Video-game play and non-symbolic numerical comparison.

Visual display was used by Stäb and Ilg to examine the abilities of video-game players and non-players to determine simple mathematical abilities.

The effect of age and gender on anti-saccade performance: Results from a large cohort of healthy aging individuals.

By 2050, the global population of people aged 65 years or older will triple. While this is accompanied with an increasing burden of age-associated diseases, it also emphasizes the need to understand the effects of healthy aging on cognitive processes. One such effect is a general slowing of processing speed, which is well documented in many domains. The execution of anti-saccades depends on a well-established brain-wide network ranging from various cortical areas and basal ganglia through the superior colliculus down to the brainstem saccade generators. To clarify the consequences of healthy aging as well as gender on the execution of reflexive and voluntary saccades, we measured a large sample of healthy, non-demented individuals (n = 731, aged 51-84 years) in the anti-saccade task. Age affected various aspects of saccade performance: The number of valid trials decreased with age. Error rate, saccadic reaction times (SRTs), and variability in saccade accuracy increased with age, whereas anti-saccade costs, accuracy, and peak velocity of anti-saccades and direction errors were not affected by age. Gender affected SRTs independent of age and saccade type with male participants having overall shorter SRTs. Our rigid and solid statistical testing using linear mixed-effect models provide evidence for a uniform slowing of processing speed independent of the actually performed eye movement. Our data do not support the assumption of a specific deterioration of frontal lobe functions with aging.

Video game players show higher performance but no difference in speed of attention shifts.

Video games have become both a widespread leisure activity and a substantial field of research. In a variety of tasks, video game players (VGPs) perform better than non-video game players (NVGPs). This difference is most likely explained by an alteration of the basic mechanisms underlying visuospatial attention. More specifically, the present study hypothesizes that VGPs are able to shift attention faster than NVGPs. Such alterations in attention cannot be disentangled from changes in stimulus-response mappings in reaction time based measurements. Therefore, we used a spatial cueing task with varying cue lead times (CLTs) to investigate the speed of covert attention shifts of 98 male participants divided into 36 NVGPs and 62 VGPs based on their weekly gaming time. VGPs exhibited higher peak and mean performance than NVGPs. However, we did not find any differences in the speed of covert attention shifts as measured by the CLT needed to achieve peak performance. Thus, our results clearly rule out faster stimulus-response mappings as an explanation for the higher performance of VGPs in line with previous studies. More importantly, our data do not support the notion of faster attention shifts in VGPs as another possible explanation.

The effects of video game play on the characteristics of saccadic eye movements.

Video game play has become a common leisure activity all around the world. To reveal possible effects of playing video games, we measured saccades elicited by video game players (VGPs) and non-players (NVGPs) in two oculomotor tasks. First, our subjects performed a double-step task. Second, we asked our subjects to move their gaze opposite to the appearance of a visual target, i.e. to perform anti-saccades. As expected on the basis of previous studies, VGPs had significantly shorter saccadic reaction times (SRTs) than NVGPs for all saccade types. However, the error rates in the anti-saccade task did not reveal any significant differences. In fact, the error rates of VGPs were actually slightly lower compared to NVGPs (34% versus 40%, respectively). In addition, VGPs showed significantly higher saccadic peak velocities in every saccade type compared to NVGP. Our results suggest that faster SRTs in VGPs were associated with a more efficient motor drive for saccades. Taken together, our results are in excellent agreement with earlier reports of beneficial video game effects through the general reduction in SRTs. Our data clearly provides additional experimental evidence for an higher efficiency of the VGPs on the one hand and refutes the notion of a reduced impulse control in VGPs on the other.

Dissociation of reach-related and visual signals in the human superior colliculus.

Electrophysiological and micro-stimulation studies in non-human animal species indicated that the superior colliculus (SC) plays a role in the control of upper limb movements. In our previous work we found reach-related signals in the deep superior colliculus in humans. Here we show that also signals in more dorsal locations are correlated with the execution of arm movements. We instructed healthy participants to reach for visual targets either presented in the left or in the right visual hemifield during an fMRI measurement. Visual stimulation was dissociated from movement execution using a pro- and anti-reaching task. Thereby, we successfully differentiated between signals at these locations induced by the visual input of target presentations on the one hand and by the execution of arm movements on the other hand. Extending our previous report, the results of this study are in good agreement with the observed anatomical distribution of reach-related neurons in macaques. Obviously, reach-related signals can be found across a considerable depth range also in humans.

Visual stability and the motion aftereffect: a psychophysical study revealing spatial updating.

Eye movements create an ever-changing image of the world on the retina. In particular, frequent saccades call for a compensatory mechanism to transform the changing visual information into a stable percept. To this end, the brain presumably uses internal copies of motor commands. Electrophysiological recordings of visual neurons in the primate lateral intraparietal cortex, the frontal eye fields, and the superior colliculus suggest that the receptive fields (RFs) of special neurons shift towards their post-saccadic positions before the onset of a saccade. However, the perceptual consequences of these shifts remain controversial. We wanted to test in humans whether a remapping of motion adaptation occurs in visual perception.The motion aftereffect (MAE) occurs after viewing of a moving stimulus as an apparent movement to the opposite direction. We designed a saccade paradigm suitable for revealing pre-saccadic remapping of the MAE. Indeed, a transfer of motion adaptation from pre-saccadic to post-saccadic position could be observed when subjects prepared saccades. In the remapping condition, the strength of the MAE was comparable to the effect measured in a control condition (33±7% vs. 27±4%). Contrary, after a saccade or without saccade planning, the MAE was weak or absent when adaptation and test stimulus were located at different retinal locations, i.e. the effect was clearly retinotopic. Regarding visual cognition, our study reveals for the first time predictive remapping of the MAE but no spatiotopic transfer across saccades. Since the cortical sites involved in motion adaptation in primates are most likely the primary visual cortex and the middle temporal area (MT/V5) corresponding to human MT, our results suggest that pre-saccadic remapping extends to these areas, which have been associated with strict retinotopy and therefore with classical RF organization. The pre-saccadic transfer of visual features demonstrated here may be a crucial determinant for a stable percept despite saccades.

Influence of global motion onset on goal-directed eye movements.

Saccades are very rapid eye movements in between two phases of fixation, which offer a precise measure of behaviour for the direction of the spotlight of attention. The onset of global motion is known to attract our attention reflexively. We asked whether brief global motion stimuli are able to modify the execution of saccades. When participants performed visually guided saccades towards a target presented in front of a structured background, saccade latency was 174 ms on average and correctness of saccades was 100%. If the presentation of the target occurred at the same time as the onset of a brief global motion signal, then the saccade latency increased dramatically to 243 ms with a slight decrease in correctness to 89%. However, if the motion stimulus preceded the presentation of the target, then the latency decreased to 114 ms while the correctness dropped close to chance levels (62%).

The neural basis of smooth pursuit eye movements in the rhesus monkey brain.

Smooth pursuit eye movements are performed in order to prevent retinal image blur of a moving object. Rhesus monkeys are able to perform smooth pursuit eye movements quite similar as humans, even if the pursuit target does not consist in a simple moving dot. Therefore, the study of the neuronal responses as well as the consequences of micro-stimulation and lesions in trained monkeys performing smooth pursuit is a powerful approach to understand the human pursuit system. The processing of visual motion is achieved in the primary visual cortex and the middle temporal area. Further processing including the combination of retinal image motion signals with extra-retinal signals such as the ongoing eye and head movement occurs in subsequent cortical areas as the medial superior temporal area, the ventral intraparietal area and the frontal and supplementary eye field. The frontal eye field especially contributes anticipatory signals which have a substantial influence on the execution of smooth pursuit. All these cortical areas send information to the pontine nuclei, which in turn provide the input to the cerebellum. The cerebellum contains two pursuit representations: in the paraflocculus/flocculus region and in the posterior vermis. While the first representation is most likely involved in the coordination of pursuit and the vestibular-ocular reflex, the latter is involved in the precise adjustments of the eye movements such as adaptation of pursuit initiation. The output of the cerebellum is directed to the moto-neurons of the extra-ocular muscles in the brainstem.

The role of areas MT and MST in coding of visual motion underlying the execution of smooth pursuit.

What is the main purpose of visual motion processing? One very important aspect of motion processing is definitively the generation of smooth pursuit eye movements. These eye movements avoid motion blur of moving objects which would obstruct the analysis of the objects' visual details. However, these eye movements can only be executed if there is a moving target. So there is a very close and inseparable relationship between smooth pursuit and motion processing. The hub for visual motion processing is situated in the middle temporal (MT) and medial superior temporal (MST) area. Despite the undoubted importance of these areas for the generation of smooth pursuit or goal-directed behavior in general, it is important to keep in mind that motion processing in addition serves perceptual purposes such as object recognition, structure-from-motion detection, scene segmentation, self-motion estimation and depth perception. This review focuses at the beginning on pursuit-related activity recorded from MT and MST, subsequently extends the view to goal-directed hand movements, and finally addresses the possible contributions of these areas to motion perception.

Initiation of smooth-pursuit eye movements by real and illusory contours.

It is well established that elementary motion detectors are only able to code for the movement of a contour perpendicular to its orientation. This shortcoming explains why the initial direction of smooth-pursuit eye movements is directed orthogonal to the orientation of a moving contour independent of its veridical direction of motion. Here, we replicated this finding and asked whether this directional error can be reduced by subjects' prediction of upcoming target moving direction and whether this directional error also occurs during tracking of an illusory contour. Our results show that prediction did not abolish the directional error, it was only slightly reduced. On the other hand, the directional error was considerably diminished during pursuit initiation towards illusory contours and most likely reflected the amount of real stimulation defining the specific illusory contour. We conclude that pursuit initiation is driven by raw retinal image motion signals, which are not yet processed for figure completion.

Anticipatory smooth-pursuit eye movements in man and monkey.

A fundamental problem in the generation of goal-directed behaviour is caused by the inevitable latency of biological sensory systems. Behaviour which is fully synchronised with the triggering sensory event can only be executed if the occurrence of this event can be predicted based on prior information. Smooth-pursuit eye movements are a classical and well-established example of goal-directed behaviour. The execution of these eye movements is thought to be very closely linked to the processing of visual motion signals. Here, we show that healthy human subjects as well as trained rhesus monkeys are able to initiate smooth-pursuit eye movements in anticipation of a moving target. These anticipatory pursuit eye movements are scaled to the velocity of the expected target. Furthermore, we can exclude the possibility that anticipatory pursuit is simply an after-pursuit of the previous trial. Visually-guided pursuit is only marginally affected by the presence of a structured background. However, the presence of a structured background severely impedes the ability to perform anticipatory pursuit. More generally, our data provide additional evidence that the cognitive oculomotor repertoires of human and monkeys are similar, at least with respect of smooth-pursuit in the prediction of an appearing target.

Primate area MST-l is involved in the generation of goal-directed eye and hand movements.

The contributions of the middle superior temporal area (MST) in the posterior parietal cortex of rhesus monkeys to the generation of smooth-pursuit eye movements as well as the contributions to motion perception are well established. Here, we present the first experimental evidence that this area also contributes to the generation of goal-directed hand movements toward a moving target. This evidence is based on the outcome of intracortical microstimulation experiments and transient lesions by small injections of muscimol at identified sites within the lateral part of area MST (MST-l). When microstimulation was applied during the execution of smooth-pursuit eye movements, postsaccadic eye velocity in the direction of the preferred direction of the stimulated site increased significantly (in 93 of 136 sites tested). When microstimulation was applied during a hand movement trial, the hand movement was displaced significantly in the same direction (in 28 of 39 sites tested). When we lesioned area MST-l transiently by injections of muscimol, steady-state eye velocity was exclusively reduced for ipsiversive smooth-pursuit eye movements. In contrast, hand movements were displaced toward the contralateral side, irrespective of the direction of the moving target. Our results provide evidence that area MST-l is involved in the processing of moving targets and plays a role in the execution of smooth-pursuit eye movements as well as visually guided hand movements.

Preparation and execution of saccades: the problem of limited capacity of computational resources.

Saccades are very fast, ballistic movements, which move the eyes from one target to another. Here, we show that the latency, precision and kinematics of saccades directed toward a target presented on a dark homogeneous background do not differ from the parameters of saccades directed toward a target presented on a structured background. However, if the visual background changed either its luminance or orientation simultaneously with the presentation of the saccade target, a significant increase in saccade latency was observed. The saccade kinematics as well as saccade precision, however, was not affected. Likewise, additional auditory stimulation applied simultaneously with the presentation of the target did not increase saccade latency. The increase in saccade latency and the maintenance of saccade kinematics indicate a sensory channel overload caused by the change in background. As a consequence, execution of the saccade was delayed until the computational resources to program the eye movement were available again.

Suppression of optokinesis during smooth pursuit eye movements revisited: the role of extra-retinal information.

When our eyes track objects that are moving in a richly structured environment, the retinal image of the stationary visual scene inevitably moves over the retina in a direction opposite to the eye movement. Such self-motion-induced global retinal slip usually provides an ideal stimulus for the optokinetic reflex. This reflex operates to compensate for global image flow. However, during smooth pursuit eye movements it must be shut down so that the reflex does not counteract the voluntary pursuit of moving targets. Here, we asked if retinal information is sufficient for this cancellation of the optokinetic reflex during smooth pursuit eye movements. In a series of experiments, we show that neither the eye movement-induced retinal image motion per se nor the relative motion between the pursuit target and the background are sufficient for suppression of optokinesis. We, therefore, conclude that extra-retinal information about smooth pursuit eye movements is required for the cancellation of the optokinetic reflex.

The neural basis of smooth-pursuit eye movements.

Smooth-pursuit eye movements are used to stabilize the image of a moving object of interest on the fovea, thus guaranteeing its high-acuity scrutiny. Such movements are based on a phylogenetically recent cerebro-ponto-cerebellar pathway that has evolved in parallel with foveal vision. Recent work has shown that a network of several cerebrocortical areas directs attention to objects of interest moving in three dimensions and reconstructs the trajectory of the target in extrapersonal space, thereby integrating various sources of multimodal sensory and efference copy information, as well as cognitive influences such as prediction. This cortical network is the starting point of a set of parallel cerebrofugal projections that use different parts of the dorsal pontine nuclei and the neighboring rostral nucleus reticularis tegmenti pontis as intermediate stations to feed two areas of the cerebellum, the flocculus-paraflocculus and the posterior vermis, which make mainly complementary contributions to the control of smooth pursuit.

Posterior parietal cortex neurons encode target motion in world-centered coordinates.

The motion areas of posterior parietal cortex extract information on visual motion for perception as well as for the guidance of movement. It is usually assumed that neurons in posterior parietal cortex represent visual motion relative to the retina. Current models describing action guided by moving objects work successfully based on this assumption. However, here we show that the pursuit-related responses of a distinct group of neurons in area MST of monkeys are at odds with this view. Rather than signaling object image motion on the retina, they represent object motion in world-centered coordinates. This representation may simplify the coordination of object-directed action and ego motion-invariant visual perception.

Motion perception without explicit activity in areas MT and MST.

It is widely accepted that middle temporal (MT) and middle superior temporal (MST) cortical areas in the brain of rhesus monkeys are essential for processing visual motion. We asked whether this assumption holds true if the moving stimulus consists of a second-order motion stimulus. In addition, we asked whether neurons in area MT and MST code for moving sound sources. To answer these questions, we trained three rhesus monkeys on a direction-discrimination task. Our monkeys were able to correctly report the direction of all motion stimuli used in this study. Firing rates of directionally selective neurons from area MT (n = 38) and MST (n = 68) were recorded during task performance. These neurons coded only for the stimulus movement if the motion stimulus was separated from the background by luminance or flicker (Fourier and drift-balanced motion). If these segregation cues were absent (in the case of theta motion and of the moving sound source), firing rates did not code for the stimulus' direction. Therefore we conclude that although areas MT and MST are undoubtedly involved in processing a moving stimulus, they are not the final cortical stages responsible for perceiving it.

Single-neuron evidence for a contribution of the dorsal pontine nuclei to both types of target-directed eye movements, saccades and smooth-pursuit.

The primate dorsolateral pontine nucleus (DLPN) is a key link in a cerebro-cerebellar pathway for smooth pursuit eye movements, a pathway assumed to be anatomically segregated from tegmental circuits subserving saccades. However, the existence of afferents from several cerebrocortical and subcortical centres for saccades suggests that the DLPN and neighbouring parts of the dorsal pontine nuclei (DPN) might contribute to saccades as well. In order to test this hypothesis, we recorded from the DPN of two monkeys trained to perform smooth pursuit eye movements as well as visually and memory-guided saccades. Out of 281 neurons isolated from the DPN, 138 were responsive in oculomotor tasks. Forty-five were exclusively activated in saccade paradigms, 68 exclusively by smooth pursuit and 25 neurons showed responses in both. Pursuit-related responses reflected sensitivity to eye position, velocity or combinations of velocity and position with minor contributions of acceleration in many cases. When tested in the memory-guided saccades paradigm, 65 out of 70 neurons activated in saccade paradigms showed significant saccade-related bursts and 20 significant activity in the memory period. Our finding of saccade-related activity in the DPN in conjunction with the existence of strong anatomical input from saccade-related cerebrocortical areas suggests that the DPN serves as a precerebellar relay for both pursuit and saccade-related information originating from cerebral cortex, in addition to the classical tecto-tegmental circuitry for saccades.

Visual-tracking neurons in area MST are activated during anticipatory pursuit eye movements.

Here, I report that rhesus monkeys are able to generate anticipatory smooth pursuit eye movements in the transient absence of a moving target, if this target moves periodically. The eye velocity before target reappearance was significantly larger if the target trajectory was predictable compared with the control condition consisting of unpredictable target trajectory. Parallel to the registration of the eye movements, single-unit activity was recorded from neurons in the middle superior temporal (MST) area of the two monkeys. The neuronal activity of visual-tracking neurons resembled the observed eye movements, i.e. these neurons increased their activity earlier if the movement of the target was predictable compared with the unpredictable control. These results provide further evidence for the existence of extra-retinal signals in the activity of visual-tracking neurons located in area MST.

Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an "imaginary" target.

Because smooth-pursuit eye movements (SPEM) can be executed only in the presence of a moving target, it has been difficult to attribute the neuronal activity observed during the execution of these eye movements to either sensory processing or to motor preparation or execution. Previously, we showed that rhesus monkeys can be trained to perform SPEM directed toward an "imaginary" target defined by visual cues confined to the periphery of the visual field. The pursuit of an "imaginary" target provides the opportunity to elicit SPEM without stimulating visual receptive fields confined to the center of the visual field. Here, we report that a subset of neurons [85 "imaginary" visual tracking (iVT)-neurons] in area MST of 3 rhesus monkeys were identically activated during pursuit of a conventional, foveal dot target and the "imaginary" target. Because iVT-neurons did not respond to the presentation of a moving "imaginary" target during fixation of a stationary dot, we are able to exclude that responses to pursuit of the "imaginary" target were artifacts of stimulation of the visual field periphery. Neurons recorded from the representation of the central parts of the visual field in neighboring area MT, usually vigorously discharging during pursuit of foveal targets, in no case responded to pursuit of the "imaginary" target. This dissociation between MT and MST neurons supports the view that pursuit responses of MT neurons are the result of target image motion, whereas those of iVT-neurons in area MST reflect an eye movement-related signal that is nonretinal in origin. iVT-neurons fell into two groups, depending on the properties of the eye movement-related signal. Whereas most of them (71%) encoded eye velocity, a minority showed responses determined by eye position, irrespective of whether eye position was changed by smooth pursuit or by saccades. Only the former group exhibited responses that led the eye movement, which is a prerequisite for a causal role in the generation of SPEM.