A distributed saccade-associated network encodes high velocity conjugate and monocular eye movements in the zebrafish hindbrain.
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ABSTRACT:
SUBMITTER: Leyden C
PROVIDER: S-EPMC8209155 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BACKGROUND:The oculomotor integrator (OI) in the vertebrate hindbrain transforms eye velocity input into persistent position coding output, which plays a crucial role in retinal image stability. For a mechanistic understanding of the integrator function and eye position control, knowledge about the tuning of the OI and other oculomotor nuclei is needed. Zebrafish are increasingly used to study integrator function and sensorimotor circuits, yet the precise neuronal tuning to motor variables remains uncharacterized. RESULTS:Here, we recorded cellular calcium signals while evoking monocular and binocular optokinetic eye movements at different slow-phase eye velocities. Our analysis reveals the anatomical distributions of motoneurons and internuclear neurons in the nucleus abducens as well as those of oculomotor neurons in caudally adjacent hindbrain volumes. Each neuron is tuned to eye position and/or velocity to variable extents and is only activated after surpassing particular eye position and velocity thresholds. While the abducens (rhombomeres 5/6) mainly codes for eye position, in rhombomeres 7/8, a velocity-to-position coding gradient exists along the rostro-caudal axis, which likely corresponds to the oculomotor structures storing velocity and position, and is in agreement with a feedforward mechanism of persistent activity generation. Position encoding neurons are recruited at eye position thresholds distributed across the behaviourally relevant dynamic range, while velocity-encoding neurons have more centred firing thresholds for velocity. In the abducens, neurons coding exclusively for one eye intermingle with neurons coding for both eyes. Many of these binocular neurons are preferentially active during conjugate eye movements and less active during monocular eye movements. This differential recruitment during monocular versus conjugate tasks represents a functional diversification in the final common motor pathway. CONCLUSIONS:We localized and functionally characterized the repertoire of oculomotor neurons in the zebrafish hindbrain. Our findings provide evidence for a mixed but task-specific binocular code and suggest that generation of persistent activity is organized along the rostro-caudal axis in the hindbrain.
| S-EPMC6936144 | biostudies-literature
Project description:Background: Clinical and laboratory assessment of people with mild traumatic brain injury (mTBI) indicate impairments in eye movements. These tests are typically done in a static, seated position. Recently, the use of mobile eye-tracking systems has been proposed to quantify subtle deficits in eye movements and visual sampling during different tasks. However, the impact of mTBI on eye movements during functional tasks such as walking remains unknown. Objective: Evaluate differences in eye-tracking measures collected during gait between healthy controls (HC) and patients in the sub-acute stages of mTBI recovery and to determine if there are associations between eye-tracking measures and gait speed. Methods: Thirty-seven HC participants and 67individuals with mTBI were instructed to walk back and forth over 10-m, at a comfortable self-selected speed. A single 1-min trial was performed. Eye-tracking measures were recorded using a mobile eye-tracking system (head-mounted infra-red Tobbii Pro Glasses 2, 100 Hz, Tobii Technology Inc. VA, United States). Eye-tracking measures included saccadic (frequency, mean and peak velocity, duration and distance) and fixation measurements (frequency and duration). Gait was assessed using six inertial sensors (both feet, sternum, right wrist, lumbar vertebrae and the forehead) and gait velocity was selected as the primary outcome. General linear model was used to compare the groups and association between gait and eye-tracking outcomes were explored using partial correlations. Results: Individuals with mTBI showed significantly reduced saccade frequency (p = 0.016), duration (p = 0.028) and peak velocity (p = 0.032) compared to the HC group. No significant differences between groups were observed for the saccade distance, fixation measures and gait velocity (p > 0.05). A positive correlation was observed between saccade duration and gait velocity only for participants with mTBI (p = 0.025). Conclusion: Findings suggest impaired saccadic eye movement, but not fixations, during walking in individuals with mTBI. These findings have implications in real-world function including return to sport for athletes and return to duty for military service members. Future research should investigate whether or not saccade outcomes are influenced by the time after the trauma and rehabilitation.
| S-EPMC8602343 | biostudies-literature
Project description:BackgroundThe anti-saccade task, when people must respond in the direction opposite to a visual stimulus, has been used as a marker of operation of the frontal cortical oculomotor area. However, early development of oculomotor control has been little studied with the infant anti-saccade paradigm, and a few studies did not recognize anti-saccades in infants in light of the results of adult anti-saccade. Since the characteristics of infant eye movements are little known, applying the criteria used in adult study is by no means the best way to study infant anti-saccade. As it is indicated that coordinated eye and head movements often enable infants to control the direction of their gaze, head movements should be examined as an infant orienting response. The aim of this study was to address how infants used eye and head movements during the anti-saccade paradigm. To distinguish infants' responses, we also investigated eye and head movements during a task for an inhibition of return. Inhibition of return, in which delayed responses occur in the direction to which attention had previously been oriented, has been thought to mark activity of the superior colliculus. Since the superior colliculus is thought to develop much earlier in life than the frontal lobes, we thought it useful to compare these task performances during infancy.MethodsInfants were divided into three groups according to age. Anti-saccade and inhibition-of-return tasks were given. Their eye and head movements during tasks were independently recorded by the corneal reflection method in the head-free condition.ResultsYounger infants tended to initiate eye movement less than older ones in both tasks. In the anti-saccade task, responses opposite to the cue tended to show longer latency than responses to the cue. Infants made faster responses toward the side opposite the cue when it was to the right than when it was left of fixation. Regarding the comparison of responses toward the side opposite the cue between two tasks, the leftward eye movement was faster than the leftward head movements in the inhibition-of-return task, while no difference of latency was observed between eye and head movements in the anti-saccade task. A qualitative analysis of the trajectory of these responses revealed that head movement trajectories were steeper in the anti-saccade than in the inhibition-of-return task.ConclusionYounger infants move head and eyes together, with head movements frequently starting first. On the other hand, both the leftward latency difference between eye and head and gentle trajectories of head in inhibition of return indicate that eye movements are more predominant over head movements in the inhibition-of-return task than in the anti-saccade task. This would suggest an earlier developing inhibition-of-return mechanism.
| S-EPMC1783854 | biostudies-literature
Project description:BackgroundVestibular reflexes coordinate movements or sensory input with changes in body or head position. Vestibular-evoked responses that involve the extraocular muscles include the vestibulo-ocular reflex (VOR), a compensatory eye movement to stabilize retinal images. Although an angular VOR attributable to semicircular canal stimulation was reported to be absent in free-swimming zebrafish larvae, recent studies reveal that vestibular-induced eye movements can be evoked in zebrafish larvae by both static tilts and dynamic rotations that tilt the head with respect to gravity.ResultsWe have determined herein the basis of sensitivity of the larval eye movements with respect to vestibular stimulus, developmental stage, and sensory receptors of the inner ear. For our experiments, video recordings of larvae rotated sinusoidally at 0.25 Hz were analyzed to quantitate eye movements under infrared illumination. We observed a robust response that appeared as early as 72 hours post fertilization (hpf), which increased in amplitude over time. Unlike rotation about an earth horizontal axis, rotation about an earth vertical axis at 0.25 Hz did not evoke eye movements. Moreover, vestibular-induced responses were absent in mutant cdh23 larvae and larvae lacking anterior otoliths.ConclusionsOur results provide evidence for a functional vestibulo-oculomotor circuit in 72 hpf zebrafish larvae that relies upon sensory input from anterior/utricular otolith organs.
| S-EPMC2941499 | biostudies-literature
Project description:The Hnf1b transcription factor acts during formation of rhombomeres (r) 5 and 6 in the hindbrain. To determine if hnf1b is absolutely required in r5/r6, we examined the hnf1b(hi2169) and hnf1b(hi1843) retroviral insertion alleles. Hnf1b(hi2169) shows highly variable residual expression of several genes in r5/r6, but this is not due to full-length hnf1b transcripts persisting in hnf1b(hi2169) embryos, nor to hnf1bl, a novel hnf1 family member expressed in r5 that we identified. Instead, we find evidence for a virus-hnf1b fusion transcript in hnf1b(hi2169) embryos and demonstrate that morpholino-mediated knockdown of this transcript leads to near-undetectable r5 gene expression. The hnf1b(hi1843) allele has a more severe phenotype with near-undetectable expression of r5/r6 genes. We next examined if hoxb1b, which functions upstream of hnf1b in r5/r6 formation, can induce expression of r5/r6 genes in hnf1b mutants. We find that microinjected hoxb1b mRNA induces ectopic gene expression anterior to the hindbrain in hnf1b(hi2169) and hnf1b(hi1843) embryos, but cannot restore gene expression in r5/r6 of the mutants. We conclude that hnf1b(hi2169) is hypomorphic to hnf1b(hi1843) and that, while hnf1b is required for r5/r6 gene expression in the hindbrain, r5/r6 gene expression can be experimentally induced independently of hnf1b anterior to the hindbrain.
| S-EPMC2761071 | biostudies-literature
Project description:BACKGROUND:Activity in neurons drives afferent competition that is critical for the refinement of nascent neural circuits. In ferrets, when an eye is lost in early development, surviving retinogeniculate afferents from the spared eye spread across the thalamus in a manner that is dependent on spontaneous retinal activity. However, how this spontaneous activity, also known as retinal waves, might dynamically regulate afferent terminal targeting remains unknown. METHODS:We recorded retinal waves from retinae ex vivo using multi-electrode arrays. Retinae came from ferrets who were binocular or who had one eye surgically removed at birth. Linear mixed effects models were used to investigate the effects of early monocular enucleation on retinal wave activity. RESULTS:When an eye is removed at birth, spontaneous bursts of action potentials by retinal ganglion cells (RGCs) in the surviving eye are shorter in duration. The shortening of RGC burst duration results in decreased pairwise RGC correlations across the retina and is associated with the retinal wave-dependent spread of retinogeniculate afferents previously reported in enucleates. CONCLUSION:Our findings show that removal of the competing eye modulates retinal waves and could underlie the dynamic regulation of competition-based refinement during retinogeniculate development.
| S-EPMC5866508 | biostudies-literature
Project description:Most people easily learn to recognize new faces and places, and with more extensive practice they can become experts at visual tasks as complex as radiological diagnosis and action video games. Such perceptual plasticity has been thoroughly studied in the context of training paradigms that require constant fixation. In contrast, when observers learn under more natural conditions, they make frequent saccadic eye movements. Here we show that such eye movements can play an important role in visual learning. Observers performed a task in which they executed a saccade while discriminating the motion of a cued visual stimulus. Additional stimuli, presented simultaneously with the cued one, permitted an assessment of the perceptual integration of information across visual space. Consistent with previous results on perisaccadic remapping [M. Szinte, D. Jonikaitis, M. Rolfs, P. Cavanagh, H. Deubel, J. Neurophysiol. 116, 1592-1602 (2016)], most observers preferentially integrated information from locations representing the presaccadic and postsaccadic retinal positions of the cue. With extensive training on the saccade task, these observers gradually acquired the ability to perform similar motion integration without making eye movements. Importantly, the newly acquired pattern of spatial integration was determined by the metrics of the saccades made during training. These results suggest that oculomotor influences on visual processing, long thought to subserve the function of perceptual stability, also play a role in visual plasticity.
| S-EPMC7149482 | biostudies-literature
Project description:To better understand how individual genes and experience influence behavior, the role of a single homeotic unit, hoxb4a, was comprehensively analyzed in vivo by clonal and retrograde fluorescent labeling of caudal hindbrain neurons in a zebrafish enhancer-trap YFP line. A quantitative spatiotemporal neuronal atlas showed hoxb4a activity to be highly variable and mosaic in rhombomere 7-8 reticular, motoneuronal and precerebellar nuclei with expression decreasing differentially in all subgroups through juvenile stages. The extensive Hox mosaicism and widespread pleiotropism demonstrate that the same transcriptional protein plays a role in the development of circuits that drive behaviors from autonomic through motor function including cerebellar regulation. We propose that the continuous presence of hoxb4a positive neurons may provide a developmental plasticity for behavior-specific circuits to accommodate experience- and growth-related changes. Hence, the ubiquitous hoxb4a pleitropism and modularity likely offer an adaptable transcriptional element for circuit modification during both growth and evolution.
| S-EPMC2693931 | biostudies-literature
Project description:The ability to recall a detailed event from a simple reminder is supported by pattern completion, a cognitive operation performed by the hippocampus wherein existing mnemonic representations are retrieved from incomplete input. In behavioral studies, pattern completion is often inferred through the false endorsement of lure (i.e., similar) items as old. However, evidence that such a response is due to the specific retrieval of a similar, previously encoded item is severely lacking. We used eye movement (EM) monitoring during a partial-cue recognition memory task to index reinstatement of lure images behaviorally via the recapitulation of encoding-related EMs or gaze reinstatement. Participants reinstated encoding-related EMs following degraded retrieval cues and this reinstatement was negatively correlated with accuracy for lure images, suggesting that retrieval of existing representations (i.e., pattern completion) underlies lure false alarms. Our findings provide evidence linking gaze reinstatement and pattern completion and advance a functional role for EMs in memory retrieval.
| S-EPMC7084073 | biostudies-literature
Project description:In the natural world, the brain must handle inherent delays in visual processing. This is a problem particularly during dynamic tasks. A possible solution to visuo-motor delays is prediction of a future state of the environment based on the current state and properties of the environment learned from experience. Prediction is well known to occur in both saccades and pursuit movements and is likely to depend on some kind of internal visual model as the basis for this prediction. However, most evidence comes from controlled laboratory studies using simple paradigms. In this study, we examine eye movements made in the context of demanding natural behavior, while playing squash. We show that prediction is a pervasive component of gaze behavior in this context. We show in addition that these predictive movements are extraordinarily precise and operate continuously in time across multiple trajectories and multiple movements. This suggests that prediction is based on complex dynamic visual models of the way that balls move, accumulated over extensive experience. Since eye, head, arm, and body movements all co-occur, it seems likely that a common internal model of predicted visual state is shared by different effectors to allow flexible coordination patterns. It is generally agreed that internal models are responsible for predicting future sensory state for control of body movements. The present work suggests that model-based prediction is likely to be a pervasive component in natural gaze control as well.
| S-EPMC3328199 | biostudies-literature