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.     

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.     

Motion detection in the presence and absence of background motion in anAnolis lizard

Anolis lizards respond to a moving object viewed in the periphery of their visual field by turning their eye to fixate the object with their central fovea. This paper describes the relative effectiveness of different patterns of motion of a small black lure in eliciting these eye movements and the way motion of a backdrop of vegetation affects the response. The stimulus was positioned 45 degrees from the animal's line of gaze and oscillated in the vertical axis at different frequencies between 0.5 and 10 Hz. At each frequency, the amplitude of the oscillation was increased until the lizard flicked its eye towards the stimulus. The minimum amplitude needed for response (0.22 degrees of visual angle) was independent of frequency and waveform. The probability of any response occurring was, however, lower at higher frequencies (7 and 10 Hz) and a 1.5 Hz square wave evoked the greatest proportion of responses. Sinusoidal oscillation of a background of vegetation at 1.6 Hz during or before motion of the stimulus lure reduced the probability of an eye flick but did not raise the minimum amplitude needed for a response. The suppressive effect was greatest when the lure was oscillated at frequencies close to that of the background. It is concluded that Anolis, which rely upon motion to detect objects in the periphery of the visual field, filter out irrelevant motion such as that of windblown vegetation by responding preferentially to particular patterns of motion and short term habituation to commonly present patterns of motion.     

Effects of Attention to Auditory Motion on Cortical Activations during Smooth Pursuit Eye Tracking

Background

In contrast to traditional views that consider smooth pursuit as a relatively automatic process, evidence has been reported for the importance of attention for accurate pursuit performance. However, the exact role that attention might play in the maintenance of pursuit remains unclear.

Methodology/Principal Findings

We analysed the neuronal activity associated with healthy subjects executing smooth pursuit eye movements (SPEM) during concurrent attentive tracking of a moving sound source, which was either in-phase or in antiphase to the executed eye movements. Assuming that attentional resources must be allocated to the moving sound source, the simultaneous execution of SPEM and auditory tracking in diverging directions should result in increased load on common attentional resources. By using an auditory stimulus as a distractor rather then a visual stimulus we guaranteed that cortical activity cannot be caused by conflicts between two simultaneous visual motion stimuli. Our results revealed that the smooth pursuit task with divided attention led to significantly higher activations bilaterally in the posterior parietal cortex and lateral and medial frontal cortex, presumably containing the parietal, frontal and supplementary eye fields respectively.

Conclusions

The additional cortical activation in these areas is apparently due to the process of dividing attention between the execution of SPEM and the covert tracking of the auditory target. On the other hand, even though attention had to be divided the attentional resources did not seem to be exhausted, since the identification of the direction of the auditory target and the quality of SPEM were unaffected by the congruence between visual and auditory motion stimuli. Finally, we found that this form of task-related attention modulated not only the cortical pursuit network in general but also affected modality specific and supramodal attention regions.     

Frame of reference transformations in motion perception during smooth pursuit eye movements

Smooth pursuit eye movements change the retinal image velocity of objects in the visual field. In order to change from a retinocentric frame of reference into a head-centric one, the visual system has to take the eye movements into account. Studies on motion perception during smooth pursuit eye movements have measured either perceived speed or perceived direction during smooth pursuit to investigate this frame of reference transformation, but never both at the same time. We devised a new velocity matching task, in which participants matched both perceived speed and direction during fixation to that during pursuit. In Experiment 1, the velocity matches were determined for a range of stimulus directions, with the head-centric stimulus speed kept constant. In Experiment 2, the retinal stimulus speed was kept approximately constant, with the same range of stimulus directions. In both experiments, the velocity matches for all directions were shifted against the pursuit direction, suggesting an incomplete transformation of the frame of reference. The degree of compensation was approximately constant across stimulus direction. We fitted the classical linear model, the model of Turano and Massof (2001) and that of Freeman (2001) to the velocity matches. The model of Turano and Massof fitted the velocity matches best, but the differences between de model fits were quite small. Evaluation of the models and comparison to a few alternatives suggests that further specification of the potential effect of retinal image characteristics on the eye movement signal is needed.     

Negative Potentials of the Human Brain Elicited in Saccadic Latency during Stimulation of the Leading and Nonleading Eyes with an Overlap

Fast presaccadic EEG potentials in saccadic latency were studied with the use of inverse averaging during monocular stimulation of the leading or nonleading eye. Two paradigms were followed, with presentation of visual stimuli consecutively or with a 200-ms overlap. Irrespective of the paradigm and the stimulated eye, the negative N ^–1 potential in the interval of 50–20 ms preceding the beginning of the saccade predominated in the hemisphere contralateral to the saccade direction, reflecting the command processes of saccadic initiation. The N ^–2 potential was more pronounced in the case of direct averaging, starting from the stimulus. Its amplitude increased with increasing concentration of attention on the fixation stimulus under the overlap conditions, and its foci predominated in the left hemisphere, in the frontal, central, and parietosagittal regions. Hence, the N ^–2 potential was assumed to reflect spatial perception and attention as initial stages of saccadic programming. The findings testify to the priority of the leading eye both in fixation and in spatial attention.     

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.     

Spatial updating in human parietal cortex

Single neurons in monkey parietal cortex update visual information in conjunction with eye movements. This remapping of stimulus representations is thought to contribute to spatial constancy. We hypothesized that a similar process occurs in human parietal cortex and that we could visualize it with functional MRI. We scanned subjects during a task that involved remapping of visual signals across hemifields. We observed an initial response in the hemisphere contralateral to the visual stimulus, followed by a remapped response in the hemisphere ipsilateral to the stimulus. We ruled out the possibility that this remapped response resulted from either eye movements or visual stimuli alone. Our results demonstrate that updating of visual information occurs in human parietal cortex.     

A Method to Quantify Visual Information Processing in Children Using Eye Tracking

Visual problems that occur early in life can have major impact on a child''s development. Without verbal communication and only based on observational methods, it is difficult to make a quantitative assessment of a child''s visual problems. This limits accurate diagnostics in children under the age of 4 years and in children with intellectual disabilities. Here we describe a quantitative method that overcomes these problems. The method uses a remote eye tracker and a four choice preferential looking paradigm to measure eye movement responses to different visual stimuli. The child sits without head support in front of a monitor with integrated infrared cameras. In one of four monitor quadrants a visual stimulus is presented. Each stimulus has a specific visual modality with respect to the background, e.g., form, motion, contrast or color. From the reflexive eye movement responses to these specific visual modalities, output parameters such as reaction times, fixation accuracy and fixation duration are calculated to quantify a child''s viewing behavior. With this approach, the quality of visual information processing can be assessed without the use of communication. By comparing results with reference values obtained in typically developing children from 0-12 years, the method provides a characterization of visual information processing in visually impaired children. The quantitative information provided by this method can be advantageous for the field of clinical visual assessment and rehabilitation in multiple ways. The parameter values provide a good basis to: (i) characterize early visual capacities and consequently to enable early interventions; (ii) compare risk groups and follow visual development over time; and (iii), construct an individual visual profile for each child.     

The influence of structured visual backgrounds on smooth-pursuit initiation,steady-state pursuit and smooth-pursuit termination

 Smooth-pursuit eye movements were recorded in two rhesus monkeys in order to compare the influence of structured visual backgrounds on smooth-pursuit initiation, steady-state pursuit and pursuit termination. Different target trajectories were used in order to study smooth-pursuit initiation and termination. The influence of visual backgrounds on pursuit initiation was characterized by recording ocular responses elicited by step-ramp target displacements starting from straight ahead. Pursuit termination was characterized by analysing the transition from steady-state smooth-pursuit to fixation when a centripetally directed target ramp was terminated by a small target step in the direction of the ramp as soon as the target had come close to the straightahead position. The quantification of steady-state pursuit was based on ocular responses elicited by either paradigm. In accordance with previous work, we found that the onset of smooth-pursuit eye movements was delayed and initial eye acceleration reduced in the presence of a structured visual background. Likewise, mean eye velocity during steady-state pursuit was reduced by structured visual backgrounds. However, neither the latency nor the time course of smooth-pursuit termination was altered when the homogeneous background was replaced by a structured visual background. The lack of sensitivity of pursuit termination to the presence of visual structured backgrounds supports a previous contention that pursuit termination is mediated by a process which is different from the ones mediating smooth-pursuit initiation and steady-state pursuit. The absence of any noticeable effect of structured backgrounds on pursuit termination suggests that at least the fast component of the optokinetic reflex is suppressed during pursuit termination. Received: 24 October 1994/Accepted in revised form: 16 December 1994     

Modality and intermittency effects on time estimation

The modality of a stimulus and its intermittency affect time estimation. The present experiment explores the effect of a combination of modality and intermittency, and its implications for internal clock explanations. Twenty-four participants were tested on a temporal bisection task with durations of 200-800 ms. Durations were signaled by visual steady stimuli, auditory steady stimuli, visual flickering stimuli, and auditory clicks. Psychophysical functions and bisection points indicated that the durations of visual steady stimuli were classified as shorter and more variable than the durations signaled by the auditory stimuli (steady and clicks), and that the durations of the visual flickering stimuli were classified as longer than the durations signaled by the auditory stimuli (steady and clicks). An interpretation of the results is that there are different speeds for the internal clock, which are mediated by the perceptual features of the stimuli timed, such as differences in time of processing.     

Anteroposterior dynamic balance reactions induced by circular translation of the visual field

The anteroposterior sway of subjects under conditions of spontaneous dynamic balance on a wobbly platform was measured during visual stimulation by a visual target executing a circular trajectory in the frontal plane. The target was either a component of the whole moving visual scene or moving on a stationary background. With the former stimulation, obtained through the use of rotating prismatic glasses, every point of the visual field appeared to describe a circular trajectory around its real position so that the whole visual field apeared to be circularly translated, undistorted, inducing a binocular pursuit movement. Under these conditions, stereotyped anteroposterior dynamic balance reactions synchronous with the position of the stimulus were elicited. The latter stimulation consisted of pursuing a luminous target describing a trajectory similar to that of the fixation point seen through the rotating prisms on the same, this time stable, visual background. Although pursuit eye movements were comparable, as demonstrated by electro-oculographic recordings, no stereotyped equilibration reaction was induced. It is concluded that the translatory motion of the background image on the retina in the latter experiments contributed to the body's stability as well as to the perception of a stable environment.     

OMR-Arena: Automated Measurement and Stimulation System to Determine Mouse Visual Thresholds Based on Optomotor Responses

Measurement of the optomotor response is a common way to determine thresholds of the visual system in animals. Particularly in mice, it is frequently used to characterize the visual performance of different genetically modified strains or to test the effect of various drugs on visual performance. Several methods have been developed to facilitate the presentation of stimuli using computer screens or projectors. Common methods are either based on the measurement of eye movement during optokinetic reflex behavior or rely on the measurement of head and/or body-movements during optomotor responses. Eye-movements can easily and objectively be quantified, but their measurement requires invasive fixation of the animals. Head movements can be observed in freely moving animals, but until now depended on the judgment of a human observer who reported the counted tracking movements of the animal during an experiment. In this study we present a novel measurement and stimulation system based on open source building plans and software. This system presents appropriate 360 stimuli while simultaneously video-tracking the animal''s head-movements without fixation. The on-line determined head gaze is used to adjust the stimulus to the head position, as well as to automatically calculate visual acuity. Exemplary, we show that automatically measured visual response curves of mice match the results obtained by a human observer very well. The spatial acuity thresholds yielded by the automatic analysis are also consistent with the human observer approach and with published results. Hence, OMR-arena provides an affordable, convenient and objective way to measure mouse visual performance.     

Signaling without the risk of illegitimate receivers: do predators respond to the acoustic signals of <Emphasis Type="Italic">Cyprinella</Emphasis> (Cyprinidae)?

Acoustic and visual signals are commonly used by fishes for communication. A significant drawback to both types of signals is that both sounds and visual stimuli are easily detected by illegitimate receivers, such as predators. Although predator attraction to visual stimuli has been well-studied in other animals, predator response to acoustic stimuli has received virtually no research attention among fishes and snakes. This study assessed whether the calls of male tricolor shiner (Cyprinella trichroistia) made during the breeding season would attract potential predators. We also examined the effect of visual stimulus of tricolor shiners on predators. Predators used were red eye bass (Micropterus coosae) and midland water snakes (Nerodia sipedon pleuralis). Neither predator was attracted to tricolor sounds when presented alone. Micropterus coosae responded significantly more to a visual stimulus, and to a combination of visual and acoustic stimuli, but with no greater intensity in the latter. Nerodia sipedon pleuralis did not responded to visual stimulus presented alone, but did respond to visual and acoustic stimuli presented simultaneously, and with greater intensity to the latter, indicating that acoustic signals may play a role in prey detection by N. sipedon pleuralis.     

Visual-manual tracking and vestibular function during a seven-day dry immersion

A seven-day dry immersion experiment provided the opportunity to study the effects of decreased proprioceptive tactile and support afferentations on the vestibular function and visual-manual tracking. Before and after immersion, six subjects participated in a video oculographic evaluation of the static torsion otolith-cervicoocular reflex (OCOR) in response to head tilt by 30° in the frontal plane and dynamic vestibular-cervicoocular reactions to head longitudinal rotations at 0.125 Hz. In addition, the hand-eye motor coordination of tracking a jerky (sinusoidal) or smooth (linear) movement of point targets along the horizontal or vertical lines was evaluated on the basis of the data of electrooculography and records of manipulations with the joystick during immersion. A computerized test was performed in virtual glasses displaying images of visual stimuli and hand motor acts. The computed parameters included the reaction’s latent time, amplitude, speed and time of eye and hand movements, and gains of optooculomotor reactions and manual tracking as a ratio of eye/hand to visual stimulus speed. Testing was carried out before the experiment, after 3 h of immersion, on days 3 and 6 of staying in the bath, in the initial hours after immersion and on the third day of recovery. It was shown that removal of support and minimization of proprioceptive afferentation had a profound effect on the ocular tracking rather than pursuing the visual stimulus by hand. The accuracy of manual tracking was better in comparison with the eye tracking in all subjects. This was the first observation of changes in the peripheral vestibular system in two out of six subjects, i.e., inversion of the static torsion OCOP and positional nystagmus against a background of converted reflex, which did not change the parameters of the visual-manual tracking.     

Slow Cortical Potentials Preceeding Visually Guided Saccades in Schizophrenics

The parameters of saccades and presaccadic slow potentials were studied in right-handed men with a dominant right eye, including 19 schizophrenics and 12 healthy subjects. For visual stimulation, three light-emitting diodes were used, which were located in the center of the visual field (the central fixation stimulus) and 10° to the right and left of it (peripheral stimuli). Two stimulation protocols were used: with a simultaneous switching off of the central fixation stimulus and switching on of the peripheral stimuli (test 1) and with an interstimulus gap of 200 ms (test 2). According to the latency, saccades were divided into anticipatory, express, and regular. Slow EEG potentials preceding regular saccades were analyzed. It was found that the proportion of anticipatory saccades is considerably higher than the normal value in schizophrenia. The analysis of the presaccadic potentials demonstrated a significant decrease in the amplitude of negative potentials in the vertex region at early stages of presaccadic preparation and its increase in the occipital region at late stages. Test 2 in the patients demonstrated an increase in the positivity focus in the frontal region of the right hemisphere. It was assumed that the alterations found in schizophrenia result from the deficit of frontal cortical fields.     

The role of background movement in goldfish vision

In experiments described in the literature objects presented to restrained goldfish failed to induce eye movements like fixation and/or tracking. We show here that eye movements can be induced only if the background (visual surround) is not stationary relative to the fish but moving. We investigated the influence of background motion on eye movements in the range of angular velocities of 5–20° s⁻¹. The response to presentation of an object is a transient shift in mean horizontal eye position which lasts for some 10 s. If an object is presented in front of the fish the eyes move in a direction such that it is seen more or less symmetrically by both eyes. If it is presented at ±70° from the fish's long axis the eye on the side of the object moves in the direction that the object falls more centrally on its retina. During these object induced eye responses the typical optokinetic nystagmus of amplitude of some 5° with alternating fast and slow phases is maintained, and the eye velocity during the slow phase is not modified by presentation of the object. Presenting an object in front of stationary or moving backgrounds leads to transient suppression of respiration which shows habituation to repeated object presentations. Accepted: 14 April 2000     

Paradoxical Interaction between Ocular Activity,Perception, and Decision Confidence at the Threshold of Vision

In humans and some other species perceptual decision-making is complemented by the ability to make confidence judgements about the certainty of sensory evidence. While both forms of decision process have been studied empirically, the precise relationship between them remains poorly understood. We performed an experiment that combined a perceptual decision-making task (identifying the category of a faint visual stimulus) with a confidence-judgement task (wagering on the accuracy of each perceptual decision). The visual stimulation paradigm required steady fixation, so we used eye-tracking to control for stray eye movements. Our data analyses revealed an unexpected and counterintuitive interaction between the steadiness of fixation (prior to and during stimulation), perceptual decision making, and post-decision wagering: greater variability in gaze direction during fixation was associated with significantly increased visual-perceptual sensitivity, but significantly decreased reliability of confidence judgements. The latter effect could not be explained by a simple change in overall confidence (i.e. a criterion artifact), but rather was tied to a change in the degree to which high wagers predicted correct decisions (i.e. the sensitivity of the confidence judgement). We found no evidence of a differential change in pupil diameter that could account for the effect and thus our results are consistent with fixational eye movements being the relevant covariate. However, we note that small changes in pupil diameter can sometimes cause artefactual fluctuations in measured gaze direction and this possibility could not be fully ruled out. In either case, our results suggest that perceptual decisions and confidence judgements can be processed independently and point toward a new avenue of research into the relationship between them.     

Influence of Retinal Image Shifts and Extra-Retinal Eye Movement Signals on Binocular Rivalry Alternations

Previous studies have indicated that saccadic eye movements correlate positively with perceptual alternations in binocular rivalry, presumably because the foveal image changes resulting from saccades, rather than the eye movement themselves, cause switches in awareness. Recently, however, we found evidence that retinal image shifts elicit so-called onset rivalry and not percept switches as such. These findings raise the interesting question whether onset rivalry may account for correlations between saccades and percept switches.We therefore studied binocular rivalry when subjects made eye movements across a visual stimulus and compared it with the rivalry in a ‘replay’ condition in which subjects maintained fixation while the same retinal displacements were reproduced by stimulus displacements on the screen. We used dichoptic random-dot motion stimuli viewed through a stereoscope, and measured eye and eyelid movements with scleral search-coils.Positive correlations between retinal image shifts and perceptual switches were observed for both saccades and stimulus jumps, but only for switches towards the subjects'' preferred eye at stimulus onset. A similar asymmetry was observed for blink-induced stimulus interruptions. Moreover, for saccades, amplitude appeared crucial as the positive correlation persisted for small stimulus jumps, but not for small saccades (amplitudes < 1°). These findings corroborate our tenet that saccades elicit a form of onset rivalry, and that rivalry is modulated by extra-retinal eye movement signals.     

Binocular coordination of the eyes during reading

Saccadic eye movements and fixations are the behavioral means by which we visually sample text during reading. Human oculomotor control is governed by a complex neurophysiological system involving the brain stem, superior colliculus, and several cortical areas. A very widely held belief among researchers investigating primate vision is that the oculomotor system serves to orient the visual axes of both eyes to fixate the same target point in space. It is argued that such precise positioning of the eyes is necessary to place images on corresponding retinal locations, such that on each fixation a single, nondiplopic, visual representation is perceived. Vision works actively through a continual sampling process involving saccades and fixations. Here we report that during normal reading, the eyes do not always fixate the same letter within a word. We also demonstrate that saccadic targeting is yoked and based on a unified cyclopean percept of a whole word since it is unaffected if different word parts are delivered exclusively to each eye via a dichoptic presentation technique. These two findings together suggest that the visual signal from each eye is fused at a very early stage in the visual pathway, even when the fixation disparity is greater than one character (0.29 deg), and that saccade metrics for each eye are computed on the basis of that fused signal.