Oculomotor Action Research Articles

Brain areas associated with visual spatial attention display topographic organization during auditory spatial attention.

Spatially selective modulation of alpha power (8-14Hz) is a robust finding in electrophysiological studies of visual attention, and has been recently generalized to auditory spatial attention. This modulation pattern is interpreted as reflecting a top-down mechanism for suppressing distracting input from unattended directions of sound origin. The present study on auditory spatial attention extends this interpretation by demonstrating that alpha power modulation is closely linked to oculomotor action. We designed an auditory paradigm in which participants were required to attend to upcoming sounds from one of 24 loudspeakers arranged in a circular array around the head. Maintaining the location of an auditory cue was associated with a topographically modulated distribution of posterior alpha power resembling the findings known from visual attention. Multivariate analyses allowed the prediction of the sound location in the horizontal plane. Importantly, this prediction was also possible, when derived from signals capturing saccadic activity. A control experiment on auditory spatial attention confirmed that, in absence of any visual/auditory input, lateralization of alpha power is linked to the lateralized direction of gaze. Attending to an auditory target engages oculomotor and visual cortical areas in a topographic manner akin to the retinotopic organization associated with visual attention.

Oculomotor freezing reflects tactile temporal expectation and aids tactile perception

The oculomotor system keeps the eyes steady in expectation of visual events. Here, recording microsaccades while people performed a tactile, frequency discrimination task enabled us to test whether the oculomotor system shows an analogous preparatory response for unrelated tactile events. We manipulated the temporal predictability of tactile targets using tactile cues, which preceded the target by either constant (high predictability) or variable (low predictability) time intervals. We find that microsaccades are inhibited prior to tactile targets and more so for constant than variable intervals, revealing a tight crossmodal link between tactile temporal expectation and oculomotor action. These findings portray oculomotor freezing as a marker of crossmodal temporal expectation. Moreover, microsaccades occurring around the tactile target presentation are associated with reduced task performance, suggesting that oculomotor freezing mitigates potential detrimental, concomitant effects of microsaccades and revealing a crossmodal coupling between tactile perception and oculomotor action.

Primate Amygdalo-Nigral Pathway for Boosting Oculomotor Action in Motivating Situations.

SummaryA primary function of the primate amygdala is to modulate behavior based on emotional cues. To study the underlying neural mechanism, we first inactivated the amygdala locally and temporarily by injecting a GABA agonist. Then, saccadic eye movements and gaze were suppressed only on the contralateral side. Next, we performed optogenetic activation after injecting a viral vector into the amygdala. Optical stimulation in the amygdala excited amygdala neurons, whereas optical stimulation of axon terminals in the substantia nigra pars reticulata inhibited nigra neurons. Optical stimulation in either structure facilitated saccades to the contralateral side. These data suggest that the amygdala controls saccades and gaze through the basal ganglia output to the superior colliculus. Importantly, this amygdala-derived circuit mediates emotional context information, whereas the internal basal ganglia circuit mediates object value information. This finding demonstrates a basic mechanism whereby basal ganglia output can be modulated by other areas conveying distinct information.

Emotional faces guide the eyes in the absence of awareness.

The ability to act quickly to a threat is a key skill for survival. Under awareness, threat-related emotional information, such as an angry or fearful face, has not only perceptual advantages but also guides rapid actions such as eye movements. Emotional information that is suppressed from awareness still confers perceptual and attentional benefits. However, it is unknown whether suppressed emotional information can directly guide actions, or whether emotional information has to enter awareness to do so. We suppressed emotional faces from awareness using continuous flash suppression and tracked eye gaze position. Under successful suppression, as indicated by objective and subjective measures, gaze moved towards fearful faces, but away from angry faces. Our findings reveal that: (1) threat-related emotional stimuli can guide eye movements in the absence of visual awareness; (2) threat-related emotional face information guides distinct oculomotor actions depending on the type of threat conveyed by the emotional expression.

How Saccade Intrusions Affect Subsequent Motor and Oculomotor Actions.

In daily activities, there is a close spatial and temporal coupling between eye and hand movements that enables human beings to perform actions smoothly and accurately. If this coupling is disrupted by inadvertent saccade intrusions, subsequent motor actions suffer from delays, and lack of coordination. To examine how saccade intrusions affect subsequent voluntary actions, we used two tasks that require subjects to make motor/oculomotor actions in response to a visual cue. One was the memory guided saccade (MGS) task, and the other the hand reaction time (RT) task. The MGS task required subjects to initiate a voluntary saccade to a memorized target location, which is indicated shortly before by a briefly presented cue. The RT task required subjects to release a button on detection of a visual target, while foveating on a central fixation point. In normal subjects of various ages, inadvertent saccade intrusions delayed subsequent voluntary motor, and oculomotor actions. We also studied patients with Parkinson's disease (PD), who are impaired not only in initiating voluntary saccades but also in suppressing unwanted reflexive saccades. Saccade intrusions also delayed hand RT in PD patients. However, MGS was affected by the saccade intrusion differently. Saccade intrusion did not delay MGS latency in PD patients who could perform MGS with a relatively normal latency. In contrast, in PD patients who were unable to initiate MGS within the normal time range, we observed slightly decreased MGS latency after saccade intrusions. What explains this paradoxical phenomenon? It is known that motor actions slow down when switching between controlled and automatic behavior. We discuss how the effect of saccade intrusions on subsequent voluntary motor/oculomotor actions may reflect a similar switching cost between automatic and controlled behavior and a cost for switching between different motor effectors. In contrast, PD patients were unable to initiate internally guided MGS in the absence of visual target and could perform only automatic visually guided saccades, and did not have to switch between automatic and controlled behavior. This lack of switching may explain the shortening of MGS latency by the saccade intrusion in PD patients.

Impulsive oculomotor action selection in Parkinson’s disease

The effects of Parkinson's disease (PD) on the dynamics of impulsive action selection and suppression have recently been studied using distributional analyses, but with mixed results, especially for selection. Furthermore, some authors have suggested that impulsivity, regarded as a personality trait, shares common features with behavioral tasks’ measures. The current study was designed to clarify the impact of PD on impulsive action selection and suppression, and investigate the link between cognitive action control and self-reported impulsivity. We administered an oculomotor version of the Simon task to 32 patients with PD and 32 matched healthy controls (HC), and conducted distributional analyses in accordance with the activation-suppression model. Patients and HC also filled out the Barratt Impulsiveness Scale (BIS) questionnaire. Results showed that patients with PD were faster overall and exhibited a greater congruence effect than HC. They also displayed enhanced impulsive action selection. By contrast, the suppression of impulsive responses was similar across both groups. Furthermore, patients had higher impulsivity scores, which were correlated with higher impulsive action selection and higher suppression. Our study yielded two interesting findings. First, PD resulted in a higher number of fast errors. The activation-suppression model suggests that patients with PD are more susceptible to the impulsive action selection induced by the irrelevant stimulus dimension. Second, impulsive action selection and suppression were both associated with trait impulsivity, as measured by the BIS, indicating that these two aspects of impulsivity share common features.

Line bisection by eye and by hand reveal opposite biases

The vision-for-action literature favours the idea that the motor output of an action-whether manual or oculomotor-leads to similar results regarding object handling. Findings on line bisection performance challenge this idea: healthy individuals bisect lines manually to the left of centre and to the right of centre when using eye fixation. In case that these opposite biases for manual and oculomotor action reflect more universal compensatory mechanisms that cancel each other out to enhance overall accuracy, one would like to observe comparable opposite biases for other material. In the present study, we report on three independent experiments in which we tested line bisection (by hand, by eye fixation) not only for solid lines, but also for letter lines; the latter, when bisected manually, is known to result in a rightward bias. Accordingly, we expected a leftward bias for letter lines when bisected via eye fixation. Analysis of bisection biases provided evidence for this idea: manual bisection was more rightward for letter as compared to solid lines, while bisection by eye fixation was more leftward for letter as compared to solid lines. Support for the eye fixation observation was particularly obvious in two of the three studies, for which comparability between eye and hand action was increasingly adjusted (paper-pencil versus touch screen for manual action). These findings question the assumption that ocular motor and manual output are always inter-changeable, but rather suggest that at least for some situations ocular motor and manual output biases are orthogonal to each other, possibly balancing each other out.

The Effect of Mass Representation and Oculomotor Overshoot on “Representational Momentum

Analogous to the physical momentum of objects in the real-world, visual memory for the final position of a moving target is usually displaced along its trajectory. Such displacement is referred to representational momentum. Several different approaches have been applied to interpret the representational momentum, which range from low-level perceptual processing to high-level cognitive mechanisms (Hubbard, 2010). An early approach tried to explain the displacement effect by cognitive factors dealing with principles of "internalized dynamics". In addition to this cognitive approach, "low-level" explanations of representational momentum also have been proposed, suggesting that sensory factors play a decisive role. In particular, one plausible interpretation attributes the displacement effect to oculomotor action. In addition, it is possible that high-level information regarding physical principles contribute to the displacement by modulating eye movements (Hubbard, 2006b). We hypothesize that if eye movements modulate or mediate the effects of such information on displacement, disrupting normal eye movement would interrupt the effective information. In the current study, three types of 3D balls (made of paper, wood or stone) rolled from left or right sides accompanied by sound corresponding to the ball material. In Experiment 1, subjects (22 college students) were instructed to indicate the stop position of the ball by pressing a button after tracking its movement for 1037ms and disappeared about 350ms. In Experiment 2, subjects (19 college students) were asked either to pursue the moving target until it disappeared or to track it till it stopped at the center of screen indicating by a "+". The other procedures are similar to the Experiment 1. The subjects’ eye positions in both experiments were recorded by SMI Hi-Speed eye tracking system with sampling rate of 350Hz. In Experiment 1, the forward shift in the direction of motion of the stone ball was larger than those of the wooden and paper balls’. There was a significant difference between the forward shift of the stone ball and wooden or paper ball. In addition, the oculomotor overshoot velocity of the stone ball was significantly faster than other two lighter balls’. In Experiment 2, when the oculomotor behavior was controlled, the forward shift in the trajectory and the oculomotor overshoot velocity were reduced compared to those in the eye tracking condition. The present findings revealed that high-level cognitive factors (mass representation) modulate both oculomotor behavior and representational momentum. Meanwhile, representational momentum is also influenced by oculomotor overshoot. Our results suggest that high-level cognitive factors (mass representation) influence representational momentum by oculomotor-related information. Yet, representational momentum is also affected by many other factors. Our study provides new evidence that perceptual factor (oculomotor information) is not the only way to produce representational momentum.

A role of the human thalamus in predicting the perceptual consequences of eye movements

Internal monitoring of oculomotor commands may help to anticipate and keep track of changes in perceptual input imposed by our eye movements. Neurophysiological studies in non-human primates identified corollary discharge (CD) signals of oculomotor commands that are conveyed via thalamus to frontal cortices. We tested whether disruption of these monitoring pathways on the thalamic level impairs the perceptual matching of visual input before and after an eye movement in human subjects. Fourteen patients with focal thalamic stroke and 20 healthy control subjects performed a task requiring a perceptual judgment across eye movements. Subjects reported the apparent displacement of a target cue that jumped unpredictably in sync with a saccadic eye movement. In a critical condition of this task, six patients exhibited clearly asymmetric perceptual performance for rightward vs. leftward saccade direction. Furthermore, perceptual judgments in seven patients systematically depended on oculomotor targeting errors, with self-generated targeting errors erroneously attributed to external stimulus jumps. Voxel-based lesion-symptom mapping identified an area in right central thalamus as critical for the perceptual matching of visual space across eye movements. Our findings suggest that trans-thalamic CD transmission decisively contributes to a correct prediction of the perceptual consequences of oculomotor actions.

Action video game experience affects oculomotor performance

Action video games have been show to affect a variety of visual and cognitive processes. There is, however, little evidence of whether playing video games can also affect motor action. To investigate the potential link between experience playing action video games and changes in oculomotor action, we tested habitual action video game players (VGPs) and non-video game players (NVGPs) in a saccadic trajectory deviation task. We demonstrate that spatial curvature of a saccadic trajectory towards or away from distractor is profoundly different between VGPs and NVGPs. In addition, task performance accuracy improved over time only in VGPs. Results are discussed in the context of the competing interplay between stimulus-driven motor programming and top–down inhibition during oculomotor execution.

Action effects in saccade control

According to the ideomotor principle, action preparation involves the activation of associations between actions and their effects. However, there is only sparse research on the role of action effects in saccade control. Here, participants responded to lateralized auditory stimuli with spatially compatible saccades toward peripheral targets (e.g., a rhombus in the left hemifield and a square in the right hemifield). Prior to the imperative auditory stimulus (e.g., a left tone), an irrelevant central visual stimulus was presented that was congruent (e.g., a rhombus), incongruent (e.g., a square), or unrelated (e.g., a circle) to the peripheral saccade target (i.e., the visual effect of the saccade). Saccade targets were present throughout a trial (Experiment 1) or appeared after saccade initiation (Experiment 2). Results showed shorter response times and fewer errors in congruent (vs. incongruent) conditions, suggesting that associations between oculomotor actions and their visual effects play an important role in saccade control.

Theta-Burst Stimulation over Human Frontal Cortex Distorts Perceptual Stability across Eye Movements

We perceive a stable outside world despite the constant changes of visual input induced by our eye movements. Internal monitoring of a corollary discharge associated with oculomotor commands may help to anticipate the perceptual consequences of impending eye movements. The primate frontal eye fields have repeatedly been presumed to participate in the maintenance of perceptual stability across eye movements. However, a direct link between integrity of frontal oculomotor areas and perceptual stability is missing so far. Here, we show that transcranial magnetic stimulation (TMS) over the right human frontal cortex impairs the integration of visual space across eye movements. We asked 9 healthy subjects to report the direction of transsaccadic stimulus displacements and applied TMS before the actual experiment in a novel offline stimulation protocol, continuous theta-burst stimulation (cTBS). A systematic perceptual distortion was observed after stimulation over the right frontal cortex that was best explained by an internal underestimation of executed eye movement amplitudes. cTBS apparently disturbed an internal prediction process for contraversive saccades, while the metrics of associated oculomotor actions remained unchanged. Our findings suggest an important role of the frontal cortex in the internal monitoring of oculomotor actions for the perceptual integration of space across eye movements.

More than Meets the Eye: Age Differences in the Capture and Suppression of Oculomotor Action

Salient visual stimuli capture attention and trigger an eye-movement toward its location reflexively, regardless of an observer’s intentions. Here we aim to investigate the effect of aging (1) on the extent to which salient yet task-irrelevant stimuli capture saccades, and (2) on the ability to selectively suppress such oculomotor responses. Young and older adults were asked to direct their eyes to a target appearing in a stimulus array. Analysis of overall performance shows that saccades to the target object were disrupted by the appearance of a task-irrelevant abrupt-onset distractor when the location of this distractor did not coincide with that of the target object. Conditional capture function analyses revealed that, compared to young adults, older adults were more susceptible to oculomotor capture, and exhibited deficient selective suppression of the responses captured by task-irrelevant distractors. These effects were uncorrelated, suggesting two independent sources off age-related decline. Thus, with advancing age, salient visual distractors become more distracting; in part because they trigger reflexive eye-movements more potently; in part because of failing top-down control over such reflexes. The fact that these process-specific age effects remained concealed in overall oculomotor performance analyses emphasizes the utility of looking beyond the surface; indeed, there may be more than meets the eye.

Emotion and action: the effect of fear on saccadic performance

According to evolutionary accounts, emotions originated to prepare an organism for action (Darwin 1872; Frijda 1986). To investigate this putative relationship between emotion and action, we examined the effect of an emotional stimulus on oculomotor actions controlled by the superior colliculus (SC), which has connections with subcortical structures involved in the perceptual prioritization of emotion, such as the amygdala through the pulvinar. The pulvinar connects the amygdala to cells in the SC responsible for the speed of saccade execution, while not affecting the spatial component of the saccade. We tested the effect of emotion on both temporal and spatial signatures of oculomotor functioning using a gap-distractor paradigm. Changes in spatial programming were examined through saccadic curvature in response to a remote distractor stimulus, while changes in temporal execution were examined using a fixation gap manipulation. We show that following the presentation of a task-irrelevant fearful face, the temporal but not the spatial component of the saccade generation system was affected.

Caudate Encodes Multiple Computations for Perceptual Decisions

Perceptual decision making is a complex process that requires multiple computations, including the accumulation of sensory evidence and an ongoing evaluation of the accumulation process to use for prediction and adjustment. Implementing these computations likely involves interactions among many brain regions. For perceptual decisions linked to oculomotor actions, neural correlates of sensory evidence accumulation have been identified in several cortical areas, including the frontal eye field and lateral intraparietal area, and one of their direct, subcortical targets, the superior colliculus. These structures are also connected indirectly, via the basal ganglia. The basal ganglia pathway has been theorized to contribute to perceptual decision making, but the nature of this contribution has yet to be examined directly. Here we show that in monkeys performing a reaction-time visual motion direction-discrimination task, neurons in a primary input structure of the basal ganglia, the caudate nucleus, encode three aspects of decision making: evidence accumulation, evaluation, and choice biases. These results indicate that the basal ganglia pathway can provide important signals to influence and assess perceptual decisions that guide oculomotor behavior.

A metanalysis of the effect of the Müller-Lyer illusion on saccadic eye movements: No general support for a dissociation of perception and oculomotor action

Milner and Goodale’s (1995) proposal of a functional division of labor between vision-for-perception and vision-for-action is supported by neuropsychological, brain-imaging, and psychophysical evidence. However, there remains considerable debate as to whether, as their proposal would predict, the effect of contextual illusions on vision-for-action can be dissociated from that on vision-for-perception. Meta-analytical efforts examining the effect of the Müller-Lyer (ML) illusion on pointing ( Bruno, Bernardis, & Gentilucci, 2008) or grasping ( Bruno & Franz, 2009) have been conducted to resolve the controversy. To complement this work, here we re-analyzed 17 papers detailing 21 independent studies investigating primary saccades to target locations that were perceptually biased by the ML illusion. Using a corrected percent illusion effect measure to compare across different studies and across experimental conditions within studies, we find that saccadic eye movements are always strongly biased by the illusion although the size of this effect can be reduced by factors such as display duration and between-trials variability in display length and orientation, possibly due to a process of saccadic adaptation. In contrast to some reports, we find no general support for differences between voluntary and reflexive saccades or between saccades performed in conjunction with a pointing movement and saccades performed without pointing. We conclude that studies on the effect of the Müller-Lyer illusion do not provide evidence for a functional dissociation between primary saccades and perception.

Contextual modulation of oculomotor control reflected in N2 and saccade reaction time distributions

Avoiding reflexive saccades triggered by salient yet task-irrelevant stimuli requires the engagement of control processes that inhibit attention toward irrelevant objects and prevent reflex-like oculomotor action. In the current study participants made saccades to visual targets to the left and right of fixation as directed by target appearance. A distractor could either be presented in the same (congruent trials) or the opposite hemifield (incongruent trials) as the target. Trial context was manipulated, creating risky (mostly incongruent blocks), safe (mostly congruent blocks), or neutral conditions. Electroencephalogram was measured to examine if any contextual modulations would be reflected in the N2 peak frequently associated with performance monitoring. The results are discussed within the framework of dual mechanisms of cognitive control and suggest that a high-risk context facilitates avoidance of capture, lessening the need for reactive control.

Development of perceptual completion originates in information acquisition.

Adults have little difficulty perceiving objects as complete despite occlusion, but newborn infants perceive moving partly occluded objects solely in terms of visible surfaces. The developmental mechanisms leading to perceptual completion have never been adequately explained. Here, the authors examine the potential contributions of oculomotor behavior and motion sensitivity to perceptual completion performance in individual infants. Young infants were presented with a center-occluded rod, moving back and forth against a textured background, to assess perceptual completion. Infants also participated in tasks to assess oculomotor scanning patterns and motion direction discrimination. Individual differences in perceptual completion performance were strongly correlated with scanning patterns but were unrelated to motion direction discrimination. The authors present a new model of development of perceptual completion that posits a critical role for targeted visual scanning, an early developing oculomotor action system.

Similar Neural Representations of the Target for Saccades and Perception during Search

Are the body's actions and the mind's perceptions the result of shared neural processing, or are they performed largely independently? The brain has two major processing streams, and some have proposed that this division segregates visual processing for action and perception. The ventral pathway is claimed to support conscious experience (perception), whereas the dorsal pathway is claimed to support the control of movement (action). Others have argued that perception and action share much of their visual processing within the primate cortex. During visual search, the brain performs a sophisticated deployment of eye movements (saccadic actions) to gather information to subserve perceptual judgments. The relationship between the neural mechanisms mediating perception and action in visual search remains unexplored. Here, we investigate the visual representation of target information in the human brain, both for perceptual decisions and for saccadic actions during visual search. We use classification image analysis, a form of reverse correlation, to estimate the behavioral receptive fields of the visual mechanisms responsible for saccadic and perceptual responses during the same visual search task. Results show that the behavioral receptive fields mediating the perceptual decisions are indistinguishable from those driving the oculomotor decisions, suggesting that similar neural mechanisms are responsible for both perception and oculomotor action during search. Diverging target representations would result in an inefficient coupling between eye movement planning and perceptual judgments. Thus, a common target representation would be more optimal and might be expected to have evolved through natural selection in the neural systems responsible for visual search.

Extra-Retinal Vision: Firing at Will

Recent evidence suggests that a key visual motion centre in the brain ignores extra-retinal motor information concerning reflexive eye movement. Instead it seems that neurons sensitive to oculomotor actions in this area fire at will.