A triple distinction of cerebellar function for oculomotor learning and fatigue compensation.

The cerebellum implements error-based motor learning via synaptic gain adaptation of an inverse model, i.e. the mapping of a spatial movement goal onto a motor command. Recently, we modeled the motor and perceptual changes during learning of saccadic eye movements, showing that learning is actually a threefold process. Besides motor recalibration of (1) the inverse model, learning also comprises perceptual recalibration of (2) the visuospatial target map and (3) of a forward dynamics model that estimates the saccade size from corollary discharge. Yet, the site of perceptual recalibration remains unclear. Here we dissociate cerebellar contributions to the three stages of learning by modeling the learning data of eight cerebellar patients and eight healthy controls. Results showed that cerebellar pathology restrains short-term recalibration of the inverse model while the forward dynamics model is well informed about the reduced saccade change. Adaptation of the visuospatial target map trended in learning direction only in control subjects, yet without reaching significance. Moreover, some patients showed a tendency for uncompensated oculomotor fatigue caused by insufficient upregulation of saccade duration. According to our model, this could induce long-term perceptual compensation, consistent with the overestimation of target eccentricity found in the patients' baseline data. We conclude that the cerebellum mediates short-term adaptation of the inverse model, especially by control of saccade duration, while the forward dynamics model was not affected by cerebellar pathology.

Eyeball translations affect saccadic eye movements beyond brainstem control.

Vision requires that we rotate our eyes frequently to look at informative structures in the scene. Eye movements are planned by the brain but their execution depends on the mechanical properties of the oculomotor plant, that is, the arrangement of eyeball position, muscle insertions, and pulley locations. Therefore, the biomechanics of rotations is sensitive to eyeball translation because it changes muscle levers. Eyeball translations are little researched as they are difficult to measure with conventional techniques. Here, we investigated the effects of eyeball translation on the coordination of eyeball rotation by high-speed MRI recordings of saccadic eye movements during blinks, which are known to produce strong translations. We found that saccades during blinks massively overshoot their targets and that these overshoots occur in a transient fashion such that the gaze is back on target at the time the blink ends. These dynamic overshoots were tightly coupled to the eyeball translation, both in time and in size. Saccades made without blinks were also accompanied by small amounts of transient eyeball retraction, the size of which scaled with saccade amplitude. These findings demonstrate a complex combination of rotation and translation of the eye. The mechanical consequences of eyeball translation on oculomotor control should be considered along with the neural implementation in the brainstem to understand the generation of eye movements and their disorders.NEW & NOTEWORTHY We found that saccades during blinks can massively overshoot their target when the eyeball is retracted. Our data imply that the overshoots are not part of the saccade plan prepared in the brainstem, but instead a consequence of the altered biomechanics resulting from concurrent eyeball translation and rotation. To our best knowledge, this is the first direct observation of dynamic properties of the oculomotor plant altering the execution of rotational eye movements.

Cerebellar signals drive motor adjustments and visual perceptual changes during forward and backward adaptation of reactive saccades.

Saccadic adaptation ($SA$) is a cerebellar-dependent learning of motor commands ($MC$), which aims at preserving saccade accuracy. Since $SA$ alters visual localization during fixation and even more so across saccades, it could also involve changes of target and/or saccade visuospatial representations, the latter ($CDv$) resulting from a motor-to-visual transformation (forward dynamics model) of the corollary discharge of the $MC$. In the present study, we investigated if, in addition to its established role in adaptive adjustment of $MC$, the cerebellum could contribute to the adaptation-associated perceptual changes. Transfer of backward and forward adaptation to spatial perceptual performance (during ocular fixation and trans-saccadically) was assessed in eight cerebellar patients and eight healthy volunteers. In healthy participants, both types of $SA$ altered $MC$ as well as internal representations of the saccade target and of the saccadic eye displacement. In patients, adaptation-related adjustments of $MC$ and adaptation transfer to localization were strongly reduced relative to healthy participants, unraveling abnormal adaptation-related changes of target and $CDv$. Importantly, the estimated changes of $CDv$ were totally abolished following forward session but mainly preserved in backward session, suggesting that an internal model ensuring trans-saccadic localization could be located in the adaptation-related cerebellar networks or in downstream networks, respectively.

Visual perception of travel distance for self-motion through crowds.

Humans can use visual motion to estimate the distance they have traveled. In static environments, optic flow generated by self-motion provides a pattern of expanding motion that is used for the estimation of travel distance. When the environment is populated by other people, their biological motion destroys the one-to-on correspondence between optic flow and travel distance. We investigated how observers estimate travel distance in a crowded environment. In three conditions, we simulated self-motion through a crowd of standing, approaching, or leading point-light walkers. For a standing crowd, optic flow is a veridical signal for distance perception. For an approaching crowd, the visual motion is the sum of the self-motion-induced optic flow and the optic flow produced by the approaching walkers. If only optic flow were to be used, travel distance estimates would be too high because of the approaching direction of the crowd toward the observer. If, on the other hand, cues from biological motion could be used to estimate the speed of the crowd, then the excessive optic from the approaching crowd flow might be compensated. In the leading crowd condition, in which walkers of the crowd keep their distance from the observer as they walk along with the observer, no optic flow is produced. In this condition, travel distance estimation would have to rely solely on biological motion information. We found that distance estimation was quite similar across these three conditions. This suggests that biological motion information can be used (a) to compensate for excessive optic flow in the approaching crowd condition and (b) to generate distance information in the leading crowd condition.

Illusory percepts of curvilinear self-motion when moving through crowds.

Self-motion generates optic flow, a pattern of expanding visual motion. Heading estimation from optic flow analysis is accurate in rigid environments, but it becomes challenging when other human walkers introduce independent motion to the scene. Previous studies showed that heading perception is surprisingly accurate when moving through a crowd of walkers but revealed strong heading biases when either articulation or translation of biological motion were presented in isolation. We hypothesized that these biases resulted from misperceiving the self-motion as curvilinear. Such errors might manifest as opposite biases depending on whether the observer perceived the crowd motion as indication of his/her self-translation or self-rotation. Our study investigated the link between heading biases and illusory path perception. Participants assessed heading and path perception while observing optic flow stimuli with varying walker movements. Self-motion perception was accurate during natural locomotion (articulation and translation), but significant heading biases occurred when walkers only articulated or translated. In this case, participants often reported a curved path of travel. Heading error and curvature pointed in opposite directions. On average, participants perceived the walker motion as evidence for viewpoint rotation leading to curvilinear path percepts.

Timing and kinematics of horizontal within-blink saccades measured by EOG.

Eyeblinks are the brief closures of the lid. They are accompanied by a cocontraction of the eye muscles that temporarily pulls the whole eyeball back into its socket. When blinks occur together with execution of saccadic gaze shifts, they interfere with the saccadic premotor circuit, causing these within-blink saccades to be slower than normal and also time-locked to blinks. To analyze the trajectory of within-blink saccades, subtraction of the entangled blink-related eye movement is required. Here we propose a combination of principal component analysis (PCA) and a regression model to subtract the blink-related component of the eye movement based on the respective blink metrics. We used electrooculography (EOG) to measure eye and lid movements of 12 participants who performed saccades with and without blinks. We found that within-blink saccades are slower than without-blink saccades and are tightly coupled in time to blink onset. Surprisingly, in some participants we observed large dynamic overshoots of up to 15° for saccades of only 5° amplitude. The finding of dynamic overshoots was independently confirmed by dynamic MRI for two of the participants and challenges the current view that within-blink saccades are programmed as slow, but straight, saccades. We hypothesize that the dynamic overshoots could be attributed to inhibition of omnipause neurons during blinks, the simultaneous cocontraction of extraocular muscles, or a combination of both.NEW & NOTEWORTHY This study observed that people make large dynamic overshoots when making a saccadic eye movement within a blink but their eyes are back on target by the time the eyelids are open. We used electrooculography (EOG) to measure eye movements even when the lid is down and introduced a novel procedure to subtract blink-related EOG components. These findings challenge the current view that within-blink saccades are programmed as slow but straight saccades.

Mislocalization after inhibition of saccadic adaptation.

Saccadic eye movements are often imprecise and result in an error between expected and actual retinal target location after the saccade. Repeated experience of this error produces changes in saccade amplitude to reduce the error and concomitant changes in apparent visual location. We investigated the relationship between these two plastic processes in a series of experiments. Following a recent paradigm of inhibition of saccadic adaptation, in which participants are instructed to look at the initial target position and to continue to look at that position even if the target were to move again, our participants nevertheless perceived a visual probe presented near the saccade target to be shifted in direction of the target error. The location percept of the target gradually shifted and diverged over time from the executed saccade. Our findings indicate that changes in perceived location can be the same even when changes in saccade amplitude differ according to instruction and can develop even when the amplitude of the saccades executed during the adaptation procedure does not change. There are two possible explanations for this divergence between the adaptation states of saccade amplitude and perceived location. Either the intrasaccadic target step might trigger updating of the association between pre- and post-saccadic target positions, causing the localization shift, or the saccade motor command adjusts together with the perceived location at a common adaptation site, downstream from which voluntary control is exerted upon the executed eye movement only.

Flexible use of post-saccadic visual feedback in oculomotor learning.

Saccadic eye movements bring objects of interest onto our fovea. These gaze shifts are essential for visual perception of our environment and the interaction with the objects within it. They precede our actions and are thus modulated by current goals. It is assumed that saccadic adaptation, a recalibration process that restores saccade accuracy in case of error, is mainly based on an implicit comparison of expected and actual post-saccadic position of the target on the retina. However, there is increasing evidence that task demands modulate saccade adaptation and that errors in task performance may be sufficient to induce changes to saccade amplitude. We investigated if human participants are able to flexibly use different information sources within the post-saccadic visual feedback in task-dependent fashion. Using intra-saccadic manipulation of the visual input, participants were either presented with congruent post-saccadic information, indicating the saccade target unambiguously, or incongruent post-saccadic information, creating conflict between two possible target objects. Using different task instructions, we found that participants were able to modify their saccade behavior such that they achieved the goal of the task. They succeeded in decreasing saccade gain or maintaining it, depending on what was necessary for the task, irrespective of whether the post-saccadic feedback was congruent or incongruent. It appears that action intentions prime task-relevant feature dimensions and thereby facilitated the selection of the relevant information within the post-saccadic image. Thus, participants use post-saccadic feedback flexibly, depending on their intentions and pending actions.

Multisensory integration in cortical regions responding to locomotion-related visual and somatomotor signals.

During real-world locomotion, in order to be able to move along a path or avoid an obstacle, continuous changes in self-motion direction (i.e. heading) are needed. Control of heading changes during locomotion requires the integration of multiple signals (i.e., visual, somatomotor, vestibular). Recent fMRI studies have shown that both somatomotor areas (human PEc [hPEc], human PE [hPE], primary somatosensory cortex [S-I]) and egomotion visual regions (cingulate sulcus visual area [CSv], posterior cingulate area [pCi], posterior insular cortex [PIC]) respond to either leg movements and egomotion-compatible visual stimulations, suggesting a role in the analysis of both visual attributes of egomotion and somatomotor signals with the aim of guiding locomotion. However, whether these regions are able to integrate egomotion-related visual signals with somatomotor inputs coming from leg movements during heading changes remains an open question. Here we used a combined approach of individual functional localizers and task-evoked activity by fMRI. In thirty subjects we first localized three egomotion areas (CSv, pCi, PIC) and three somatomotor regions (S-I, hPE, hPEc). Then, we tested their responses in a multisensory integration experiment combining visual and somatomotor signals relevant to locomotion in congruent or incongruent trials. We used an fMR-adaptation paradigm to explore the sensitivity to the repeated presentation of these bimodal stimuli in the six regions of interest. Results revealed that hPE, S-I and CSv showed an adaptation effect regardless of congruency, while PIC, pCi and hPEc showed sensitivity to congruency. PIC exhibited a preference for congruent trials compared to incongruent trials. Areas pCi and hPEc exhibited an adaptation effect only for congruent and incongruent trials, respectively. PIC, pCi and hPEc sensitivity to the congruency relationship between visual (locomotion-compatible) cues and (leg-related) somatomotor inputs suggests that these regions are involved in multisensory integration processes, likely in order to guide/adjust leg movements during heading changes.

Salient objects dominate the central fixation bias when orienting toward images.

Short-latency saccades are often biased toward salient objects or toward the center of images, for example, when inspecting photographs of natural scenes. Here, we measured the contribution of salient objects and central fixation bias to visual selection over time. Participants made saccades to images containing one salient object on a structured background and were instructed to either look at (i) the image center, (ii) the salient object, or (iii) at a cued position halfway in between the two. Results revealed, first, an early involuntary bias toward the image center irrespective of strategic behavior or the location of objects in the image. Second, the salient object bias was stronger than the center bias and prevailed over the latter when they directly competed for visual selection. In a second experiment, we tested whether the center bias depends on how well the image can be segregated from the monitor background. We asked participants to explore images that either did or did not contain a salient object while we manipulated the contrast between image background and monitor background to make the image borders more or less visible. The initial orienting toward the image was not affected by the image-monitor contrast, but only by the presence of objects-with a strong bias toward the center of images containing no object. Yet, a low image-monitor contrast reduced this center bias during the subsequent image exploration.

Pitting optic flow, object motion, and biological motion against each other.

Heading estimation from optic flow is crucial for safe locomotion but becomes inaccurate if independent object motion is present. In ecological settings, such motion typically involves other animals or humans walking across the scene. An independently walking person presents a local disturbance of the flow field, which moves across the flow field as the walker traverses the scene. Is the bias in heading estimation produced by the local disturbance of the flow field or by the movement of the walker through the scene? We present a novel flow field stimulus in which the local flow disturbance and the movement of the walker can be pitted against each other. Each frame of this stimulus consists of a structureless random dot distribution. Across frames, the body shape of a walker is molded by presenting different flow field dynamics within and outside the body shape. In different experimental conditions, the flow within the body shape can be congruent with the walker's movement, incongruent with it, or congruent with the background flow. We show that heading inaccuracy results from the local flow disturbance rather than the movement through the scene. Moreover, we show that the local disturbances of the optic flow can be used to segment the walker and support biological motion perception to some degree. The dichotomous result that the walker can be segmented from the scene but that heading perception is nonetheless influenced by the flow produced by the walker confirms separate visual pathways for heading estimation, object segmentation, and biological motion perception.

Combining biological motion perception with optic flow analysis for self-motion in crowds.

Heading estimation from optic flow relies on the assumption that the visual world is rigid. This assumption is violated when one moves through a crowd of people, a common and socially important situation. The motion of people in the crowd contains cues to their translation in the form of the articulation of their limbs, known as biological motion. We investigated how translation and articulation of biological motion influence heading estimation from optic flow for self-motion in a crowd. Participants had to estimate their heading during simulated self-motion toward a group of walkers who collectively walked in a single direction. We found that the natural combination of translation and articulation produces surprisingly small heading errors. In contrast, experimental conditions that either present only translation or only articulation produced strong idiosyncratic biases. The individual biases explained well the variance in the natural combination. A second experiment showed that the benefit of articulation and the bias produced by articulation were specific to biological motion. An analysis of the differences in biases between conditions and participants showed that different perceptual mechanisms contribute to heading perception in crowds. We suggest that coherent group motion affects the reference frame of heading perception from optic flow.

Trans-saccadic adaptation of perceived size independent of saccadic adaptation.

Systematic shortening or lengthening of target objects during saccades modifies saccade amplitudes and perceived size of the objects. These two events are concomitant when size change during the saccade occurs asymmetrically, thereby shifting the center of mass of the object. In the present study, we asked whether or not the two are necessarily linked. We tested human participants in symmetrical systematic shortening and lengthening of a vertical bar during a horizontal saccade, aiming to not modify the saccade amplitude. Before and after a phase of trans-saccadic changes of the target bar, participants manually indicated the sizes of various vertically oriented bars by open-loop grip aperture. We evaluated the effect of trans-saccadic changes of bar length on manual perceptual reports and whether this change depended on saccade amplitude. As expected, we did not induce any change in horizontal or vertical components of saccade amplitude, but we found a significant difference in perceived size after the lengthening experiment compared to after the shortening experiment. Moreover, after the lengthening experiment, perceived size differed significantly from pre-lengthening baseline. These findings suggest that a change of size perception can be induced trans-saccadically, and its mechanism does not depend on saccadic amplitude change.

Roles of visual and non-visual information in the perception of scene-relative object motion during walking.

Perceiving object motion during self-movement is an essential ability of humans. Previous studies have reported that the visual system can use both visual information (such as optic flow) and non-visual information (such as vestibular, somatosensory, and proprioceptive information) to identify and globally subtract the retinal motion component due to self-movement to recover scene-relative object motion. In this study, we used a motion-nulling method to directly measure and quantify the contribution of visual and non-visual information to the perception of scene-relative object motion during walking. We found that about 50% of the retinal motion component of the probe due to translational self-movement was removed with non-visual information alone and about 80% with visual information alone. With combined visual and non-visual information, the self-movement component was removed almost completely. Although non-visual information played an important role in the removal of self-movement-induced retinal motion, it was associated with decreased precision of probe motion estimates. We conclude that neither non-visual nor visual information alone is sufficient for the accurate perception of scene-relative object motion during walking, which instead requires the integration of both sources of information.

Postsaccadic eye position contributes to oculomotor error estimation in saccadic adaptation.

We investigated whether the proprioceptive eye position signal after the execution of a saccadic eye movement is used to estimate the accuracy of the movement. If so, saccadic adaptation, the mechanism that maintains saccade accuracy, could use this signal in a similar way as it uses visual feedback after the saccade. To manipulate the availability of the proprioceptive eye position signal we utilized the finding that proprioceptive eye position information builds up gradually after a saccade over a time interval comparable to typical saccade latencies. We confined the retention time of gaze at the saccade landing point by asking participants to make fast return saccades to the fixation point that preempt the usability of proprioceptive eye position signals. In five experimental conditions we measured the influence of the visual and proprioceptive feedback, together and separately, on the development of adaptation. We found that the adaptation of the previously shortened saccades in the case of visual feedback being unavailable after the saccade was significantly weaker when the use of proprioceptive eye position information was impaired by fast return saccades. We conclude that adaptation can be driven by proprioceptive eye position feedback.NEW & NOTEWORTHY We show that proprioceptive eye position information is used after a saccade to estimate motor error and adapt saccade control. Previous studies on saccadic adaptation focused on visual feedback about saccade accuracy. A multimodal error signal combining visual and proprioceptive information is likely more robust. Moreover, combining proprioceptive and visual measures of saccade performance can be helpful to keep vision, proprioception, and motor control in alignment and produce a coherent representation of space.

Fixation related shifts of perceptual localization counter to saccade direction.

Perisaccadic compression of the perceived location of flashed visual stimuli toward a saccade target occurs from about 50 ms before a saccade. Here we show that between 150 and 80 ms before a saccade, perceived locations are shifted toward the fixation point. To establish the cause of the "reverse" presaccadic perceptual distortion, participants completed several versions of a saccade task. After a cue to saccade, a probe bar stimulus was briefly presented within the saccade trajectory. In Experiment 1 participants made (a) overlap saccades with immediate return saccades, (b) overlap saccades, and (c) step saccades. In Experiment 2 participants made gap saccades in complete darkness. In Experiment 3 participants maintained fixation with the probe stimuli masked at various interstimulus intervals. Participants indicated the bar's location using a mouse cursor. In all conditions in Experiment 1 presaccadic compression was preceded by compression toward the initial fixation. In Experiment 2, saccadic compression was maintained but the preceding countercompression was not observed. Stimuli masked at fixation were not compressed. This suggests the two opposing compression effects are related to the act of executing an eye movement. They are also not caused by the requirement to make two sequential saccades ending at the initial fixation location and are not caused by continuous presence of the fixation markers. We propose that countercompression is related to fixation activity and is part of the sequence of motor preparations to execute a cued saccade.

Heading perception from optic flow in the presence of biological motion.

We investigated whether biological motion biases heading estimation from optic flow in a similar manner to nonbiological moving objects. In two experiments, observers judged their heading from displays depicting linear translation over a random-dot ground with normal point light walkers, spatially scrambled point light walkers, or laterally moving objects composed of random dots. In Experiment 1, we found that both types of walkers biased heading estimates similarly to moving objects when they obscured the focus of expansion of the background flow. In Experiment 2, we also found that walkers biased heading estimates when they did not obscure the focus of expansion. These results show that both regular and scrambled biological motion affect heading estimation in a similar manner to simple moving objects, and suggest that biological motion is not preferentially processed for the perception of self-motion.

Heading Through a Crowd.

The ability to navigate through crowds of moving people accurately, efficiently, and without causing collisions is essential for our day-to-day lives. Vision provides key information about one's own self-motion as well as the motions of other people in the crowd. These two types of information (optic flow and biological motion) have each been investigated extensively; however, surprisingly little research has been dedicated to investigating how they are processed when presented concurrently. Here, we showed that patterns of biological motion have a negative impact on visual-heading estimation when people within the crowd move their limbs but do not move through the scene. Conversely, limb motion facilitates heading estimation when walkers move independently through the scene. Interestingly, this facilitation occurs for crowds containing both regular and perturbed depictions of humans, suggesting that it is likely caused by low-level motion cues inherent in the biological motion of other people.

No special treatment of independent object motion for heading perception.

How do we judge the direction of self-motion (i.e., heading) in the presence of independent object motion? Previous studies that examined this question confounded the effects of a moving object's speed and its position on heading judgments, and did not examine whether the visual system uses salient nonmotion visual cues (such as color contrast and binocular disparity) to segment a moving object from global optic flow prior to heading estimation. The current study addressed these issues with both behavioral testing and computational modeling. Our results show that the visual system does not treat independent object motion separately for the perception of heading during self-motion. This is surprising because we all can segment a moving object from global optic flow and perceive its scene-relative motion independent of self-motion. Our findings support the claim that the perception of self-motion with independent object motion and the perception of object motion during self-motion are performed by different neural mechanisms.

Experience-dependent long-term facilitation of skew adaptation.

Adaptation to changes in the environment allows the visual system to achieve optimal perception in a continuously changing visual world. One particular example regarding recurrently encountered changes in everyday vision is geometrical distortions of the environment when wearing spectacles for vision correction, e.g., image shear by skew geometric distortions in progressive additional lenses. For optimal visual performance, it would be beneficial if the visual system uses previous history of recurrent distortions and learns to adapt fast when they are reapplied, yet this has not been systematically shown. The present study evaluates experience-dependent long-term facilitation of fast adaptation to image skew, i.e., a shear from the x- and y- axis, using ecological stimuli. Immediate and long-term facilitation of fast adaptation induced by minutes time scales of extended skew exposures was tested. Fast adaptation was quantified via the magnitude of perceptual bias after a brief exposure to image skew in a constant stimulus procedure. Immediate facilitation was tested by comparing the magnitudes of fast adaptation that are measured on the same day before, i.e., baseline, and after extended skew exposure. The retention of the facilitation was evaluated by comparing the fast adaptation measured after, on average, 57 days of the previous extended skew exposure with the baseline. After one hour of skew exposure, the amount of fast adaptation significantly increased from the baseline measurement indicating immediate facilitation of the fast adaptation. This facilitation was retained at, on average, 57 days after the extended exposure. Thus, the results depicted experience dependent long-term facilitation of skew adaptation that potentially explains visual habituation to distortions of spectacles.