an inverse Gaussian distribution. This probability density function describes well the distributions of the intervals between fast phases that were either determined experimentally, or simulated using a neurophysiologically plausible neural network model of fast-phase generation, during constant velocity optokinetic nystagmus. Received: 1 June 1995/Accepted in revised form: 15 February 1996     

Oculomotor areas in the rabbit's midbrain and pretectum

The role of some meso- and diencephalic structures in eye movements was investigated by ablation and stimulation experiments. Optokinetic nystagmus was abolished by small lesions in the lateral pretectum, but not by complete removal of the superior colliculi. Stimulation of the superior colliculus and other visual centers was effective in eliciting nystagmus (slow phase ipsilateral), but the most efficient trigger zones are found in the lateral pretectum and the midbrain tegmentum. Only from these areas could nystagmus still be elicited after degeneration of the primary optic fibers. The lateral pretectal trigger zone is probably identical with the nucleus of the optic tract. It is postulated that this nucleus is an essential station for horizontal optokinetic reactions. Saccades were obtained by stimulation of the mesencephalic central grey, but not for any visual centers such as the superior colliculus.     

Oculomotor areas in the rabbits midbrain and pretectum.

The role of some meso- and diencephalic structures in eye movements was investigated by ablation and stimulation experiments. Optokinetic nystagmus was abolished by small lesions in the lateral pretectum, but not by complete removal of the superior colliculi. Stimulation of the superior colliculus and other visual centers was effective in eliciting nystagmus (slow phase ipsilateral), but the most efficient trigger zones are found in the lateral pretectum and the midbrain tegmentum. Only from these areas could nystagmus still be elicited after degeneration of the primary optic fibers. The lateral pretectal trigger zone is probably identical with the nucleus of the optic tract. It is postulated that this nucleus is an essential station for horizontal optokinetic reactions. Saccades were obtained by stimulation of the mesencephalic central grey, but not for any visual centers such as the superior colliculus.     

Central adaptation models of the vestibulo-ocular and optokinetic systems

A theoretical analysis of two models of the vestibulo-ocular and optokinetic systems was performed. Each model contains a filter element in the vestibular periphery to account for peripheral adaptation, and a filter element in the central vestibulooptokinetic circuit to account for central adaptation. Both models account for1 adaptation, i.e. a response decay to a constant angular acceleration input, in both peripheral vestibular afferent and vestibulo-ocular reflex (VOR) responses and2 the reversal phases of optokinetic after-nystagmus (OKAN) and the VOR and3 oscillatory behavior such as periodic alternating nystagmus. The two models differ regarding the order of their VOR transfer function. Also, they predict different OKAN patterns following a prolonged optokinetic stimulus. These models have behavioral implications and suggest future experiments.     

Responses of optokinetic neurons in the pretectum and accessory optic system of the pigeon to large-field plaids

The accessory optic system and pretectum are highly conserved brainstem visual pathways that process the visual consequences of self-motion (i.e. optic flow) and generate the optokinetic response. Neurons in these nuclei have very large receptive fields in the contalateral eye, and exhibit direction-selectivity to large-field moving stimuli. Previous research on visual motion pathways in the geniculostriate system has employed "plaids" composed of two non-parallel sine-wave gratings to investigate the visual system's ability to detect the global direction of pattern motion as opposed to the direction of motion of the components within the plaids. In this study, using standard extracellular techniques, we recorded the responses of 47 neurons in the nucleus of the basal optic root of the accessory optic system and 49 cells in the pretectal nucleus lentiformis mesencephali of pigeons to large-field gratings and plaids. We found that most neurons were classified as pattern-selective (41-49%) whereas fewer were classified as component-selective (8-17%). There were no striking differences between nucleus of the basal optic root and lentiformis mesencephali neurons in this regard. These data indicate that most of the input to the optokinetic system is orientation-insensitive but a small proportion is orientation-selective. The implications for the connectivity of the motion processing system are discussed.     

Effect of the distance of optokinetic stimuli from the eyes on certain parameters of the optokinetic nystagmus.

The above effect was studied in 65 subjects with normal vision (mean age 20 years) in investigations in which the following factors were successively changed: distance of optokinetic stimuli from the eyes; this distance and angular velocity of stimuli; distance and frequency of stimuli or finally distance and accommodation level. The angular velocity of the pursuit nystagmus phase was found to be by far the highest and simultaneously the closest to the angular velocity of optokinetic stimuli when the latter are 1.5m from the eyes. With shorter distances, the velocity of the pursuit movements lags steadily behind that of stimulus velocity. This change is conditioned by changes in OKN amplitude since its frequency as a whole does not change. Even though the accommodation level significantly affects the velocity of the pursuit nystagmus phase, the dependence on the distance of optokinetic stimuli from the eyes persists even after atropinization. The interpretation of these findings must take into account sepcifically the demands on accommodation, convergence, and on visual attention which are increased with shorter distances.     

A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement.

The directional selectivity of retinal ganglion cell responses represents a primitive pattern recognition that operates within a retinal neural circuit. The cellular origin and mechanism of directional selectivity were investigated by selectively eliminating retinal starburst amacrine cells, using immunotoxin-mediated cell targeting techniques. Starburst cell ablation in the adult retina abolished not only directional selectivity of ganglion cell responses but also an optokinetic eye reflex derived by stimulus movement. Starburst cells therefore serve as the key element that discriminates the direction of stimulus movement through integrative synaptic transmission and play a pivotal role in information processing that stabilizes image motion.     

Optokinetic horizontal head nystagmus in the frog after regeneration of transected retinal fibres

The recovery of optokinetic responses during regeneration of transected retinal fibres was studied. Regenerated optic fibres were demonstrated by the cobaltfilling technique. After transection of the chiasma in the midline in most of the cases regenerating retinal fibres did not cross, but terminated in ipsilateral visual centres. Aberrant fibres were found in the telencephalon, the periventricular region of the diencephalon, anterior-, posterior- and ventral tegmental commissures and in the isthmic nucleus. In one group of animals optokinetic responses did not return after regeneration of retinal fibres. Re-innervation was either symmetrical on both sides from one eye, or terminal fibres were disorganized. In the second group of animals normal optokinetic nystagmus (OKN) returned. In these cases the fibres were symmetrically distributed on both sides or, alternatively, the crossed fibres outnumbered the ipsilateral ones. The third group of animals showed reversed OKN, spontaneous turning of the head, circling or head nystagmus. Here the majority of regenerated fibres termined ipsilaterally. When the OKN returned, the retinal projection was always restored in the pretectal region. Contrary to our earlier work, we concluded that the basal optic nucleus is not essential for horizontal optokinetic head nystagmus because in a few animals, retinal fibres did not invated this nucleus, and in spite of this the OKN could be evoked. We think now that the most important structure (as an input channel) for horizontal OKN of frogs is the pretectal region.     

The optokinetic response in wild type and white zebra finches

Optic flow is a main source of information about self movement and the three-dimensional composition of the environment during locomotion. It is processed by the accessory optic system in all vertebrates. The optokinetic response is elicited by rotational optic flow, e.g. in a rotating drum lined with vertical stripes. We investigated here the effect of rotational optic flow on the optokinetic response in wild type and white zebra finches. The highest stimulus velocity eliciting an optokinetic response (upper velocity threshold) was dependent on stimulus direction and illumination level, but was not different between the colour morphs. The upper velocity threshold was higher with temporal to nasal movements in monocularly exposed birds and symmetrical with binocular exposure. Its increase with illumination level followed Fechner's law and reached a plateau at about 560 Lux. In bright daylight, white birds did not show optokinetic responses. We conclude that the altered wiring of the visual system of white birds has no influence on accessory optic system function. The unwillingness of white birds to respond with optokinetic response in bright daylight may be due to a substantial lack of inhibition within the visual system as demonstrated earlier, which may enhance the sensibility to glare.     

运动图形刺激时家兔的视动震颤反应

旨在用实验方法研究家兔的视动震颤（ＯＫＮ）眼动特点以及单侧前庭迷路损伤对ＯＫＮ的影响,结果表明：单眼刺激时,家兔的ＯＫＮ反应存在着从颞侧到鼻侧方向的方向优势;恒定速度刺激时,刺激开始后,家兔的ＯＫＮ眼动跟踪速度具有从小到大最后趋于稳态的建立过程,刺激消失后,存在眼动速度由大到小直到消失的视动后震颤（ＯＫＡＮ）反应,这两个过程反应了ＯＫＮ系统中可能存在速度存储机制及其对ＯＫＮ眼动的控制作用;单侧前庭     

The optokinetic head nystagmogram of the frog.

An electronic device for recording optokinetic head nystagmus is described. By feeding a point-like mass (radiator) with an alternating current generator, alternating voltage can be measured on a large flat plate (receptor), which depends on the distance of the radiator from the receptor. The radiator was fixed on the head of the frog, and could move between a pair of receptors. Voltage changes during head motions can be recorded in the form of nystagmogram. The head nystagmogram of the frog proved to be similar to that of mammals. Rotation of the optokinetic drum to one direction for several minutes resulted in habituation (decrease of frequency or stopping of head motions). Based on the frequency and amplitude pattern several types of optokinetic head nystagmus could be identified.     

家兔的开环及闭环视动震颤（OKN）研究

研究了家兔闭环及开环状态的ＯＫＮ反应。闭环时,ＯＫＮ眼动速度与刺激速度成正比,增益接近１。当固定受刺激眼形成开环状态时,ＯＫＮ眼动速度远大于刺激速度,增益可达１０２左右,说明ＯＫＮ系统是由运动跟踪的负反馈机制控制的;刺激范围缩小则眼动反应减弱,表明ＯＫＮ系统对运动信息具有空间总和作用;以视野中不同高度的局部刺激时,发现视网膜中央视带比周边部对ＯＫＮ刺激的敏感性高;单光点刺激视带中央可诱发出清楚的ＯＫＮ反应,这为临床上应用ＯＫＮ客观测定视网膜功能和运动感知提供了可能性。     

The interstitial nucleus of Cajal of the cat. II. Effects of kainic acid lesion on vertical optokinetic nystagmus and after-nystagmus

The effects of bilateral lesions of the interstitial nucleus of Cajal (INC) by ka?nic acid on vertical optokinetic nystagmus (OKN) and after-nystagmus (OKAN) were studied in four cats: in three cats, in the acute stage from 1 to 60 days after the lesions; in the fourth cat, they were studied 3 years after the lesions were made. Histological control of lesions showed that the whole INC was bilaterally destroyed in two cats of the acute group and only the upper part of INC in the third cat. In the chronic cat, the density of cell bodies in both INC was lower than normal. In the acute group, the cats exhibited a spontaneous downward eye drift in light and in darkness. During an upward optokinetic stimulation, the effect of INC lesions was dramatic: upward slow phases and downward quick phases of OKN were abolished. Sixty days post lesions, small upward slow eye movements were again observed. During a downward optokinetic stimulation, the defect was much less; in particular, after a slight impairment of downward slow phases, during the first days post lesions, they recovered quickly. The secondary optokinetic after nystagmus (OKAN II) ensuing a downward OKN was cancelled and did not reappear 60 days post lesions. In the chronic stage, three years after the lesions, during an upward optokinetic stimulation, the cat showed upward slow phases with velocities close to normal. However, upward slow phases were curved: the velocity at the end of the slow phases was lower than at the beginning. After an upward OKN (the direction of slow phases gives the direction of the OKN and OKAN), the ensuing OKAN was present but abnormal.     

运图象刺动激的视动振颤(OKN)眼动反应的速度跟踪特性

本文用传统的转筒式运动条纹刺激及电视运动条纹图形刺激两种方法进行了OKN实验,对所引起的OKN反应进行了定量比较,结果证明两者的刺激效果是相似的;用电视运动图象刺激方法,分别在中心视场和周边视场进行刺激实验,阐明了OKN主要是由作用于视网膜中央区域的运动图象刺激所引起的;并对OKN的动态反应进行了实验分析,在正弦速度刺激下,OKN增益主要取决于刺激运动的加速度,而不是单纯取决于刺激运动的速度或频率,并在脉冲速度刺激的OKN实验中,用动态反应时间阐明了这一结论.     

Static cervical-ocular reflex and optokinetic reflex interaction in rabbits

Summary The effect that tonic eye deviations, induced by angular deviation of the torso, have on the characteristics of optokinetic (OK) nystagmus was studied in rabbits. When the slow component of the OK nystagmus moved in the direction of the tonic eye deviation, the amplitude of the slow and fast components of the nystagmus was decreased and their frequency was increased, whereas when the slow component moved in the opposite direction, the amplitude and the frequency of the nystagmus were not different from those when the head and torso were aligned.Under the influence of neck reflexes, the total range of eye movements was double that when the torso was aligned with the head. The place in the orbit where the fast-component is initiated — the so-called fast-component threshold — was deviated in the direction of the neck-reflex-induced tonic eye deviation. The characteristics of the fast component, however, except for its amplitude, were not affected by the change of location of the fast-component threshold.These data indicate that the OK reflex function, as judged by measurement of the slow component velocity, is not affected by neck-vestibular reflexes. They also show that the fast-component threshold is dependent on parameters other than the actual orbital position and that there must be an internal representation of the range of possible eye movements within the brain to regulate the production of fast components.Abbreviations OK optokinetic - CW clockwise - CCW counterclockwise - CNS central nervous system This work was supported by grants NS07059, NS09823, and NS08335 from the National Institutes of Health     

The effect of lateral inclinations upon optokinetic and postoptokinetic nystagmus in pigeons

Optokinetic stimulation with the angle velocity 10 degrees/s was carried out in pigeons in differently bent postures. No difference in effects of dynamic and static inclinations upon optokinetic and postoptokinetic nystagmus was found. Neither any rigid connection was found between the inclination direction and the sign of the response change. The data obtained are at variance with the hypothesis of gravity-dependent changes of the "velocity accumulator" time constant as the only cause of changes in the optokinetic and postoptokinetic responses under conditions of dynamic or static inclinations.     

Two types of response property in otolith-optokinetic interaction.

Otolithic influence on optokinetic eye-movements (visual-vestibular interaction) was investigated using oscillation of a lateral linear acceleration-step combined with optokinetic stimulation. According to our preliminary study using a 40-deg/s optokinetic stimulus speed at 0.3 and 0.5 G acceleration-steps, the interaction was characterized by a linear addition during the agonistic stimulus condition, but by suppression of the otolith-ocular reflex during the antagonistic stimulus condition. In the present study, we further examined the interaction using 3 different optokinetic speeds at an acceleration step of 0.3 G. It was revealed an additional type of response property that was characterized by marked elevation in the eye velocity with increase in the optokinetic stimulus speed, probably due to the gain increase in the optokinetic response velocity. In either type of the response property, however, the interaction seemed to be nonlinear in the otolith system, being in contrast to linear interaction postulated for the semicircular canal system.     

The fast phase of optokinetic nystagmus in the locust

ABSTRACT. When their visual environment is rotated about them, freely moving locusts make the typical slow (following) and fast (flick back) phases of optokinetic nystagmus. The fast phase was examined and is compared with that of Crustacea and vertebrates. It is unusual in the locust in that it is symmetrical about the body midline. Mechanoreceptors play a significant role in maintaining the fast phase reset function.     

On the distribution of fast-phase intervals in optokinetic and vestibular nystagmus

 Histograms of fast-phase intervals in human optokinetic and vestibular nystagmus were generated, and fitted to statistical distributions used in previous studies. The distributions did not depend on stimulation type (optokinetic or vestibular). An inverse Gaussian or a gamma distribution fitted the data better than did a reciprocal Gaussian distribution, but none fitted the data especially well. In some cases, however, the interpretation of these distributions is more physiologically satisfactory than in others. Recommendations are made on which class of models is preferred, and the experiments needed to support the particular models. Our results call into question the validity of previous studies that fit statistical distributions to data sets of a size comparable to ours. Received: 26 June 2001 / Accepted in revised form: 20 February 2002