Hindbrain modules differentially transform activity of single collicular neurons to coordinate movements.

Seemingly simple behaviors such as swatting a mosquito or glancing at a signpost involve the precise coordination of multiple body parts. Neural control of coordinated movements is widely thought to entail transforming a desired overall displacement into displacements for each body part. Here we reveal a different logic implemented in the mouse gaze system. Stimulating superior colliculus (SC) elicits head movements with stereotyped displacements but eye movements with stereotyped endpoints. This is achieved by individual SC neurons whose branched axons innervate modules in medulla and pons that drive head movements with stereotyped displacements and eye movements with stereotyped endpoints, respectively. Thus, single neurons specify a mixture of endpoints and displacements for different body parts, not overall displacement, with displacements for different body parts computed at distinct anatomical stages. Our study establishes an approach for unraveling motor hierarchies and identifies a logic for coordinating movements and the resulting pose.

Sensory tuning in neuronal movement commands.

Movement control is critical for successful interaction with our environment. However, movement does not occur in complete isolation of sensation, and this is particularly true of eye movements. Here, we show that the neuronal eye movement commands emitted by the superior colliculus (SC), a structure classically associated with oculomotor control, encompass a robust visual sensory representation of eye movement targets. Thus, similar saccades toward different images are associated with different saccade-related "motor" bursts. Such sensory tuning in SC saccade motor commands appeared for all image manipulations that we tested, from simple visual features to real-life object images, and it was also strongest in the most motor neurons in the deeper collicular layers. Visual-feature discrimination performance in the motor commands was also stronger than in visual responses. Comparing SC motor command feature discrimination performance to that in the primary visual cortex during steady-state gaze fixation revealed that collicular motor bursts possess a reliable perisaccadic sensory representation of the peripheral saccade target's visual appearance, exactly when retinal input is expected to be most uncertain. Our results demonstrate that SC neuronal movement commands likely serve a fundamentally sensory function.

Parametric information about eye movements is sent to the ears.

Eye movements alter the relationship between the visual and auditory spatial scenes. Signals related to eye movements affect neural pathways from the ear through auditory cortex and beyond, but how these signals contribute to computing the locations of sounds with respect to the visual scene is poorly understood. Here, we evaluated the information contained in eye movement-related eardrum oscillations (EMREOs), pressure changes recorded in the ear canal that occur in conjunction with simultaneous eye movements. We show that EMREOs contain parametric information about horizontal and vertical eye displacement as well as initial/final eye position with respect to the head. The parametric information in the horizontal and vertical directions can be modeled as combining linearly, allowing accurate prediction of the EMREOs associated with oblique (diagonal) eye movements. Target location can also be inferred from the EMREO signals recorded during eye movements to those targets. We hypothesize that the (currently unknown) mechanism underlying EMREOs could impose a two-dimensional eye-movement-related transfer function on any incoming sound, permitting subsequent processing stages to compute the positions of sounds in relation to the visual scene.

Synchronous spiking of cerebellar Purkinje cells during control of movements.

SignificanceThe information that one region of the brain transmits to another is usually viewed through the lens of firing rates. However, if the output neurons could vary the timing of their spikes, then, through synchronization, they would spotlight information that may be critical for control of behavior. Here we report that, in the cerebellum, Purkinje cell populations that share a preference for error convey, to the nucleus, when to decelerate the movement, by reducing their firing rates and temporally synchronizing the remaining spikes.

Peri-Saccadic Orientation Identification Performance and Visual Neural Sensitivity Are Higher in the Upper Visual Field.

Visual neural processing is distributed among a multitude of sensory and sensory-motor brain areas exhibiting varying degrees of functional specializations and spatial representational anisotropies. Such diversity raises the question of how perceptual performance is determined, at any one moment in time, during natural active visual behavior. Here, exploiting a known dichotomy between the primary visual cortex (V1) and superior colliculus (SC) in representing either the upper or lower visual fields, we asked whether peri-saccadic orientation identification performance is dominated by one or the other spatial anisotropy. Humans (48 participants, 29 females) reported the orientation of peri-saccadic upper visual field stimuli significantly better than lower visual field stimuli, unlike their performance during steady-state gaze fixation, and contrary to expected perceptual superiority in the lower visual field in the absence of saccades. Consistent with this, peri-saccadic superior colliculus visual neural responses in two male rhesus macaque monkeys were also significantly stronger in the upper visual field than in the lower visual field. Thus, peri-saccadic orientation identification performance is more in line with oculomotor, rather than visual, map spatial anisotropies.SIGNIFICANCE STATEMENT Different brain areas respond to visual stimulation, but they differ in the degrees of functional specializations and spatial anisotropies that they exhibit. For example, the superior colliculus (SC) both responds to visual stimulation, like the primary visual cortex (V1), and controls oculomotor behavior. Compared with the primary visual cortex, the superior colliculus exhibits an opposite pattern of upper/lower visual field anisotropy, being more sensitive to the upper visual field. Here, we show that human peri-saccadic orientation identification performance is better in the upper compared with the lower visual field. Consistent with this, monkey superior colliculus visual neural responses to peri-saccadic stimuli follow a similar pattern. Our results indicate that peri-saccadic perceptual performance reflects oculomotor, rather than visual, map spatial anisotropies.

Compression of time in double-step saccades.

Temporal intervals appear compressed at the time of saccades. Here, I asked if saccadic compression of time is related to motor planning or to saccade execution. To dissociate saccade motor planning from its execution, I used the double-step paradigm, in which subjects have to perform two horizontal saccades successively. At various times around the saccade sequence, I presented two large horizontal bars, which marked an interval lasting 100 ms. After 700 ms, a second temporal interval was presented, varying in duration across trials. Subjects were required to judge which interval appeared shorter. I found that during the first saccades in the double-step paradigm, temporal intervals were compressed. Maximum temporal compression coincided with saccade onset. Around the time of the second saccade, I found temporal compression as well, however, the time of maximum compression preceded saccade onset by about 70 ms. I compared the magnitude and time of temporal compression between double-step saccades and amplitude-matched single saccades, which I measured separately. Although I found no difference in time compression magnitude, the time when maximum compression occurred differed significantly. I conclude that the temporal shift of time compression in double-step saccades demonstrates the influence of saccade motor planning on time perception.NEW & NOTEWORTHY Visually defined temporal intervals appear compressed at the time of saccades. Here, I tested time perception during double-step saccades dissociating saccade planning from execution. Although around the time of the first saccade, peak compression was found at saccade onset, compression around the time of the second saccade peaked 70 ms before saccade onset. The results suggest that saccade motor planning influences time perception.

Inhibitory tagging both speeds and strengthens saccade target selection in the superior colliculus during visual search.

It has been suggested that, during difficult visual search tasks involving time pressure and multiple saccades, inhibitory tagging helps to facilitate efficient saccade target selection by reducing responses to objects in the scene once they have been searched and rejected. The superior colliculus (SC) is a midbrain structure involved in target selection, and recent findings suggest an influence of inhibitory tagging on SC activity. Precisely how, and by how much, inhibitory tagging influences target selection by SC neurons, however, is unclear. The purpose of this study, therefore, was to characterize and quantify the influence of inhibitory tagging on target selection in the SC. Rhesus monkeys performed a visual search task involving time pressure and multiple saccades. Early in the fixation period between saccades in the context of this task, a subset of SC neurons reliably discriminated the stimulus selected as the next saccade goal, consistent with a role in target selection. Discrimination occurred earlier and was more robust, however, when unselected stimuli in the search array had been previously fixated on the same trial. This indicates that inhibitory tagging both speeds and strengthens saccade target selection in the SC during multisaccade search. The results provide constraints on models of target selection based on SC activity.NEW & NOTEWORTHY An important aspect of efficient behavior during difficult, time-limited visual search tasks is the efficient selection of sequential saccade targets. Inhibitory tagging, i.e., a reduction of neural activity associated with previously fixated objects, may help to facilitate such efficient selection by modulating the selection process in the superior colliculus (SC). In this study, we characterized and quantified this modulation and found that, indeed, inhibitory tagging both speeds and strengthens target selection in the SC.

Influence of gaze, vision, and memory on hand kinematics in a placement task.

People usually reach for objects to place them in some position and orientation, but the placement component of this sequence is often ignored. For example, reaches are influenced by gaze position, visual feedback, and memory delays, but their influence on object placement is unclear. Here, we tested these factors in a task where participants placed and oriented a trapezoidal block against two-dimensional (2-D) visual templates displayed on a frontally located computer screen. In experiment 1, participants matched the block to three possible orientations: 0° (horizontal), +45° and -45°, with gaze fixated 10° to the left/right. The hand and template either remained illuminated (closed-loop), or visual feedback was removed (open-loop). Here, hand location consistently overshot the template relative to gaze, especially in the open-loop task; likewise, orientation was influenced by gaze position (depending on template orientation and visual feedback). In experiment 2, a memory delay was added, and participants sometimes performed saccades (toward, away from, or across the template). In this task, the influence of gaze on orientation vanished, but location errors were influenced by both template orientation and final gaze position. Contrary to our expectations, the previous saccade metrics also impacted placement overshoot. Overall, hand orientation was influenced by template orientation in a nonlinear fashion. These results demonstrate interactions between gaze and orientation signals in the planning and execution of hand placement and suggest different neural mechanisms for closed-loop, open-loop, and memory delay placement.NEW & NOTEWORTHY Eye-hand coordination studies usually focus on object acquisition, but placement is equally important. We investigated how gaze position influences object placement toward a 2-D template with different levels of visual feedback. Like reach, placement overestimated goal location relative to gaze and was influenced by previous saccade metrics. Gaze also modulated hand orientation, depending on template orientation and level of visual feedback. Gaze influence was feedback-dependent, with location errors having no significant effect after a memory delay.

Eye-hand coordination all the way: from discrete to continuous hand movements.

The differentiation between continuous and discrete actions is key for behavioral neuroscience. Although many studies have characterized eye-hand coordination during discrete (e.g., reaching) and continuous (e.g., pursuit tracking) actions, all these studies were conducted separately, using different setups and participants. In addition, how eye-hand coordination might operate at the frontier between discrete and continuous movements remains unexplored. Here we filled these gaps by means of a task that could elicit different movement dynamics. Twenty-eight participants were asked to simultaneously track with their eyes and a joystick a visual target that followed an unpredictable trajectory and whose position was updated at different rates (from 1.5 to 240 Hz). This procedure allowed us to examine actions ranging from discrete point-to-point movements (low refresh rate) to continuous pursuit (high refresh rate). For comparison, we also tested a manual tracking condition with the eyes fixed and a pure eye tracking condition (hand fixed). The results showed an abrupt transition between discrete and continuous hand movements around 3 Hz contrasting with a smooth trade-off between fixations and smooth pursuit. Nevertheless, hand and eye tracking accuracy remained strongly correlated, with each of these depending on whether the other effector was recruited. Moreover, gaze-cursor distance and lag were smaller when eye and hand performed the task conjointly than separately. Altogether, despite some dissimilarities in eye and hand dynamics when transitioning between discrete and continuous movements, our results emphasize that eye-hand coordination continues to smoothly operate and support the notion of synergies across eye movement types.NEW & NOTEWORTHY The differentiation between continuous and discrete actions is key for behavioral neuroscience. By using a visuomotor task in which we manipulate the target refresh rate to trigger different movement dynamics, we explored eye-hand coordination all the way from discrete to continuous actions. Despite abrupt changes in hand dynamics, eye-hand coordination continues to operate via a gradual trade-off between fixations and smooth pursuit, an observation confirming the notion of synergies across eye movement types.

Navigating Visual Challenges: How Parkinson's Disease Alters Cognitive Priorities in Visual Search.

OBJECTIVE: Parkinson's disease (PD) hampers visual search tasks such as reading, driving, and navigation. We examined expectations from past experiences, guiding cognition and contextual priors, on visual search in PD. METHODS: We compared eye movements as PD and healthy participants searched for a hidden object (target) in cluttered real-world scenes. RESULTS: PD participants prolonged fixation on high-probability (high-prior) locations for the target, consistent across expected and unexpected scenario. Such emphasis on contextual visual priors, evidenced by high fixation duration on high-probability areas, was beneficial when the target was at the expected location but presented challenges when the target was situated in an unlikely place. CONCLUSION: This study contributes to understanding how PD impacts visual search behavior and cognitive processing. The findings indicate that PD alters attention allocation and visual processing by affecting the utilization of contextual visual priors. It provides insights for potential interventions targeting visuo-cognitive deficits in PD patients. Published 2024. This article is a U.S. Government work and is in the public domain in the USA.

Catch-Up Saccades in Vestibular Hypofunction: A Contribution of the Cerebellum?

Long-term deficits of the vestibulo-ocular reflex (VOR) elicited by head rotation can be partially compensated by catch-up saccades (CuS). These saccades are initially visually guided, but their latency can greatly decrease resulting in short latency CuS (SL-CuS). It is still unclear what triggers these CuS and what are the underlying neural circuits. In this study, we aimed at evaluating the impact of cerebellar pathology on CuS by comparing their characteristics between two groups of patients with bilateral vestibular hypofunction, with or without additional cerebellar dysfunction. We recruited 12 patients with both bilateral vestibular hypofunction and cerebellar dysfunction (BVH-CD group) and 12 patients with isolated bilateral vestibular hypofunction (BVH group). Both groups were matched for age and residual VOR gain. Subjects underwent video head impulse test recording of the horizontal semicircular canals responses as well as recording of visually guided saccades in the step, gap, and overlap paradigms. Latency and gain of the different saccades were calculated. The mean age for BVH-CD and BVH was, respectively, 67.8 and 67.2 years, and the mean residual VOR gain was, respectively, 0.24 and 0.26. The mean latency of the first catch-up saccade was significantly longer for the BVH-CD group than that for the BVH group (204 ms vs 145 ms, p < 0.05). There was no significant difference in the latency of visually guided saccades between the two groups, for none of the three paradigms. The gain of covert saccades tended to be lower in the BVH-CD group than in BVH group (t test; p = 0.06). The mean gain of the 12° or 20° visually guided saccades were not different in both groups. Our results suggest that the cerebellum plays a role in the generation of compensatory SL-CuS observed in BVH patients.

Eyes as a window to brain pathology in parkinson's disease: a narrative review.

There is a renewed interest on eye movements analysis and retinal alterations in Parkinson's disease. This may identify markers for at-risk subpopulation, early diagnosis and evolutive profiles for research or personalized medicine.

Effector-selective modulation of the effective connectivity within frontoparietal circuits during visuomotor tasks.

Despite extensive research, the functional architecture of the subregions of the dorsal posterior parietal cortex (PPC) involved in sensorimotor processing is far from clear. Here, we draw a thorough picture of the large-scale functional organization of the PPC to disentangle the fronto-parietal networks mediating visuomotor functions. To this aim, we reanalyzed available human functional magnetic resonance imaging data collected during the execution of saccades, hand, and foot pointing, and we combined individual surface-based activation, resting-state functional connectivity, and effective connectivity analyses. We described a functional distinction between a more lateral region in the posterior intraparietal sulcus (lpIPS), preferring saccades over pointing and coupled with the frontal eye fields (FEF) at rest, and a more medial portion (mpIPS) intrinsically correlated to the dorsal premotor cortex (PMd). Dynamic causal modeling revealed feedforward-feedback loops linking lpIPS with FEF during saccades and mpIPS with PMd during pointing, with substantial differences between hand and foot. Despite an intrinsic specialization of the action-specific fronto-parietal networks, our study reveals that their functioning is finely regulated according to the effector to be used, being the dynamic interactions within those networks differently modulated when carrying out a similar movement (i.e. pointing) but with distinct effectors (i.e. hand and foot).

Visual, delay, and oculomotor timing and tuning in macaque dorsal pulvinar during instructed and free choice memory saccades.

Causal perturbations suggest that primate dorsal pulvinar plays a crucial role in target selection and saccade planning, though its basic neuronal properties remain unclear. Some functional aspects of dorsal pulvinar and interconnected frontoparietal areas-e.g. ipsilesional choice bias after inactivation-are similar. But it is unknown if dorsal pulvinar shares oculomotor properties of cortical circuitry, in particular delay and choice-related activity. We investigated such properties in macaque dorsal pulvinar during instructed and free-choice memory saccades. Most recorded units showed visual (12%), saccade-related (30%), or both types of responses (22%). Visual responses were primarily contralateral; diverse saccade-related responses were predominantly post-saccadic with a weak contralateral bias. Memory delay and pre-saccadic enhancement was infrequent (11-9%)-instead, activity was often suppressed during saccade planning (25%) and further during execution (15%). Surprisingly, only few units exhibited classical visuomotor patterns combining cue and continuous delay activity or pre-saccadic ramping; moreover, most spatially-selective neurons did not encode the upcoming decision during free-choice delay. Thus, in absence of a visible goal, the dorsal pulvinar has a limited role in prospective saccade planning, with patterns partially complementing its frontoparietal partners. Conversely, prevalent visual and post-saccadic responses imply its participation in integrating spatial goals with processing across saccades.

Saccades and presaccadic stimulus repetition alter cortical network topology and dynamics: evidence from EEG and graph theoretical analysis.

Parietal and frontal cortex are involved in saccade generation, and their output signals modify visual signals throughout cortex. Local signals associated with these interactions are well described, but their large-scale progression and network dynamics are unknown. Here, we combined source localized electroencephalography (EEG) and graph theory analysis (GTA) to understand how saccades and presaccadic visual stimuli interactively alter cortical network dynamics in humans. Twenty-one participants viewed 1-3 vertical/horizontal grids, followed by grid with the opposite orientation just before a horizontal saccade or continued fixation. EEG signals from the presaccadic interval (or equivalent fixation period) were used for analysis. Source localization-through-time revealed a rapid frontoparietal progression of presaccadic motor signals and stimulus-motor interactions, with additional band-specific modulations in several frontoparietal regions. GTA analysis revealed a saccade-specific functional network with major hubs in inferior parietal cortex (alpha) and the frontal eye fields (beta), and major saccade-repetition interactions in left prefrontal (theta) and supramarginal gyrus (gamma). This network showed enhanced segregation, integration, synchronization, and complexity (compared with fixation), whereas stimulus repetition interactions reduced synchronization and complexity. These cortical results demonstrate a widespread influence of saccades on both regional and network dynamics, likely responsible for both the motor and perceptual aspects of saccades.

Monitoring the acute and subacute recovery of cognitive ocular motor changes after a sports-related concussion.

Identifying when recovery from a sports-related concussion (SRC) has occurred remains a challenge in clinical practice. This study investigated the utility of ocular motor (OM) assessment to monitor recovery post-SRC between sexes and compared to common clinical measures. From 139 preseason baseline assessments (i.e. before they sustained an SRC), 18 (12 males, 6 females) consequent SRCs were sustained and the longitudinal follow-ups were collected at 2, 6, and 13 days post-SRC. Participants completed visually guided, antisaccade (AS), and memory-guided saccade tasks requiring a saccade toward, away from, and to a remembered target, respectively. Changes in latency (processing speed), visual-spatial accuracy, and errors were measured. Clinical measures included The Sports Concussion Assessment Tool, King-Devick test, Stroop task, and Digit span. AS latency was significantly longer at 2 days and returned to baseline by 13-days post-SRC in females only (P < 0.001). Symptom numbers recovered from 2 to 6 days and 13 days (P < 0.05). Persistently poorer AS visual-spatial accuracy was identified at 2, 6 and 13 days post-SRC (P < 0.05) in both males and females but with differing trajectories. Clinical measures demonstrated consistent improvement reminiscent of practice effects. OM saccade assessment may have improved utility in tracking recovery compared to conventional measures and between sexes.

When you look at your past: Eye movement during autobiographical retrieval.

Until recently, little was known about whether or how autobiographical memory (i.e., memory of personal information) activates eye movement. This issue is now being addressed by several studies demonstrating not only how autobiographical memory activates eye movement, but also how eye movement influences the characteristics of autobiographical retrieval. This paper summarizes this research and presents a hypothesis according to which fixations and saccades during autobiographical retrieval mirror the construction of the visual image of the retrieved event. This hypothesis suggests that eye movements during autobiographical retrieval mirror the attempts of the visual system to generate and manipulate mental representations of autobiographical retrieval. It offers a theoretical framework for a burgeoning area of research that provides a rigorous behavioral evaluation of the phenomenological experience of memory.

Oculomotor Abnormalities and Aberrant Neuro-Developmental Markers: Composite Endophenotype for Bipolar I Disorder: Anomalies Oculomotrices et Marqueurs Neuro-Développementaux Aberrants : Endophénotype Composite du Trouble Bipolaire I.

BACKGROUND: Neurological soft signs (NSSs), minor physical anomalies (MPAs), and oculomotor abnormalities were plausible biomarkers in bipolar disorder (BD). However, specific impairments in these markers in patients after the first episode mania (FEM), in comparison with first-degree relatives (high risk [HR]) of BD and healthy subjects (health control [HC]) are sparse. AIM OF THE STUDY: This study aimed at examining NSSs, MPAs, and oculomotor abnormalities in remitted adult subjects following FEM and HR subjects in comparison with matched healthy controls. Investigated when taken together, could serve as composite endophenotype for BD. METHODS: NSSs, MPAs, and oculomotor abnormalities were evaluated in FEM (n = 31), HR (n = 31), and HC (n = 30) subjects, matched for age (years) (p = 0.44) and sex (p = 0.70) using neurological evaluation scale, Waldrop's physical anomaly scale and eye tracking (SPEM) and antisaccades (AS) paradigms, respectively. RESULTS: Significant differences were found between groups on NSSs, MPAs, and oculomotor parameters. Abnormalities are higher in FEM subjects compared to HR and HC subjects. Using linear discriminant analysis, all 3 markers combined accurately classified 72% of the original 82 subjects (79·2% BD, 56·70% HR, and 82·1% HC subjects). CONCLUSIONS: AS and SPEM could enhance the utility of NSSs, and MPAs as markers for BD. The presence of these abnormalities in FEM suggests their role in understanding the etiopathogenesis of BD in patients who are in the early course of illness. These have the potential to be composite endophenotypes and have further utility in early identification in BD.

Eye movement abnormalities and Atypical Neurodevelopmental markers as Composite Measurable components in the pathway between disease manifestation and genetics in Bipolar I Disorder.

Saccade Latency and Metrics in the Interleaved Pro- and Anti-Saccade Task in Open Skill Sports Athletes.

Evidence has demonstrated that athletes exhibit superior cognitive performance associated with executive control. In the oculomotor system, this function has been examined using the interleaved pro-saccade and anti-saccade task (IPAST), wherein participants, prior to target appearance, are instructed to either automatically look at the peripheral target (pro-saccade) or suppress the automatic response and voluntarily look in the opposite direction (anti-saccade). While the IPAST has provided much insight into sensorimotor and inhibitory processing, it has yet to be performed in athletes. Moreover, limited research has examined saccade metrics in athletes. Here, we examined saccade latency and movement kinematics in the IPAST among athletes (N = 40) and nonathletes (NON) (N = 40). Higher direction error rates were obtained in the anti-saccade compared to the pro-saccade condition, with no differences between athletes and NON noted. Significantly faster saccade latencies were observed in athletes compared to NON in both conditions, in addition to faster pro-saccades compared to anti-saccades. Furthermore, athletes showed significantly higher frequencies and faster latencies of express saccades compared to NON in correct pro-saccades. Additionally, athletes exhibited significantly faster latencies of express saccades compared to NON in erroneous anti-saccades. Differences in saccade metrics between athletes and NON were not seen. Overall, these findings demonstrate that athletes display altered saccade performance likely associated with sensorimotor and preparatory processing, highlighting the potential of using IPAST to objectively investigate sensorimotor and cognitive functions in athletes.

False memory-guided eye movements: insights from a DRM-Saccade paradigm.

The Deese-Roediger and McDermott (DRM) paradigm and visually guided saccade tasks are both prominent research tools in their own right. This study introduces a novel DRM-Saccade paradigm, merging both methodologies. We used rule-based saccadic eye movements whereby participants were presented with items at test and were asked to make a saccade to the left or right of the item to denote a recognition or non-recognition decision. We measured old/new recognition decisions and saccadic latencies. Experiment 1 used a pro/anti saccade task to a single target. We found slower saccadic latencies for correct rejection of critical lures, but no latency difference between correct recognition of studied items and false recognition of critical lures. Experiment 2 used a two-target saccade task and also measured corrective saccades. Findings corroborated those from Experiment 1. Participants adjusted their initial decisions to increase accurate recognition of studied items and rejection of unrelated lures but there were no such corrections for critical lures. We argue that rapid saccades indicate cognitive processing driven by familiarity thresholds. These occur before slower source-monitoring is able to process any conflict. The DRM-Saccade task could effectively track real-time cognitive resource use during recognition decisions.