Population coding of saccadic eye movements by neurons in the superior colliculus

The deeper layers of the superior colliculus are involved in the initiation and execution of saccadic (high velocity) eye movements. A large population of coarsely tuned collicular neurons is active before each saccade. The mechanisms by which the signals that precisely control the direction and amplitude of a saccade are extracted from the activity of the population are unknown. It has been assumed that the exact trajectory of a saccade is determined by the activity of the entire population and that information is not extracted from only the most active cells in the population at a subsequent stage of neural processing. The trajectory of a saccade could be based on vector summation of the movement tendencies provided by each member of the population of active neurons or be determined by a weighted average of the vector contributions of each neuron in the active population. Here we present the results of experiments in which a small subset of the active population was reversibly deactivated with lidocaine. These results are consistent with the predictions of the latter population-averaging hypothesis and support the general idea that the direction, amplitude and velocity of saccadic eye movements are based on the responses of the entire population of cells active before a saccadic eye movement.     

Influence of the thalamus on spatial visual processing in frontal cortex

Each of our movements activates our own sensory receptors, and therefore keeping track of self-movement is a necessary part of analysing sensory input. One way in which the brain keeps track of self-movement is by monitoring an internal copy, or corollary discharge, of motor commands. This concept could explain why we perceive a stable visual world despite our frequent quick, or saccadic, eye movements: corollary discharge about each saccade would permit the visual system to ignore saccade-induced visual changes. The critical missing link has been the connection between corollary discharge and visual processing. Here we show that such a link is formed by a corollary discharge from the thalamus that targets the frontal cortex. In the thalamus, neurons in the mediodorsal nucleus relay a corollary discharge of saccades from the midbrain superior colliculus to the cortical frontal eye field. In the frontal eye field, neurons use corollary discharge to shift their visual receptive fields spatially before saccades. We tested the hypothesis that these two components-a pathway for corollary discharge and neurons with shifting receptive fields-form a circuit in which the corollary discharge drives the shift. First we showed that the known spatial and temporal properties of the corollary discharge predict the dynamic changes in spatial visual processing of cortical neurons when saccades are made. Then we moved from this correlation to causation by isolating single cortical neurons and showing that their spatial visual processing is impaired when corollary discharge from the thalamus is interrupted. Thus the visual processing of frontal neurons is spatiotemporally matched with, and functionally dependent on, corollary discharge input from the thalamus. These experiments establish the first link between corollary discharge and visual processing, delineate a brain circuit that is well suited for mediating visual stability, and provide a framework for studying corollary discharge in other sensory systems.     

Dynamic coding of behaviourally relevant stimuli in parietal cortex.

A general function of cerebral cortex is to allow the flexible association of sensory stimuli with specific behaviours. Many neurons in parietal, prefrontal and motor cortical areas are activated both by particular movements and by sensory cues that trigger these movements, suggesting a role in linking sensation to action. For example, neurons in the lateral intraparietal area (LIP) encode both the location of visual stimuli and the direction of saccadic eye movements. LIP is not believed to encode non-spatial stimulus attributes such as colour. Here we investigated whether LIP would encode colour if colour was behaviourally linked to the eye movement. We trained monkeys to make an eye movement in one of two directions based alternately on the colour or location of a visual cue. When cue colour was relevant for directing eye movement, we found a substantial fraction of LIP neurons selective for cue colour. However, when cue location was relevant, colour selectivity was virtually absent in LIP. These results demonstrate that selectivity of cortical neurons can change as a function of the required behaviour.     

Neuronal switching of sensorimotor transformations for antisaccades

The influence of cognitive context on orienting behaviour can be explored using the mixed memory-prosaccade, memory-antisaccade task. A symbolic cue, such as the colour of a visual stimulus, instructs the subject to make a brief, rapid eye movement (a saccade) either towards the stimulus (prosaccade) or in the opposite direction (antisaccade). Thus, the appropriate sensorimotor transformation must be switched on to execute the instructed task. Despite advances in our understanding of the neuronal processing of antisaccades, it remains unclear how the brain selects and computes the sensorimotor transformation leading to an antisaccade. Here we show that area LIP of the posterior parietal cortex is involved in these processes. LIP's population activity turns from the visual direction to the motor direction during memory-antisaccade trials. About one-third of the visual neurons in LIP produce a brisk, transient discharge in certain memory-antisaccade trials. We call this discharge 'paradoxical' because its timing is visual-like but its direction is motor. The paradoxical discharge shows, first, that switching occurs already at the level of visual cells, as previously proposed by Schlag-Rey and colleagues; and second, that this switching is accomplished very rapidly, within 50 ms from the arrival of the visual signals in LIP.     

Selective gating of visual signals by microstimulation of frontal cortex

Several decades of psychophysical and neurophysiological studies have established that visual signals are enhanced at the locus of attention. What remains a mystery is the mechanism that initiates biases in the strength of visual representations. Recent evidence argues that, during spatial attention, these biases reflect nascent saccadic eye movement commands. We examined the functional interaction of saccade preparation and visual coding by electrically stimulating sites within the frontal eye fields (FEF) and measuring its effect on the activity of neurons in extrastriate visual cortex. Here we show that visual responses in area V4 could be enhanced after brief stimulation of retinotopically corresponding sites within the FEF using currents below that needed to evoke saccades. The magnitude of the enhancement depended on the effectiveness of receptive field stimuli as well as on the presence of competing stimuli outside the receptive field. Stimulation of non-corresponding FEF representations could suppress V4 responses. The results suggest that the gain of visual signals is modified according to the strength of spatially corresponding eye movement commands.     

一种山区急弯路段驾驶人熟练度甄别方法

为探究驾驶人眼动行为与驾驶熟练程度以及道路线型之间的响应特性,设计并组织山区公路实车驾驶行为试验。招募20名驾驶人,实时采集被试驾驶人在急弯路段的6个注视及扫视行为表征参数。试验表明:眼睛注视点在左转急弯路段的水平方向分布范围是-0.5~0.1 m,在右转急弯路段的水平方向分布范围是-0.2~0.5 m;眼睛水平注视角变化的主要范围是0°~30°;扫视速度的变化范围区间是0~1(°)·ms~(-1),扫视幅度的变化范围是5°~25°。基于采集的眼动行为参数,构建驾驶人视觉搜索模态矩阵。采用主成分分析法对影响因子进行降维,并建立驾驶人眼动特征综合评价模型。结果显示,眼动综合评分与驾驶里程呈正相关关系,表明该模型可用于量化甄别驾驶人驾驶熟练程度,并为驾驶能力评估提供有效的理论依据。     

Coding of smooth eye movements in three-dimensional space by frontal cortex

Through the development of a high-acuity fovea, primates with frontal eyes have acquired the ability to use binocular eye movements to track small objects moving in space. The smooth-pursuit system moves both eyes in the same direction to track movement in the frontal plane (frontal pursuit), whereas the vergence system moves left and right eyes in opposite directions to track targets moving towards or away from the observer (vergence tracking). In the cerebral cortex and brainstem, signals related to vergence eye movements--and the retinal disparity and blur signals that elicit them--are coded independently of signals related to frontal pursuit. Here we show that these types of signal are represented in a completely different way in the smooth-pursuit region of the frontal eye fields. Neurons of the frontal eye field modulate strongly during both frontal pursuit and vergence tracking, which results in three-dimensional cartesian representations of eye movements. We propose that the brain creates this distinctly different intermediate representation to allow these neurons to function as part of a system that enables primates to track and manipulate objects moving in three-dimensional space.     

Optimal eye movement strategies in visual search

To perform visual search, humans, like many mammals, encode a large field of view with retinas having variable spatial resolution, and then use high-speed eye movements to direct the highest-resolution region, the fovea, towards potential target locations. Good search performance is essential for survival, and hence mammals may have evolved efficient strategies for selecting fixation locations. Here we address two questions: what are the optimal eye movement strategies for a foveated visual system faced with the problem of finding a target in a cluttered environment, and do humans employ optimal eye movement strategies during a search? We derive the ideal bayesian observer for search tasks in which a target is embedded at an unknown location within a random background that has the spectral characteristics of natural scenes. Our ideal searcher uses precise knowledge about the statistics of the scenes in which the target is embedded, and about its own visual system, to make eye movements that gain the most information about target location. We find that humans achieve nearly optimal search performance, even though humans integrate information poorly across fixations. Analysis of the ideal searcher reveals that there is little benefit from perfect integration across fixations--much more important is efficient processing of information on each fixation. Apparently, evolution has exploited this fact to achieve efficient eye movement strategies with minimal neural resources devoted to memory.     

Predictable eye-head coordination during driving.

Large changes in the direction of gaze are made with a combination of fast saccadic eye movements and rather slower head movements. Since the first study on freely moving subjects, most authors have agreed that the head movement component of gaze is very variable, with a high 'volitional' component. But in some circumstances head and eye movements can be quite predictable, for example when a subject is asked to shift gaze as quickly as possible. Under these conditions, laboratory studies have shown that the eye and head motor-systems both receive gaze-change commands, although they execute them in rather different ways. Here I reconsider the way gaze direction is changed during free movement, but in the performance of a task where the subject is too busy to exert conscious control over head or eye movements. Using a new portable and inexpensive method for recording head and eye movements, I examine the oculomotor behaviour of car drivers, particularly during the large gaze changes made at road junctions. The results show that the pattern of eye and head movements is highly predictable, given only the sequence of gaze targets.     

Miniature eye movements enhance fine spatial detail

Our eyes are constantly in motion. Even during visual fixation, small eye movements continually jitter the location of gaze. It is known that visual percepts tend to fade when retinal image motion is eliminated in the laboratory. However, it has long been debated whether, during natural viewing, fixational eye movements have functions in addition to preventing the visual scene from fading. In this study, we analysed the influence in humans of fixational eye movements on the discrimination of gratings masked by noise that has a power spectrum similar to that of natural images. Using a new method of retinal image stabilization, we selectively eliminated the motion of the retinal image that normally occurs during the intersaccadic intervals of visual fixation. Here we show that fixational eye movements improve discrimination of high spatial frequency stimuli, but not of low spatial frequency stimuli. This improvement originates from the temporal modulations introduced by fixational eye movements in the visual input to the retina, which emphasize the high spatial frequency harmonics of the stimulus. In a natural visual world dominated by low spatial frequencies, fixational eye movements appear to constitute an effective sampling strategy by which the visual system enhances the processing of spatial detail.     

Representation of a perceptual decision in developing oculomotor commands

Behaviour often depends on the ability to make categorical judgements about sensory information acquired over time. Such judgements require a comparison of the evidence favouring the alternatives, but how the brain forms these comparisons is unknown. Here we show that in a visual discrimination task, the accumulating balance of sensory evidence favouring one interpretation over another is evident in the neural circuits that generate the behavioural response. We trained monkeys to make a direction judgement about dynamic random-dot motions and to indicate their judgement with an eye movement to a visual target. We interrupted motion viewing with electrical microstimulation of the frontal eye field and analysed the resulting, evoked eye movements for evidence of ongoing activity associated with the oculomotor response. Evoked eye movements deviated in the direction of the monkey's judgement. The magnitude of the deviation depended on motion strength and viewing time. The oculomotor signals responsible for these deviations reflected the accumulated motion information that informed the monkey's choices on the discrimination task. Thus, for this task, decision formation and motor preparation appear to share a common level of neural organization.     

Illusory shifts in visual direction accompany adaptation of saccadic eye movements.

A central problem in human vision is to explain how the visual world remains stable despite the continual displacements of the retinal image produced by rapid saccadic movements of the eyes. Perceived stability has been attributed to 'efferent-copy' signals, representing the saccadic motor commands, that cancel the effects of saccade-related retinal displacements. Here we show, by means of a perceptual illusion, that traditional cancellation theories cannot explain stability. The perceptual illusion was produced by first inducing adaptive changes in saccadic gain (ratio of saccade size to target eccentricity). Following adaptation, subjects experienced an illusory mislocalization in which widely separated targets flashed before and after saccades appeared to be in the same place. The illusion shows that the perceptual system did not take the adaptive changes into account. Perceptual localization is based on signals representing the size of the initially-intended saccade, not the size of the saccade that is ultimately executed. Signals representing intended saccades initiate a visual comparison process used to maintain perceptual stability across saccades and to generate the oculomotor error signals that ensure saccadic accuracy.     

Developmental plasticity in the visual and auditory representations in the mammalian superior colliculus

Environmental factors play an important role in certain aspects of the development of sensory systems. But the way in which the maturation of different sensory modalities is coordinated is poorly understood. We have investigated this question neurophysiologically in the mammalian superior colliculus (SC), which contains topographically aligned maps of visual and auditory space. We report here that an essentially normal auditory map, in approximate register with the visual map, is found in the SC of adult ferrets reared with abnormal binaural localization cues. Also, if, early in life, one eye is deviated laterally, there is a compensatory shift in the auditory map, but early eye rotation totally disorders the auditory representation. These results imply that development of the auditory map is affected by visual activity or by information about eye position and that there is definite, but limited, capacity for the auditory map to reorganize so that it remains aligned with the visual map.     

草原公路直线段路侧景观对驾驶员视觉特性的影响

 视觉系统是驾驶员获取行车信息的主要通道,而公路路侧景观是引起驾驶员视觉刺激的重要因素之一。以不同路侧景观的草原公路直线段作为研究对象,利用眼动仪采集5名驾驶员的眼动指标并进行分析。结果表明,驾驶员在景观相对复杂路段的瞳孔直径和扫视幅度较大,眨眼持续时间与注视持续时间较小;不同路侧景观对驾驶员的眨眼持续时间、注视持续时间、扫视幅度影响不显著;对驾驶员的瞳孔直径影响显著。本研究可为分析草原公路路侧景观对驾驶员疲劳的影响提供参考。     

A relative signalling model for the formation of a topographic neural map

The highly ordered wiring of retinal ganglion cell (RGC) neurons in the eye to their synaptic targets in the superior colliculus of the midbrain has long served as the dominant experimental system for the analysis of topographic neural maps. Here we describe a quantitative model for the development of one arm of this map--the wiring of the nasal-temporal axis of the retina to the caudal-rostral axis of the superior colliculus. The model is based on RGC-RGC competition that is governed by comparisons of EphA receptor signalling intensity, which are made using ratios of, rather than absolute differences in, EphA signalling between RGCs. Molecular genetic experiments, exploiting a combinatorial series of EphA receptor knock-in and knockout mice, confirm the salient predictions of the model, and show that it both describes and predicts topographic mapping.     

Postsaccadic visual references generate presaccadic compression of space

With every rapid gaze shift (saccade), our eyes experience a different view of the world. Stable perception of visual space requires that points in the new image are associated with corresponding points in the previous image. The brain may use an extraretinal eye position signal to compensate for gaze changes, or, alternatively, exploit the image contents to determine associated locations. Support for a uniform extraretinal signal comes from findings that the apparent position of objects briefly flashed around the time of a saccade is often shifted in the direction of the saccade. This view is challenged, however, by observations that the magnitude and direction of the displacement varies across the visual field. Led by the observation that non-uniform displacements typically occurred in studies conducted in slightly illuminated rooms, here we determine the dependence of perisaccadic mislocalization on the availability of visual spatial references at various times around a saccade. We find that presaccadic compression occurs only if visual references are available immediately after, rather than before or during, the saccade. Our findings indicate that the visual processes of transsaccadic spatial localization use mainly postsaccadic visual information.     

Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex

In studies of the neural mechanisms giving rise to behaviour, changes in the neural and behavioural responses produced by a given stimulus have been widely reported. This 'gain control' can boost the responses to sensory inputs that are particularly relevant, select among reflexes for execution by motoneurons or emphasize specific movement targets. Gain control is also an integral part of the smooth-pursuit eye movement system. One signature of gain control is that a brief perturbation of a stationary target during fixation causes tiny eye movements, whereas the same perturbation of a moving target during the active state of accurate pursuit causes large responses. Here we show that electrical stimulation of the smooth-pursuit eye movement region in the arcuate sulcus of the frontal lobe ('the frontal pursuit area', FPA) mimics the active state of pursuit. Such stimulation enhances the response to a brief perturbation of target motion, regardless of the direction of motion. We postulate that the FPA sets the gain of pursuit, thereby participating in target selection for pursuit.     

Visual discrimination of target displacement remains after damage to the striate cortex in humans

Damage to the striate cortex usually causes blindness in those regions of the visual field which map to the area of neural damage. Nonetheless, there are reports that some patients with such damage can localize and perform certain visual discriminations between light stimuli presented within the 'blind' area of the visual field. Experiments on animals with different brain areas ablated suggest that visual function is served by two principal projection pathways from the retina. That to the striate cortex is primarily responsible for fine discrimination between stimulus parameters such as colour and spatial pattern, whereas that to the superior colliculus in the midbrain is responsible for visual localization of stimuli. The residual visual functions in patients with cortical damage are usually attributed to the non-striate retinal projection to the superior colliculus. We now present measurements of spatial discrimination in two observers with large visual field defects (scotomata) caused by damage to the striate cortical region. Both exhibit a near normal ability to discriminate displacements of targets when two lights are flashed sequentially in their defective visual field, but they are unable to discriminate spatial pattern or size. We argue that these results are consistent with the 'two visual systems' interpretation of ablation studies on non-human species.     

Numerical representation for action in the parietal cortex of the monkey

The anterior part of the parietal association area in the cerebral cortex of primates has been implicated in the integration of somatosensory signals, which generate neural images of body parts and apposed objects and provide signals for sensorial guidance of movements. Here we show that this area is active in primates performing numerically based behavioural tasks. We required monkeys to select and perform movement A five times, switch to movement B for five repetitions, and return to movement A, in a cyclical fashion. Cellular activity in the superior parietal lobule reflected the number of self-movement executions. For the most part, the number-selective activity was also specific for the type of movement. This type of numerical representation of self-action was seen less often in the inferior parietal lobule, and rarely in the primary somatosensory cortex. Such activity in the superior parietal lobule is useful for processing numerical information, which is necessary to provide a foundation for the forthcoming motor selection.     

不同抑制能力大学生图形推理的眼动特征

对160名大学生被试进行6个执行功能任务的测量,从中筛选出高抑制能力和低抑制能力被试各15人,考察被试在不同难易程度图形推理题目上的得分、反应时以及眼动模式的差别.研究发现抑制能力与推理得分之间的相关并不显著,但低抑制能力的被试注视频率显著高于高抑制能力的被试,而平均注视时间则显著低于,另外低抑制能力组倾向于采用选项剔除策略,而高抑制能力组倾向于采用规则构建策略.