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Brainstem Control of Saccadic Eye Movements
... Importantly, saccadic parameters are coupled to the activity of excitatory burst neurons (EBNs) in the brainstem. More specifically, peak saccade velocity is correlated with the maximum firing rate of EBNs, saccade duration is correlated with their burst duration, and the number of spikes in the burst is correlated with saccade amplitude (Fuchs et al., 1985;Galley, 1989;Sparks, 2002). Therefore, as the execution of saccades depends on the firing of brainstem neurons, any inhibition of these neurons should also be reflected in slower saccade velocities and longer saccade durations. ...
... Of interest, the SC also controls the execution of saccades in the brainstem (Sparks, 2002;Watanabe & Munoz, 2011). Therefore, it is possible, but yet unknown, that the motor inhibition thought to follow unexpected sounds may also affect the firing of EBNs, which is related to the peak velocity of saccades (Fuchs et al., 1985). If novel sounds affect the execution of saccades, then we should observe a reduction in their velocity and an increase in their duration. ...
... However, such inhibition would be expected to affect all oculomotor behaviour, including the execution of saccades. Because saccadic variables such as peak velocity are assumed to be closely correlated with the firing of brainstem neurons (e.g., Di Stasi et al., 2013;Fuchs et al., 1985), our results suggest that novel sounds do not affect the neural circuits that control the movement of the eyes during a saccade. While this result may appear at odds with Wessel and Aron's (2013) global motor suppression account, this suppression could be very time-sensitive and disappear by the time the eyes are in motion. ...
Novel or unexpected sounds that deviate from an otherwise repetitive sequence of the same sound cause behavioural distraction. Recent work has suggested that distraction also occurs during reading as fixation durations increased when a deviant sound was presented at the fixation onset of words. The present study tested the hypothesis that this increase in fixation durations occurs due to saccadic inhibition. This was done by manipulating the temporal onset of sounds relative to the fixation onset of words in the text. If novel sounds cause saccadic inhibition, they should be more distracting when presented during the second half of fixations when saccade programming usually takes place. Participants read single sentences and heard a 120 ms sound when they fixated five target words in the sentence. On most occasions (p= 0.9), the same sine wave tone was presented (“standard”), while on the remaining occasions (p= 0.1) a new sound was presented (“novel”). Critically, sounds were played either during the first half of the fixation (0 ms delay) or during the second half of the fixation (120 ms delay). Consistent with the saccadic inhibition hypothesis, novel sounds led to longer fixation durations in the 120 ms compared to the 0 ms delay condition. However, novel sounds did not generally influence the execution of the subsequent saccade. These results suggest that unexpected sounds have a rapid influence on saccade planning, but not saccade execution.
... Importantly, saccadic parameters are coupled to the activity of excitatory burst neurons (EBNs) in the brainstem. More specifically, peak saccade velocity is correlated with the maximum firing rate of EBNs, saccade duration is correlated with their burst duration, and the number of spikes in the burst is correlated with saccade amplitude (Fuchs, Kaneko, & Scudder, 1985;Galley, 1989;Sparks, 2002). Therefore, as the execution of saccades depends on the firing of brainstem neurons, any inhibition of these neurons should also be reflected in slower saccade velocities and longer saccade durations. ...
... Of interest, the SC also controls the execution of saccades in the brainstem (Sparks, 2002;Watanabe & Munoz, 2011). Therefore, it is possible, but yet unknown, that the motor inhibition thought to follow unexpected sounds may also affect the firing of EBNs, which is related to the peak velocity of saccades (Fuchs et al., 1985). If novel sounds affect the execution of saccades, then we should observe a reduction in their velocity and an increase in their duration. ...
... However, such inhibition would be expected to affect all oculomotor behaviour, including the execution of saccades. Because saccadic variables such as peak velocity are assumed to be closely correlated with the firing of brainstem neurons (e.g.,Di Stasi, Catena, Cañas, Macknik, & Martinez-Conde, 2013;Fuchs et al., 1985), our results suggest that novel sounds do not affect the neural circuits that control the movement of the eyes during a saccade. While this result may appear at odds withWessel and Aron's (2013) global motor suppression account, this suppression could be very timesensitive and disappear by the time the eyes are in motion. ...
Novel or unexpected sounds that deviate from an otherwise repetitive sequence of the same sound cause behavioural distraction. Recent work has suggested that distraction also occurs during reading as fixation durations increased when a deviant sound was presented at the fixation onset of words. The present study tested the hypothesis that this increase in fixation durations occurs due to saccadic inhibition. This was done by manipulating the temporal onset of sounds relative to the fixation onset of words in the text. If novel sounds cause saccadic inhibition, they should be more distracting when presented during the second half of fixations when saccade programming usually takes place. Participants read single sentences and heard a 120 ms sound when they fixated five target words in the sentence. On most occasions (p= 0.9), the same sine wave tone was presented ("standard"), while on the remaining occasions (p= 0.1) a new sound was presented ("novel"). Critically, sounds were played either during the first half of the fixation (0 ms delay) or during the second half of the fixation (120 ms delay). Consistent with the saccadic inhibition hypothesis, novel sounds led to longer fixation durations in the 120 ms compared to the 0 ms delay condition. However, novel sounds did not generally influence the execution of the subsequent saccade. These results suggest that unexpected sounds have a rapid influence on saccade planning, but not saccade execution.
... 429 Available eye movement control signals in the oculomotor system include those 430 that follow this ramp-and-hold temporal profile, or tonic activity that is proportional to eye 431 position throughout periods of both movement and fixation. In addition to such tonic 432 signals, oculomotor areas also contain neurons that exhibit burst patterns, or elevated 433 discharge in association with the saccade itself, as well as combinations of burst and 434 tonic patterns (for reviews, see Fuchs et al., 1985;Takahashi and Shinoda, 2018). It 435 remains to be seen which of these signals or signal combinations might be sent to the 436 auditory periphery and where they might come from. ...
... It 435 remains to be seen which of these signals or signal combinations might be sent to the 436 auditory periphery and where they might come from. The paramedian pontine reticular 437 formation (PPRF) is a strong candidate for a source, having been implicated in 438 providing corollary discharge signals of eye movements in visual experiments (Sparks 439 et al., 1987) (see also Guthrie et al., 1983), and containing each of these basic temporal 440 signal profiles (Fuchs et al., 1985;Takahashi and Shinoda, 2018). Regardless of the 441 source and nature of the descending corollary discharge signal, the oscillations 442 observed here should be thought of as possibly constituting a biomarker for an 443 underlying, currently unknown, mechanism, rather than necessarily the effect itself. ...
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 modelled 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.
Significance Statement
When the eyes move, the alignment between the visual and auditory scenes changes. We are not perceptually aware of these shifts -- which indicates that the brain must incorporate accurate information about eye movements into auditory and visual processing. Here we show that the small sounds generated within the ear by the brain contain accurate information about contemporaneous eye movements in the spatial domain: the direction and amplitude of the eye movements could be inferred from these small sounds. The underlying mechanism(s) likely involve(s) the ear’s various motor structures, and could facilitate the translation of incoming auditory signals into a frame of reference anchored to the direction of the eyes and hence the visual scene.
... During the last decades, neurophysiologists and neuroanatomists gathered in the monkey considerable knowledge that enabled identifying the core networks involved in the generation of eye movements (Büttner-Ennever, 2006;Fuchs et al., 1985;Goffart et al., 2017a;Grantyn et al., 2002;Henn et al., 1984;Horn and Leigh, 2011;Keller and Heinen, 1991;Krauzlis, 2004;Krauzlis et al., 2017;Moschovakis et al., 1996;Mustari et al., 2009;Phillips et al., 1996;Raphan and Cohen, 1978;Scudder et al., 2002;Sparks, 2002;Sparks and Mays, 1990;Ugolini et al., 2006). Technical developments offered the possibility to measure precisely the time course of these movements and to study correlations between the firing rate of neurons and kinematic parameters such as movement amplitude, velocity, acceleration and various differences (e.g., gaze error, velocity error, etc.). ...
... It remains to be seen which of these signals or signal combinations might be sent to the auditory periphery and where they might come from. The paramedian pontine reticular formation is a strong candidate for a source, having been implicated in providing corollary discharge signals of eye movements in visual experiments (61) (see also ref. 62) and containing each of these basic temporal signal profiles (59,60). Regardless of the source and nature of the descending corollary discharge signal, the oscillations observed here should be thought of as possibly constituting a biomarker for an underlying, currently unknown, mechanism, rather than necessarily the effect itself. ...
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.
... Saccades are rapid conjugate eye movements that shift the direction of gaze from one location to another in order to accurately aim the highly-innervated fovea at areas or objects of interest (Fuchs et al., 1985). Modern infrared camera techniques allow for accurate measurement of these eye-movements, and their dynamics and neural substrates have been studied extensively (Hopp and Fuchs, 2004;Alahyane et al., 2008;Kelly et al., 2010;Collins and Wallman, 2012;Belyusar et al., 2013). ...
Background
Altered patterns of eye-movements during scene exploration, and atypical gaze preferences in social settings, have long been noted as features of the Autism phenotype. While these are typically attributed to differences in social engagement and interests (e.g., preferences for inanimate objects over face stimuli), there are also reports of differential saccade measures to non-social stimuli, raising the possibility that fundamental differences in visuo-sensorimotor processing may be at play. Here, we tested the plasticity of the eye-movement system using a classic saccade-adaptation paradigm to assess whether individuals with ASD make typical adjustments to their eye-movements in response to experimentally introduced errors. Saccade adaptation can be measured in infants as young as 10 months, raising the possibility that such measures could be useful as early neuro-markers of ASD risk.
Methods
Saccade amplitudes were measured while children and adults with ASD ( N = 41) and age-matched typically developing (TD) individuals ( N = 68) made rapid eye-movements to peripherally presented targets. During adaptation trials, the target was relocated from 20-degrees to 15-degrees from fixation once a saccade to the original target location was initiated, a manipulation that leads to systematic reduction in saccade amplitudes in typical observers.
Results
Neither children nor adults with ASD showed any differences relative to TD peers in their abilities to appropriately adapt saccades in the face of persistently introduced errors.
Conclusion
Of the three studies to date of saccade adaptation in ASD, none have shown deficits in saccade adaptation that are sufficient to generalize to the whole or a subgroup of the ASD population. Unlike prior studies, we found no evidence for a slower adaptation rate during the early adaptation phase, and no of evidence greater variance of saccade amplitudes in ASD. In post hoc analysis, there was evidence for larger primary saccades to non-adapted targets, a finding requiring replication in future work.
... Methods for detail quantitative description of the model) (Fuchs et al., 1985;Takahashi et al., 2022). The input of the model is a 24° displacement command, which is compared with the . ...
Internal models are essential for the production of accurate movements. The accuracy of saccadic eye movements is thought to be mediated by an internal model of oculomotor mechanics encoded in the cerebellum. The cerebellum may also be part of a feedback loop that predicts the displacement of the eyes and compares it to the desired displacement in real time to ensure that saccades land on target. To investigate the role of the cerebellum in these two aspects of saccade production, we delivered saccade-triggered light pulses to channelrhodopsin-2-expressing Purkinje cells in the oculomotor vermis (OMV) of two macaque monkeys. Light pulses delivered during the acceleration phase of ipsiversive saccades slowed the deceleration phase. The long latency of these effects and their scaling with light pulse duration are consistent with an integration of neural signals at or downstream of the stimulation site. In contrast, light pulses delivered during contraversive saccades reduced saccade velocity at short latency and were followed by a compensatory reacceleration which caused gaze to land near or on the target. We conclude that the contribution of the OMV to saccade production depends on saccade direction; the ipsilateral OMV is part of a forward model that predicts eye displacement, whereas the contralateral OMV is part of an inverse model that creates the force required to move the eyes with optimal peak velocity for the intended displacement.
Significance Statement
Theory and experiment suggest that saccade production involves an internal model of oculomotor mechanics that resides inside the cerebellum. How cerebellar neurons implement this model is poorly understood. To illuminate this issue, we stimulated Purkinje cells in the oculomotor vermis (OMV) optogenetically during saccades and examined the resultant movement deviations. Stimulation of the contralateral OMV affected saccade dynamics at short latency, suggesting that the contralateral OMV is part of the feedforward pathway that produces the saccade motor command. In contrast, perturbation of the ipsilateral OMV affected saccade dynamics at longer latency, prolonging the saccade deceleration phase and leading to hypermetria. These effects are consistent with perturbation of the eye displacement integrator in the feedback loop of the saccade generator.
... In the macaque monkey, the oculomotor nuclei and many of the neurons in the brain stem composing the eye movement generator operate such that increasing the pulse frequency and/or train duration of electrical stimulation increases the magnitude of an ocular displacement (Cohen and Komatsuzuki, 1972;Schiller and Stryker, 1972). Furthermore, the greater the displacement the higher the firing frequency of the neurons (Fuchs et al., 1985;Schiller, 1970). Finally, head displacement and the rate of lateral locomotion (i.e., circling behavior), as induced from the brain stem via stimulation, increases systematically as a function of pulse frequency and train duration, as illustrated in rats Yeomans, 1986, 1987;Yeomans and Tehovnik, 1988). ...
We conduct a comparative evaluation of the visual systems from the retina to the muscles of the mouse and the macaque monkey noting the differences and similarities between these two species. The topics covered include (1) visual-field overlap, (2) visual spatial resolution, (3) V1 cortical point-image [i.e., V1 tissue dedicated to analyzing a unit receptive field], (4) object versus motion encoding, (5) oculomotor range, (6) eye, head, and
body movement coordination, and (7) neocortical and cerebellar function. We also discuss blindsight in rodents and primates which provides insights on how the neocortex mediates conscious vision in these species. This review is timely because the field of visuomotor neurophysiology is expanding beyond the macaque monkey to include the mouse; there is therefore a need for a comparative analysis between these two species on how the brain generates visuomotor responses.
... Even this hypothesis lacked morphological 552 evidence to support it, as axonal projection by IBNs to OPNs had not been observed (Yoshida et al., 553 1982;Strassman et al., 1986). Thus, the pathway from the SC to IBNs was considered to be 554 trisynaptic, via long-lead EBNs and short-lead EBNs (Fuchs et al., 1985). However, our previous study revealed that IBNs receive strong monosynaptic excitation from the contralateral SC 556 (Sugiuchi et al., 2005;Takahashi and Shinoda, 2018), and the present study shows that IBNs are, in 557 fact, the dominant source for inhibition of OPNs from the caudal SCs. ...
Omnipause neurons (OPNs) in the nucleus raphe interpositus have tonic activity while the eyes are stationary (“fixation”) but stop firing immediately before and during saccades. To locate the source of suppression, we analyzed synaptic inputs from the rostral and caudal superior colliculi (SCs) to OPNs by using intracellular recording and staining, and investigated pathways transmitting the inputs in anesthetized cats of both sexes. Electrophysiologically or morphologically identified OPNs received monosynaptic excitation from the rostral SCs with contralateral dominance, and received disynaptic inhibition from the caudal SCs with ipsilateral dominance. Cutting the tectoreticular tract transversely between the contralateral OPN and inhibitory burst neuron (IBN) regions eliminated inhibition from the caudal SCs, but not excitation from the rostral SCs in OPNs. In contrast, a midline section between IBN regions eliminated disynaptic inhibition in OPNs from the caudal SCs but did not affect the monosynaptic excitation from the rostral SCs. Stimulation of the contralateral IBN region evoked monosynaptic inhibition in OPNs, which was facilitated by preconditioning SC stimulation. Three-dimensional reconstruction of HRP-stained cells revealed that individual OPNs have axons that terminate in the opposite IBN area, while individual IBNs have axon collaterals to the opposite OPN area. These results show that there are differences in the neural circuit from the rostral and caudal SCs to the brainstem premotor circuitry and that IBNs suppress OPNs immediately before and during saccades. Thus, the IBNs, which are activated by caudal SC saccade neurons, shut down OPN firing and help to trigger saccades and suppress (“latch”) OPN activity during saccades.
... In the macaque monkey, the oculomotor nuclei and many of the neurons in the brain stem composing the eye movement generator operate such that increasing the pulse frequency and/or train duration of electrical stimulation increases the magnitude of an ocular displacement (Cohen and Komatsuzuki, 1972;Schiller and Stryker, 1972). Furthermore, the greater the displacement the higher the firing frequency of the neurons (Fuchs et al., 1985;Schiller, 1970). Finally, head displacement and the rate of lateral locomotion (i.e., circling behavior), as induced from the brain stem via stimulation, increases systematically as a function of pulse frequency and train duration, as illustrated in rats Yeomans, 1986, 1987;Yeomans and Tehovnik, 1988). ...
We conduct a comparative evaluation of the visual systems from the retina to the muscles of the mouse and the macaque monkey noting the differences and similarities between these two species. The topics covered include (1) visual-field overlap, (2) visual spatial resolution, (3) V1 cortical point-image [i.e., V1 tissue dedicated to analyzing a unit receptive field], (4) object versus motion encoding, (5) oculomotor range, (6) eye, head, and body movement coordination, and (7) neocortical and cerebellar function. We also discuss blindsight in rodents and primates which provides insights on how the neocortex mediates conscious vision in these species. This review is timely because the field of visuomotor neurophysiology is expanding beyond the macaque monkey to include the mouse; there is therefore a need for a comparative analysis between these two species on how the brain generates visuomotor responses.
... A crucial aspect of eye tracking data are fixation points, i.e. the moments of visual intake [22]. However, saccades, i.e. rapid eye movements, are equally important [13]. As such, we focus on a combination of point-based and AOI-based visualization techniques [2]. ...
Visualizing eye tracking data can provide insights in many research fields. However, visualizing such data efficiently and cost-effectively is challenging without well-designed tools. Easily accessible web-based approaches equipped with intuitive and interactive visualizations offer to be a promising solution. Many of such tools already exist, however, they mostly use one specific visualization technique. In this paper, we describe a web application which uses a combination of different visualization methods for eye tracking data. The visualization techniques are interactively linked to provide several perspectives on the eye tracking data. We conclude the paper by discussing challenges, limitations, and future work.
... Therefore, it is possible that impairment in SNr activity, as seen in PD, results in increased neuronal fluctuations in the superior colliculus, causing an increase in the frequency of fixational saccades. In addition to the superior colliculus, the cerebellar pathway also controls saccade generation via the burst neurons (Büttner-Ennever and Horn 1994;Fuchs et al. 1985;Hepp et al. 1989;Moschovakis et al. 1991). The cerebellar vermis lobules VI and VII and the fastigial ocular motor regions are connected to the burst neurons, hence modulating the saccade generation. ...
Miniature yoked eye movements, fixational saccades, are critical to counteract visual fading. Fixational saccades are followed by a return saccades forming squarewaves. Present in healthy states, squarewaves, if too many or too big, affect visual stability. Parkinson’s disease (PD), where visual deficits are not uncommon, is associated with the squarewaves that are excessive in number or size. Our working hypothesis is that the basal ganglia are at the epicenter of the abnormal fixational saccades and squarewaves in PD; the effects are manifested through their connections to the superior colliculus (affecting saccade frequency and amplitude) and the cerebellum (affecting velocity and amplitude). We predict that the subthalamic deep brain stimulation (DBS) variably affects the amplitude, frequency, and velocity of fixational saccade and that the effect depends on the electrode’s proximity or the volume of activated tissue in the subthalamic nucleus’ connections with the superior colliculus or the cerebellum. We found that DBS modulated saccade amplitude, frequency, and velocity in 11 PD patients. Although all three parameters were affected, the extent of the effects varied amongst subjects. The modulation was dependent upon the location and size of the electrically activated volume of the subthalamic region.
... This suggests that different saccadic parameters are associated with different neural processes that vary in their sensitivity to GABAergic effects. While peak velocity is closely related to activity of burst neurons in pontine reticular formation (Fuchs et al., 1985), latency reflects a composite measure of higher-level functions including perceptual processes, attention, target selection, decision-making and programming premotor commands (Carpenter, 2004;Hutton, 2008). Adverse lorazepam effects on latency may result from delayed programming of the saccadic command (Masson et al., 2000) through GABAergic effects in frontal or parietal eye fields (Roy-Byrne et al., 1993;Sommer and Tehovnik, 1997). ...
Background
Benzodiazepines have reliable adverse effects on saccadic eye movements, but the impact of sex as a potential modulator of these effects is less clear. A recent study reported stronger adverse effects on the spatial consistency of saccades in females, which may reflect sex differences in cerebellar mechanisms.
Aims
We aimed to further examine the role of sex as a potential modulator of benzodiazepine effects by employing the saccadic adaptation paradigm, which is known to be sensitive to cerebellar functioning.
Methods
A total of n=50 healthy adults performed a horizontal step prosaccade task and a saccadic adaptation task under 0.5 mg lorazepam, 1 mg lorazepam and placebo in a double-blind, within-subjects design.
Results
In the prosaccade task, lorazepam had adverse effects on measures of peak velocity, latency and spatial consistency. The administration of 0.5 mg lorazepam led to significant reductions in gain-decrease adaptation, while a dose of 1 mg did not impair adaptation learning. Gain-increase adaptation was generally less pronounced, and unaffected by the drug. There were no significant drug×sex interactions in either task.
Conclusions
We conclude that a low dose of lorazepam impairs gain-decrease adaptation independent of sex. At higher doses, however, increasing fatigue may facilitate adaptation and thus counteract the adverse effects observed at lower doses. With regards to prosaccades, our findings confirm peak velocity as well as latency and spatial measures as sensitive biomarkers of GABAergic effects.
... The oculomotor function of the SC was first discovered by electrical stimulation (Adamuk, 1872;Donders, 1872), and later induced via strychnine (Apter, 1946) in anesthetized cats. Extensive studies in alert monkeys via electrical stimulation (Robinson, 1972), neuronal recordings (Mohler and Wurtz, 1976), and lesions (Wurtz and Goldberg, 1972) then characterized the non-human primate topography of the SC [see several review papers including: (Fuchs et al., 1985;Sparks and Hartwich-Young, 1989;Sparks and Jay, 1986;Wurtz and Albano, 1980)]. In particular, the intermediate layers of monkey SC contain a retinotopically organized saccadic eye-movement map (Schiller and Stryker, 1972). ...
The superior colliculus (SC) is a layered midbrain structure involved in directing eye movements and coordinating visual attention. Electrical stimulation and neuronal recordings in the intermediate layers of monkey SC have shown a retinotopic organization for the mediation of saccadic eye-movements. However, in human SC the topography of saccades is unknown. Here, a novel experimental paradigm and highresolution (1.2-mm) functional magnetic resonance imaging methods were used to measure activity evoked by saccadic eye movements within SC. Results provide three critical observations about the topography of the human SC: (1) saccades along the superior-inferior visual axis are mapped across the medial-lateral anatomy of the SC; (2) the saccadic eye-movement representation is in register with the retinotopic organization of visual stimulation; and (3) activity evoked by saccades occurs deeper within SC than that evoked by visual stimulation. These approaches lay the foundation for studying the organization of human subcortical eye-movement mechanisms.
Highlights
High-resolution functional MRI enabled imaging from intermediate layers of human SC
Saccades along superior-inferior visual field are mapped across medial-lateral SC
Saccadic eye movement maps lie deeper in SC and are in alignment with retinotopy
ETOC Blurb
Savjani et al. found the polar angle representation of saccadic eye movements in human SC. The topography is similar in monkey SC, is in register with the retinotopic organization evoked by visual stimulation, but lies within deeper layers. These methods enable investigation of human subcortical eye-movement organization and visual function.
... 395 However, it is also not clear that the underlying effect is, in fact, oscillatory. [42] [see also 43], and containing each of these basic temporal signal 414 profiles [40,41]. Regardless of the source and nature of the descending corollary 415 discharge signal, the oscillations observed here should be thought of as possibly 416 constituting a biomarker for an underlying, currently unknown, mechanism, rather than 417 necessarily the effect itself. ...
Interactions between sensory pathways such as the visual and auditory systems are known to occur in the brain, but where they first occur is uncertain. Here we show a novel multimodal interaction evident at the eardrum. Ear canal microphone measurements in humans ( n =19 ears in 16 subjects) and monkeys ( n =5 ears in 3 subjects) performing a saccadic eye movement task to visual targets indicated that the eardrum moves in conjunction with the eye movement. The eardrum motion was oscillatory and began as early as 10 ms before saccade onset in humans or with saccade onset in monkeys. These eardrum movements, which we dub Eye Movement Related Eardrum Oscillations (EMREOs), occurred in the absence of a sound stimulus. The EMREOs’ amplitude and phase depended on the direction and horizontal amplitude of the saccade. They lasted throughout the saccade and well into subsequent periods of steady fixation. We discuss the possibility that the mechanisms underlying EMREOs create eye movement-related binaural cues that may aid the brain in evaluating the relationship between visual and auditory stimulus locations as the eyes move.
SIGNIFICANCE STATEMENT
The peripheral hearing system contains several motor mechanisms that allow the brain to modify the auditory transduction process. Movements or tensioning of either the middle-ear muscles or the outer hair cells modify eardrum motion, producing sounds that can be detected by a microphone placed in the ear canal (e.g. as otoacoustic emissions). Here, we report a novel form of eardrum motion produced by the brain via these systems -- oscillations synchronized with and covarying with the direction and amplitude of saccades. These observations suggest that a vision-related process modulates the first stage of hearing. In particular, these eye-movement related eardrum oscillations may help the brain connect sights and sounds despite changes in the spatial relationship between the eyes and the ears.
... Our measurements of the BOLD response as a function of depth confirmed similar depth profiles, including the previous finding that the mean depth profiles across subjects for saccadic activity was shifted deeper into SC compared with those obtained from visual stimulation. This is consistent with the functional organization of SC delineated in animal models (Fuchs, Kaneko, & Scudder, 1985;Sparks & Hartwich-Young, 1989;Wurtz & Albano, 1980). The profiles generated using our new method did not show significant differences from those utilizing the cylinder method ( Figure 5). ...
Dorsal human midbrain contains two nuclei with clear laminar organization, the superior and inferior colliculi. These nuclei extend in depth between the superficial dorsal surface of midbrain and a deep midbrain nucleus, the periaqueductal gray matter (PAG). The PAG, in turn, surrounds the cerebral aqueduct (CA). This study examined the use of two depth metrics to characterize depth and thickness relationships within dorsal midbrain using the superficial surface of midbrain and CA as references. The first utilized nearest-neighbor Euclidean distance from one reference surface, while the second used a level-set approach that combines signed distances from both reference surfaces. Both depth methods provided similar functional depth profiles generated by saccadic eye movements in a functional MRI task, confirming their efficacy for delineating depth for superficial functional activity. Next, the boundaries of the PAG were estimated using Euclidean distance together with elliptical fitting, indicating that the PAG can be readily characterized by a smooth surface surrounding PAG. Finally, we used the level-set approach to measure tissue depth between the superficial surface and the PAG, thus characterizing the variable thickness of the colliculi. Overall, this study demonstrates depth-mapping schemes for human midbrain that enables accurate segmentation of the PAG and consistent depth and thickness estimates of the superior and inferior colliculi.
... The neural substrates of saccade adaptation in the double-step paradigm are relatively well-known, given the sophisticated understanding of visuo-oculomotor pathways, acquired mostly through single-cell recordings in the awake monkey (for reviews see Fuchs, Kaneko, & Scudder, 1985;Munoz, 2002;Sparks, 2002;Krauzlis, 2005;White & Munoz, 2017). Many studies have investigated how error signals are processed in the brain. ...
When a saccadic eye movement does not land accurately on its visual target, subsequent saccades to the same target are subject to a corrective adjustment, which has been called saccade adaptation. Saccade adaptation has emerged as a go-to model for sensorimotor learning. Because observers show limited awareness of image manipulations during saccades, adaptive changes in saccade amplitude have long been thought to rely on the passive processing of visual error signals. However, it turns out that task-relevance has a modulatory effect on adaptation and that it can even be a sufficient cause for adaptation. Indeed, adaptation can be driven by a shift in task-relevant information even in the absence of a bottom-up visual error. This task-driven adaptation shares similar characteristics to bottom-up adaptation, that is adaptation triggered by a displacement of the eye-movement target. The effect of task-relevance is consistent with an integrated view of the saccadic system, where bottom-up and top-down signals converge to define the saccade target and the orienting of attention. We point to possible neural substrates of top-down adaptation, which largely remains to be elucidated in contrast to the detailed experimental and modeling work linking the cerebellum to bottom-up adaptation.
... 395 However, it is also not clear that the underlying effect is, in fact, oscillatory. [42] [see also 43], and containing each of these basic temporal signal 414 profiles [40,41]. Regardless of the source and nature of the descending corollary 415 discharge signal, the oscillations observed here should be thought of as possibly 416 constituting a biomarker for an underlying, currently unknown, mechanism, rather than 417 necessarily the effect itself. ...
Eye movements alter the relationship between the visual and auditory spatial scenes. Signals related to eye movements affect the brain's auditory pathways from the ear through auditory cortex and beyond, but how these signals might contribute to computing the locations of sounds with respect to the visual scene is poorly understood. Here, we evaluated the information contained in the signals observed at the earliest processing stage, eye movement-related eardrum oscillations (EMREOs). We report that human EMREOs carry information about both horizontal and vertical eye displacement as well as initial/final eye position. We conclude that all of the information necessary to contribute to a suitable coordinate transformation of auditory spatial cues into a common reference frame with visual information is present in this signal. We hypothesize that the underlying mechanism causing EMREOs could impose a transfer function on any incoming sound signal, which could permit subsequent processing stages to compute the positions of sounds in relation to the visual scene.
... The copyright holder for this preprint this version posted June 18, 2020. . https://doi.org/10.1101/2020.06.16.156125 doi: bioRxiv preprint Inhibitory coordinated control mechanisms have been implicated in other coordinated behaviors such as when making oblique saccades (33), looking and reaching (22,34), and reaching and grasping (35). Our results demonstrate that inhibitory coordinated control plays a role in mechanisms of visual-spatial cognition more broadly. ...
Understanding how natural behaviors are controlled depends on understanding the neural mechanisms of multiregional communication. Eye-hand coordination, a natural behavior shared by primates, is controlled by the posterior parietal cortex (PPC), a brain structure that expanded substantially in primate evolution. Here, we show that neurons within the saccade and reach regions within PPC communicate over a visuomotor channel to coordinate looking and reaching. During gaze-anchoring behavior, when saccades are transiently-inhibited by coordinated reaches, PPC neuron firing rates covary with beta-frequency (15-25 Hz) neuronal coherence. Decreases in parietal saccade neuron spiking correlated with gaze-anchoring behavior when the channel was “open” and not “closed”. Functional inhibition across beta-frequency-coherent communication channels may be a general mechanism for flexibly coordinating our natural behavior.
One Sentence Summary
Inhibitory communication through a visuomotor channel mediates the coordination of eye and hand movements.
... Our measurements of the BOLD response as a function of depth confirmed similar depth profiles, including the previous finding that the mean depth profiles across subjects for saccadic activity was shifted deeper into SC compared to those obtained from visual stimulation. This is consistent with the functional organization of SC delineated in animal models (Fuchs, Kaneko, & Scudder, 1985;Sparks & Hartwich-Young, 1989;Wurtz & Albano, 1980). The profiles generated using our new method did not show significant differences from those utilizing the cylinder method (Fig. 5); substantial differences in Euclidean and level-set depth metrics only emerge at depths >3 mm. ...
Dorsal human midbrain contains two nuclei with clear laminar organization, the superior and inferior colliculi. These nuclei extend in depth between the superficial dorsal surface of midbrain and a deep midbrain nucleus, the periaqueductal gray matter (PAG). The PAG, in turn, surrounds the cerebral aqueduct (CA). This study examined the use of two depth metrics to characterize depth and thickness relationships within dorsal midbrain using the superficial surface of midbrain and CA as references. The first utilized nearest-neighbor Euclidean distance from one reference surface, while the second used a level-set approach that combines signed distance from both reference surfaces. Both depth methods provided similar functional depth profiles generated by saccadic eye movements in a functional MRI task, confirming their efficacy for superficial functional activity. Next, the boundaries of the PAG were estimated using Euclidean distance together with elliptical fitting, indicating that the PAG can be readily characterized by a smooth surface surrounding PAG. Finally, we used the level-set approach to measure tissue depth between the superficial surface and the PAG, thus characterizing the variable thickness of the colliculi. Overall, this study demonstrates depth-mapping schemes for human midbrain that enables accurate segmentation of the PAG and consistent depth and thickness estimates of the superior and inferior colliculi.
... However, the required brevity of stimulus presentation is contentious. Regular saccade latencies are of the order of 135-220 ms, but this includes time for fixation neurons of the superior colliculus to disengage (Fuchs, Kaneko, & Scudder, 1985;Wurtz, 1996) and removal of the fixation stimulus prior to presentation of the target, as was done in all of the cited studies using emotional faces as stimuli, may shorten the critical window for stimulus presentation to 90 -120 ms (Saslow, 1967;Walker, Kentridge, & Findlay, 1995), though not for some tasks, including reading (Liversedge et al., 2004). To be safe, in the present study we enforced fixation on specific facial locations by presenting faces in a fixationcontingent manner for approximately 80 ms. ...
At normal interpersonal distances all features of a face cannot fall within one's fovea simultaneously. Given that certain facial features are differentially informative of different emotions, does the ability to identify facially expressed emotions vary according to the feature fixated and do saccades preferentially seek diagnostic features? Previous findings are equivocal. We presented faces for a brief time, insufficient for a saccade, at a spatial position that guaranteed that a given feature-an eye, cheek, the central brow, or mouth-fell at the fovea. Across 2 experiments, observers were more accurate and faster at discriminating angry expressions when the high spatial-frequency information of the brow was projected to their fovea than when 1 or other cheek or eye was. Performance in classifying fear and happiness (Experiment 1) was not influenced by whether the most informative features (eyes and mouth, respectively) were projected foveally or extrafoveally. Observers more accurately distinguished between fearful and surprised expressions (Experiment 2) when the mouth was projected to the fovea. Reflexive first saccades tended toward the left and center of the face rather than preferentially targeting emotion-distinguishing features. These results reflect the integration of task-relevant information across the face constrained by the differences between foveal and extrafoveal processing (Peterson & Eckstein, 2012). (PsycINFO Database Record (c) 2020 APA, all rights reserved).
... It has known internal 469 connectivity, documented by electrophysiology and anatomical tracing with horseradish 470 peroxidase (Hikosaka et al., 1978; Langer and Kaneko, 1990). The connectivity leads to 471switching behavior in computational models and the output pathways from the brain's switching 472 circuit are appropriate to prevent saccades during preparation until it is time for the movement 473(Fuchs et al., 1985;Robinson, 1973). ...
We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related cortical areas without prematurely inducing movement. The smooth eye movement region of the frontal eye fields (FEFSEM) is a critical node in the neural circuit controlling smooth pursuit eye movement. Preparatory activity evolves in the monkey FEFSEM during fixation in parallel with an objective measure of visual-motor gain. We propose that the use of FEFSEM output as a gain signal rather than a movement command allows for preparation to progress in pursuit without causing movement. We also show that preparatory modulation of firing rate in FEFSEM predicts movement, providing evidence against the 'movement-null' space hypothesis as an explanation of how preparatory activity can progress without movement. Finally, there is a partial reorganization of FEFSEM population activity between preparation and movement that would allow for a directionally non-specific component of preparatory visual-motor gain enhancement in pursuit.
... We also classified neurons as either mainly position or mainly velocity encoding ( Fig. 3) in this experiment, although intermediate "multi-dimensional" responsivity likely occurs as well. ABN neurons should receive slow-phase velocity signals during optokinetic stimulation, e.g., via the pretectum, vestibular nuclei, cerebellum, and the OI (Fig. 1a′ [8,23,[37][38][39]) since a muscle force step is needed to overcome the dampened, viscous kinetics of the oculomotor plant [40,41]. In order to investigate the differential coding of oculomotor neurons and to visualize the anatomical distribution of position and velocity coding within rhombomeres 7/8, we developed a binocular closed-loop stimulation protocol to disentangle eye position from eye velocity correlations by eliciting different eye velocities at different eye positions ( Fig. 5a-a″, see the "Methods" section). ...
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.
... Most eye tracking technology uses infrared imaging to track movement of the user's gaze over time [8]. Eye trackers can detect the rapid, unconscious movements of the eyes (called saccades); however, it is the longer periods without movement (called fixations) that typically correspond to the user's conscious visual attention [14,32]. ...
Many images on the Web, including photographs and artistic images, feature spatial relationships between objects that are inaccessible to someone who is blind or visually impaired even when a text description is provided. While some tools exist to manually create accessible image descriptions, this work is time consuming and requires specialized tools. We introduce an approach that automatically creates spatially registered image labels based on how a sighted person naturally interacts with the image. Our system collects behavioral data from sighted viewers of an image, specifically eye gaze data and spoken descriptions, and uses them to generate a spatially indexed accessible image that can then be explored using an audio-based touch screen application. We describe our approach to assigning text labels to locations in an image based on eye gaze. We then report on two formative studies with blind users testing EyeDescribe. Our approach resulted in correct labels for all objects in our image set. Participants were able to better recall the location of objects when given both object labels and spatial locations. This approach provides a new method for creating accessible images with minimum required effort.
... It has known internal 377 connectivity, documented by electrophysiology and anatomical tracing with horseradish 378 peroxidase(Hikosaka et al., 1978;Langer and Kaneko, 1990). The connectivity leads to 379 switching behavior in computational models and the output pathways from the brain's switching 380 circuit are appropriate to prevent saccades during preparation until it is time for the movement 381(Fuchs et al., 1985;Robinson, 1973). ...
We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related cortical areas without prematurely inducing movement. The smooth eye movement region of the frontal eye fields (FEFSEM) is a critical node in the neural circuit controlling smooth pursuit eye movement. Preparatory activity evolves in FEFSEM during fixation in parallel with an objective measure of visual-motor gain. We propose that the use of FEFSEM output as a gain signal allows for preparation to progress in the pursuit system without causing movement. We also show that preparatory modulation of firing rate in FEFSEM progresses in a way that predicts movement, providing evidence against the 'movement-null' space hypothesis of how preparatory activity can progress without movement. Finally, there is partial reorganization of FEFSEM population activity between preparation and movement. We propose that this reorganization allows for a directionally non-specific component of preparatory visual-motor gain enhancement in the pursuit system.
... We also classified neurons as either mainly position or mainly velocity encoding (Fig. 3) in this experiment, although intermediate "multi-dimensional" responsivity likely occurs as well. ABN neurons should receive slow-phase velocity signals during optokinetic stimulation, e.g., via the pretectum, vestibular nuclei, cerebellum, and the OI (Fig. 1a′ [8,23,[37][38][39]) since a muscle force step is needed to overcome the dampened, viscous kinetics of the oculomotor plant [40,41]. In order to investigate the differential coding of oculomotor neurons and to visualize the anatomical distribution of position and velocity coding within rhombomeres 7/8, we developed a binocular closed-loop stimulation protocol to disentangle eye position from eye velocity correlations by eliciting different eye velocities at different eye positions ( Fig. 5a-a″, see the "Methods" section). ...
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 velocity and position storage mechanisms. Position encoding neurons are recruited at eye position thresholds distributed across the behavioral dynamic range, while velocity encoding neurons have more centered 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, which 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.
... EBNs for horizontal saccades are in the paramedian pontine reticular formation (PPRF), projecting to the ipsilateral abducens nucleus, and IBNs for horizontal saccades are in the paramedian pontomedullary reticular formation (PPMRF), projecting to the contralateral abducens nucleus. Accordingly, it is generally accepted that the shortest excitatory pathway from the SC to Abd MNs is trisynaptic and the shortest inhibitory pathway is quadrisynaptic via EBNs (Fuchs et al., 1985;Hepp et al., 1989;Scudder et al., 2002) (Fig. 1, right). The activities of these MLBNs are closely related to the duration and velocity of saccades (Keller, 1974). ...
We review neural connections of the superior colliculus (SC) and brainstem saccade-related neurons in relation to saccade generation mechanism. The caudal and rostral SC play a role in saccade generation and visual fixation, respectively. This functional differentiation suggests that different connections should exist between these two SC areas and their brainstem target neurons. We examined synaptic potentials evoked by stimulation of the rostral and caudal SC in inhibitory burst neurons (IBNs) and omnipause neurons (OPNs) in anesthetized cats. The caudal and rostral SC produced monosynaptic excitation and disynaptic inhibition in IBNs, respectively. Intracellular HRP staining showed that single IBNs sent their axons to abducens motoneurons, IBNs and OPNs on the opposite side. OPNs received monosynaptic excitation from the rostral SC, and disynaptic inhibition from the caudal SC via opposite IBNs. These neural connections are discussed in relation to the saccade triggering system and the model proposed by Miura and Optican.
... These commands are transmitted to the burst, tonic, and omnipause neurons in the pons, medulla, and the reticular formation. These neurons innervate the motoneurons, which activate the ocular muscles (Fuchs, Kaneko, & Scudder, 1985), and influence saccade size and velocity (Scudder et al., 2002). Saccades take flight when ocular muscles apply a burst of mechanical force. ...
The oculomotor system is subject to noise, and adaptive processes compensate for consistent errors in gaze targeting. Recent evidence suggests that positional errors induced by eye blinks are also corrected by an adaptive process: When a fixation target is displaced during repeated blinks, subsequent blinks are accompanied by an automatic compensating eye movement anticipating the updated target location after the blink. Here, we further tested the extent of this "blink adaptation." Participants were tasked to look at a white target dot on a black screen and encouraged to blink voluntarily, or air puffs were used to elicit reflexive blinks. In separate runs, the target was displaced by 0.7° in either of the four cardinal directions during blinks. Participants adapted to positional changes during blinks, i.e., the postblink gaze position was biased in the direction of the dot displacement. Adaptation occurred for both voluntary and reflexive blinks. However, adaptation was unequal across different adaptation directions: Horizontally, temporal displacements experienced larger adaptation than nasal displacements; vertically, downward displacements led to larger adaptation than upward displacements. Results paralleled anisotropies commonly found for saccade amplitudes, and thus it is likely that gaze corrections across eye blinks share general constraints of the oculomotor system with saccades.
... Memory-guided saccades are performed in the absence of stimulus-relevant visual input and are guided solely by a representation of the target maintained in WM. Because the neurons most proximally related to the production of a saccade are distinct from those neurons supporting WM representations, producing a memory-guided saccade, at a minimum, is likely to involve a process whereby WM's spatial information is transferred, or "read out", into a second pattern of oculomotor-related neurons whose activity directly contributes to the production of a corresponding saccadic eye-movement (Fig 2a) [13,20]. We modeled this read out process using a simple extension of the stochastic accumulator framework (S1 Text), which has been used previously to account for behavioral responses and speed-accuracy relationships in other contexts [21][22][23][24]. ...
Working memory performance is a key indicator of cognitive and developmental status. While recent evidence indicates that stabilizing neural gain supports the stabilization of working memory during adolescence, the computational mechanisms linking neural stabilization to behavior are poorly understood. We develop a mechanistic account of behavior during the memory-guided saccade task based on a stochastic accumulator framework. Results indicate that a specific balance of independent gain signals affecting working memory representations and oculomotor response thresholds can account for a peculiar U-shaped feature of the speed-accuracy relationship. Additionally, aspects of behavioral variability and mean behavioral performance, as well as subtle shifts in the shape of the speed-accuracy relationship across development, can be accounted for by the stabilization of these two sources of variability. Thus, the stabilization of neural variability can, in part, account for developmental improvements in behavioral variability as well as some improvement in mean behavioral performance.
... The contralateral cFN adds to the saccade command during the beginning of the movement by its excitation of the ipsilateral MLBNs. The ipsilateral cFN provides a braking signal at the end by means of a late burst and subsequent excitation of the contralateral MLBNs (Fuchs et al., 1985). The motor command to the oculomotor plant, delivered through motor neurons, is the net difference between the contralateral and ipsilateral MLBNs, simulated as one grouped unit. ...
Recent electrophysiological observations related to saccadic eye movements in rhesus monkeys, suggest a prediction of the sensory consequences of movement in the Purkinje cell layer of the cerebellar oculomotor vermis (OMV). A definite encoding of real-time motion of the eye has been observed in simple-spike responses of the combined burst-pause Purkinje cell populations, organized based upon their complex-spike directional tuning. However, the underlying control mechanisms that could lead to such action encoding are still unclear. We propose a saccade control model, with emphasis on the structure of the OMV and its interaction with the extra-cerebellar components. In the simulated bilateral organization of the OMV, each caudal fastigial nucleus is arranged to receive incoming projections from combined burst-pause Purkinje cell populations. The OMV, through the caudal fastigial nuclei, interacts with the brainstem to provide adaptive saccade gain corrections that minimize the visual error in reaching a given target location. The simulation results corroborate the experimental Purkinje cell population activity patterns and their relation with saccade kinematic metrics. The Purkinje layer activity that emerges from the proposed organization, precisely predicted the speed of the eye at different target eccentricities. Simulated granular layer activity suggests no separate dynamics with respect to shaping the bilateral Purkine layer activity. We further examine the validity of the simulated OMV in maintaining the accuracy of saccadic eye movements in the presence of signal dependent variabilities, that can occur in extra-cerebellar pathways.
... The superior colliculus (SC), in the midbrain, has long been considered an essential structure for eye movement control (for reviews, see Fuchs et al., 1985;Sparks and Mays, 1990;Sommer and Wurtz, 2008). Eye movements are necessary for visual sensation because the majority of ganglion cells are of the transient type, which quickly adapt, and thus static images on the retina quickly disappear from perception. ...
The superior colliculus (SC) is an essential structure for the control of eye movements. In rodents, the SC is also considered to play an important role in whisking behavior, in which animals actively move their vibrissae (mechanosensors) to gather tactile information about the space around them during exploration. We investigated how the SC contributes to vibrissal movement control. We found that when the SC was unilaterally lesioned, the resting position of the vibrissae shifted backward on the side contralateral to the lesion. The unilateral SC lesion also induced an increase in the whisking amplitude on the contralateral side. To explore the anatomical basis for SC involvement in vibrissal movement control, we then quantitatively evaluated axonal projections from the SC to the brainstem using neuronal labeling with a virus vector. Neurons of the SC mainly sent axons to the contralateral side in the lower brainstem. We found that the facial nucleus received input directly from the SC, and that the descending projections from the SC also reached the intermediate reticular formation and pre-Bötzinger complex, which are both considered to contain neural oscillators generating rhythmic movements of the vibrissae. Together, these results indicate the existence of a neural circuit in which the SC modulates vibrissal movements mainly on the contralateral side, via direct connections to motoneurons, and via indirect connections including the central pattern generators.
... Our results suggest that an additional process generates catchup saccades when a large pursuit stimulus has a central spot. The saccadic system may be recruited to assist in attentive foveation of a central goal, since saccades primarily foveate (Fuchs et al. 1985;Van Gisbergen et al. 1981), and attention and the saccadic system are linked (e.g., see Kowler et al. 1995 andMcPeek et al. 1999). Attentive foveation might occur in parallel with the smooth eye velocity generation, explaining why it does not affect pursuit gain. ...
... At the muscular level, centripetal saccades seem driven by lower mechanical constraints than centrifugal saccades (Koene & Erkelens, 2002). Indeed, the connections between the paramedian pontine reticular formation (PPRF, pulse generator of horizontal saccades) and extraocular muscles suggest that agonist/ antagonist pairs of muscles are organized in a push-pull arrangement (Fuchs, Kaneko, & Scudder, 1985;Ling, Fuchs, Siebold, & Dean, 2007;Moschovakis & Highstein, 1994;Pelisson & Prablanc, 1988;Robinson, 1989;Van Gisbergen, Robinson, & Gielen, 1981). Therefore, in case of a centripetal saccade, orbital passive elastic forces pull the eyes toward their primary position (Robinson, 1981). ...
It is well known that the saccadic system presents multiple asymmetries. Notably, temporal (as opposed to nasal) saccades, centripetal (as opposed to centrifugal) saccades (i.e., the recentering bias) and saccades from the abducting eye (as opposed to the concomitant saccades from the adducting eye) exhibit higher peak velocities. However, these naso-temporal and centripetal-centrifugal asymmetries have always been studied separately. It is thus unknown which asymmetry prevails when there is a conflict between both asymmetries, i.e., in case of centripetal nasal saccades or centrifugal temporal saccades. This study involved binocular recordings of eye movements to examine both the naso-temporal and centripetal-centrifugal asymmetries so as to determine how they work together. Twenty-eight participants had to make saccades toward stimuli presented either centrally or in the periphery in binocular conditions. We found that temporal and abducting saccades always exhibit higher peak velocities than nasal and adducting saccades, irrespective of their centripetal or centrifugal nature. However, we showed that the velocity advantage for centripetal saccades is only found for temporal and not for nasal saccades. Such a result is of importance as it could provide new insights about the physiological origins of the asymmetries found in the saccadic system.
... The oculomotor function of the SC was first discovered by electrical stimulation (Adamuk, 1872;Donders, 1872), and later induced via strychnine (Apter, 1946) in anesthetized cats. Extensive studies in alert monkeys via electrical stimulation (Robinson, 1972), neuronal recordings (Mohler and Wurtz, 1976), and lesions (Wurtz and Goldberg, 1972) then characterized the non-human primate topography of the SC [see several reviews (Fuchs et al., 1985;Sparks and Hartwich-Young, 1989;Sparks and Jay, 1986;Wurtz and Albano, 1980):]. The intermediate layers of monkey SC contain a retinotopically organized saccadic eye-movement map (Schiller and Stryker, 1972). ...
The superior colliculus (SC) is a layered midbrain structure involved in directing both head and eye movements and coordinating visual attention. Although a retinotopic organization for the mediation of saccadic eye-movements has been shown in monkey SC, in human SC the topography of saccades has not been confirmed. Here, a novel experimental paradigm was performed by five participants (one female) while high-resolution (1.2-mm) functional magnetic resonance imaging was used to measure activity evoked by saccadic eye movements within human SC. Results provide three critical observations about the topography of the SC: (1) saccades along the superior-inferior visual axis are mapped across the medial-lateral anatomy of the SC; (2) the saccadic eye-movement representation is in register with the retinotopic organization of visual stimulation; and (3) activity evoked by saccades occurs deeper within SC than that evoked by visual stimulation. These approaches lay the foundation for studying the organization of human subcortical - and enhanced cortical mapping - of eye-movement mechanisms.
... If motion sensitivity in the peripheral visual field follows a time course similar to motion sensitivity in central vision, then some of the characteristic failure of detection accidents of older drivers may arise from a peripheral motion processing (PMP) deficit that reduces the power of a moving stimulus to attract visual attention (Steinman, Steinman, Trick, & Lehmkuhle, 1994) and to produce a reflexive saccadic eye movement toward it (Fuchs, Kaneko, & Scudder, 1985;Stein, 1984). According to this hypothesis, a PMP deficit reduces the salience of a moving object, thus disrupting the preattentive stage of scan-path generation and serial search. ...
Internal models are essential for the production of accurate movements. The accuracy of saccadic eye movements is thought to be mediated by an internal model of oculomotor mechanics encoded in the cerebellum. The cerebellum may also be part of a feedback loop that predicts the displacement of the eyes and compares it to the desired displacement in real time to ensure that saccades land on target. To investigate the role of the cerebellum in these two aspects of saccade production, we delivered saccade-triggered light pulses to channelrhodopsin-2-expressing Purkinje cells in the oculomotor vermis (OMV) of two male macaque monkeys. Light pulses delivered during the acceleration phase of ipsiversive saccades slowed the deceleration phase. The long latency of these effects and their scaling with light pulse duration are consistent with an integration of neural signals at or downstream of the stimulation site. In contrast, light pulses delivered during contraversive saccades reduced saccade velocity at short latency and were followed by a compensatory reacceleration which caused gaze to land on or near the target. We conclude that the contribution of the OMV to saccade production depends on saccade direction; the ipsilateral OMV is part of a forward model that predicts eye displacement, whereas the contralateral OMV is part of an inverse model that creates the force required to move the eyes with optimal peak velocity for the intended displacement.
The uniqueness of eyes, facial geometry, and gaze direction makes eye tracking a very challenging technological pursuit. Although camera-based eye-tracking systems are popular, the obtrusiveness of their bulky equipment along with their high computational cost and power consumption is considered problematic for wearable applications. Noncontact gaze monitoring using capacitive sensing technique has been attempted but failed due to low sensitivity and parasitic capacitance. Here, we study the interaction between a novel capacitive sensor and eye movement for wearable eye-tracking. The capacitive sensors are made of a pair of asymmetric electrodes; one comprising carbon nanotube-paper composite fibers (CPC) and the other being a rectangular metal electrode. The interaction between the asymmetric sensor and a spherical object mimicking an eyeball is analyzed numerically. Using a face simulator, both single- and differential capacitive measurements are characterized with respect to proximity, geometry, and human body charge. Using a prototype eye tracker, multiple sensor locations are studied to determine the optimal configurations. The capacitive responses to vertical and horizontal gaze directions are analyzed in comparison to those of a commercial eye tracking system. The performance is demonstrated for sensitive eye-movement tracking, closed-eye monitoring, and human-machine interface. This research has important implications for the development of capacitive, wearable eye trackers, which can facilitate fields of human-machine interface, cognitive monitoring, neuroscience research, and rehabilitation.
This article deals with the neural circuits involved in the generation of horizontal and vertical saccades. Following an explanation about the horizontal saccade system, the vertical saccade system, which has not been described in textbooks, is discussed in detail. Comparing the results with the well-known vestibuloocular pathways, we propose that the saccade system uses the same frame of reference as the vestibuloocular system. The last part of this article explains that the neural circuits for saccades and the quick phase of vestibular nystagmus share a common pathway.
It has generally been accepted that voluntary eye movements are organized in horizontal and vertical systems, based on the results of clinical studies in humans and lesion studies in animals. However, this issue is still under debate, because the neural circuits for vertical saccades are yet to be identified. The riMLF was identified as a premotor center for vertical gaze by Büttner-Ennever, although the exact pathways from the superior colliculus to the vertical ocular motoneurons are unknown. Using intracellular recording and staining techniques, we found that both systems use the same 3D cartesian coordinates as the semicircular canal coordinates. The oldest phylogenetic system, the vestibular system, is used as a common coordinate system by the newer system, the voluntary eye movement subsystem, which constantly captures visual information in relation to the gravitational axis, and the sensory and motor coordinate systems that form the basis of visual cognition in the brain are unified using the common vestibular coordinate system. Use Assumption of the common coordinate system conflicts with Listing's law, but the excitatory commissural connection between the superior colliculi that we discovered is considered to provide the neural substrate for Listing's law.
It is generally accepted that voluntary quick eye movements (saccades) are organized in the horizontal and vertical eye movement systems. Therefore, oblique saccades are considered to be generated by the vector sum of the outputs from the coordinated horizontal and vertical saccade systems, but the precise neural mechanism of generation of oblique saccades remains unresolved. The superior colliculus (SC) is known to be the center for saccades. Our previous studies show that many efferent neurons in the SC project to the midbrain and the pontine reticular formation, but their branching patterns and exact terminal areas in the brainstem are not known. In this study, we used an electrophysiological method for investigating branching patterns of single tectofugal neurons that project to various last-order premotor neurons for horizontal and vertical saccades in the brainstem of the cat. We recorded antidromic spikes and examined the effects of stimulation of the vertical and horizontal last-order premotor neuron areas (Forel's field H, FFH; excitatory burst neuron (EBN) region and inhibitory burst neuron (IBN) region for horizontal saccades). The results showed that there are four types of branching patterns of single tectofugal neurons that project to the last-order horizontal and vertical premotor neuron areas, and the upper cervical spinal cord. Among these, two types of the tectofugal neurons (about 69%) have axonal branches that project to the ipsilateral FFH and the contralateral EBN region, and furthermore, about 69% of them have another axonal branch that extends to the spinal cord. This finding indicates that single tectofugal neurons innervating both horizontal and vertical saccade generators with their axonal collaterals can easily synchronize the onsets of the horizontal and vertical saccade generating systems, and provides evidence that the branching patterns of single tectofugal neurons determine the functional synergies for coordinated oblique eye and head movements. © 2022 Japan Society for Equilibrium Research. All rights reserved.
Primates use rapid eye movements, called saccades, to scan their surroundings. Most of the well-studied neuronal elements that generate saccades are located in the brainstem, but recently our labs and others showed that the midline cerebellum is required for the production of accurate and stereotypical saccades. This oculomotor cerebellum receives mossy fiber inputs from saccade-related areas in the brainstem and sends its outputs to the brainstem saccade burst generator. How Purkinje cell simple spike activity is formed, and how the activity affects the movement in real-time are not well understood. In this chapter, we describe techniques to address these questions. Using optogenetics we manipulate the simple spike activity of cerebellar Purkinje cells while the saccade is ongoing. We also express optogenetic opsin to inhibit a subset of mossy fiber inputs to the cerebellum and examine the effects of the inhibition on simple spike activity.
The caudal fastigial nuclei (cFN) are the output nuclei by which the medio-posterior cerebellum influences the production of saccades toward a visual target. On the basis of the organization of their efferences to the premotor burst neurons and the bilateral control of saccades, the hypothesis was proposed that the same unbalanced activity accounts for the dysmetria of all saccades during cFN unilateral inactivation, regardless of whether the saccade is horizontal, oblique, or vertical. We further tested this hypothesis by studying, in two head-restrained macaques, the effects of unilaterally inactivating the caudal fastigial nucleus on saccades toward a target moving vertically with a constant, increasing or decreasing speed. After local muscimol injection, vertical saccades were deviated horizontally toward the injected side with a magnitude that increased with saccade size. The ipsipulsion indeed depended upon the tested target speed, but not its instantaneous value because it did not increase (decrease) when the target accelerated (decelerated). By subtracting the effect on contralesional horizontal saccades from the effect on ipsilesional ones, we found that the net bilateral effect on horizontal saccades was strongly correlated with the effect on vertical saccades. We explain how this correlation corroborates the bilateral hypothesis and provide arguments against the suggestion that instantaneous saccade velocity would somehow be "encoded" by the discharge of Purkinje cells in the oculomotor vermis.
The primate superior colliculus (SC) has recently been shown to possess both a large foveal representation as well as a varied visual processing repertoire. This structure is also known to contribute to eye movement generation. Here we describe our current understanding of how SC visual and movement-related signals interact within the realm of small eye movements associated with the foveal scale of visuomotor behavior. Within the SC's foveal representation, there is a full spectrum of visual, visual-motor, and motor-related discharge for fixational eye movements. Moreover, a substantial number of neurons only emit movement-related discharge when microsaccades are visually-guided, but not when similar movements are generated towards a blank. This represents a particularly striking example of integrating vision and action at the foveal scale. Beyond that, SC visual responses themselves are strongly modulated, and in multiple ways, by the occurrence of small eye movements. Intriguingly, this impact can extend to eccentricities well beyond the fovea, causing both sensitivity enhancement and suppression in the periphery. Because of large foveal magnification of neural tissue, such long-range eccentricity effects are neurally warped into smaller differences in anatomical space, providing a structural means for linking peripheral and foveal visual modulations around fixational eye movements. Finally, even the retinal-image visual flows associated with tiny fixational eye movements are signaled fairly faithfully by peripheral SC neurons with relatively large receptive fields. These results demonstrate how studying active vision at the foveal scale represents an opportunity for understanding primate vision during natural behaviors involving ever-present foveating eye movements.
Vision is obtained with a continuous motion of the eyes. The kinematic analysis of eye motion, during any visual or ocular task, typically reveals two (kinematic) components: saccades, which quickly replace the visual content in the retinal fovea, and drifts, which slowly scan the image after each saccade. While the saccadic exchange of regions of interest (ROIs) is commonly considered to be included in motor-sensory closed-loops, it is commonly assumed that drifts function in an open-loop manner, that is, independent of the concurrent visual input. Accordingly, visual perception is assumed to be based on a sequence of open-loop processes, each initiated by a saccade-triggered retinal snapshot. Here we directly challenged this assumption by testing the dependency of drift kinematics on concurrent visual inputs using real-time gaze-contingent-display. Our results demonstrate a dependency of the trajectory on the concurrent visual input, convergence of speed to condition-specific values and maintenance of selected drift-related motor-sensory controlled variables, all strongly indicative of drifts being included in a closed-loop brain-world process, and thus suggesting that vision is inherently a closed-loop process.
The oculomotor capture triggered by a peripheral onset is subject to habituation, a basic form of learning consisting in a response decrement toward a repeatedly presented stimulus. However, it is unclear whether habituation of reflexive saccades takes place at the saccadic programming or execution stage (or both). To address this issue, we exploited the fact that during fixation the programming of a reflexive saccade exerts a robust but short-lasting phasic inhibition in the absolute microsaccadic frequency. Hence, if habituation of reflexive saccades occurs at the programming stage, then this should also affect the microsaccadic frequency, with a progressive reduction of the inhibitory phase. Conversely, if habituation occurs only at the later stage of saccade execution, the no change in the microsaccadic pattern is expected. Participants were repeatedly exposed to a peripheral onset distractor, and when eye movements were allowed, we replicated the oculomotor capture habituation. Crucially, however, when fixation was maintained the microsaccadic response did not change as exposure to the onset progressed, suggesting that habituation of reflexive saccades does not take place at the programming stage in the superior colliculus (SC), but at the later stage of saccade execution in the brainstem, where the competition between different saccades might be resolved. This scenario challenges one of the main assumptions of the competitive integration model for oculomotor control, which assumes that competition between exogenous and endogenous saccade programs occurs in the (SC). Our results and interpretation are instead in agreement with neurophysiological studies in non-human primates showing that saccadic adaption, another form of oculomotor plasticity, takes place downstream from the SC.
This review examines kinetic properties and distribution of the eleven isoforms of myosin heavy chain (MyHC) expressed in extraocular muscle (EOM) fibre types and the regulation and function of these MyHCs. Although recruitment and discharge characteristics of ocular motoneurons during fixation and eye movements are well documented, work directly linking these properties with motor unit contractile speed and MyHC composition is lacking. Recruitment of motor units according to Henneman’s size principle has some support in EOMs but needs consolidation. Both neurogenic and myogenic mechanisms regulate MyHC expression as in other muscle allotypes. Developmentally, multiply‐innervated (MIFs) and singly‐innervated fibres (SIFs) are derived presumably from distinct myoblast lineages, ending up expressing MyHCs in the slow and fast ends of the kinetic spectrum, respectively. They modulate the synaptic inputs of their motoneurons through different retrogradely transported neurotrophins, thereby specifying their tonic and phasic impulse patterns. Immunohistochemical analyses of EOMs regenerating in situ and in limb muscle beds suggest that the very impulse patterns driving various ocular movements equip effectors with appropriate MyHC compositions and speeds to accomplish their tasks. These experiments also suggest that satellite cells of SIFs and MIFs are distinct lineages expressing different MyHCs during regeneration. MyHC compositions and functional characteristics of orbital fibres show longitudinal variations that facilitate linear ocular rotation during saccades. Palisade endings on global MIFs are postulated to respond to active and passive tensions by triggering axon reflexes that play important roles during fixation, saccades and vergence. How EOMs implement Listings law during ocular rotation is discussed.
The cerebellum is known to make movements fast, smooth, and accurate. Many hypotheses emphasize the role of the cerebellum in computing learned predictions important for sensorimotor calibration and feedforward control of movements. Hypotheses of the computations performed by the cerebellum in service of motor control borrow heavily from control systems theory, with models that frequently invoke copies of motor commands, called corollary discharge. This review describes evidence for corollary discharge inputs to the cerebellum and highlights the hypothesized roles for this information in cerebellar motor-related computations. Insights into the role of corollary discharge in motor control, described here, are intended to inform the exciting but still untested roles of corollary discharge in cognition, perception, and thought control relevant in psychiatric disorders.
Sensory signals for eye movements (visual and vestibular) are initially coded in different frames of reference but finally translated into common coordinates, and share the same final common pathway, namely the same population of extraocular motoneurons. From clinical studies in humans and lesion studies in animals, it is generally accepted that voluntary saccadic eye movements are organized in horizontal and vertical Cartesian coordinates. However, this issue is not settled yet, because neural circuits for vertical saccades remain unidentified. We recently determined brainstem neural circuits from the superior colliculus to ocular motoneurons for horizontal and vertical saccades with combined electrophysiological and neuroanatomical techniques. Comparing well-known vestibuloocular pathways with our findings of commissural excitation and inhibition between both superior colliculi, we proposed that the saccade system uses the same frame of reference as the vestibuloocular system, common semicircular canal coordinate. This proposal is mainly based on marked similarities (1) between output neural circuitry from one superior colliculus to extraocular motoneurons and that from a respective canal to its innervating extraocular motoneurons, (2) of patterns of commissural reciprocal inhibitions between upward saccade system on one side and downward system on the other, and between anterior canal system on one side and posterior canal system on the other, and (3) between the neural circuits of saccade and quick phase of vestibular nystagmus sharing brainstem burst neurons. In support of the proposal, commissural excitation of the superior colliculi may help to maintain Listing's law in saccades in spite of using semicircular canal coordinate.
Background:
Saccadic eye movements are controlled by a network of parietal, frontal, striatal, cerebellar and brainstem regions. The saccadic peak velocity is an established biomarker of benzodiazepine effects, with benzodiazepines reliably reducing the peak velocity.
Aims:
In this study, we aimed to replicate the effects of benzodiazepines on peak velocity and we investigated effects on previously less studied measures of saccades. We also explored the roles of sex, task characteristics and the baseline variables age, intelligence and trait anxiety in these effects.
Method:
Healthy adults ( N = 34) performed a horizontal step prosaccade task under 1 mg lorazepam, 2 mg lorazepam and placebo in a double-blind, within-subjects design.
Results:
We replicated the dose-dependent reduction in peak velocity with lorazepam and showed that this effect is stronger for saccades to targets at smaller eccentricities. We also demonstrated that this effect is independent of sex and other baseline variables. Lorazepam effects were widespread, however, occurring on mean and variability measures of most saccadic variables. Additionally, there were sex-dependent lorazepam effects on spatial consistency of saccades, indicating more adverse effects in females.
Conclusions:
We conclude that saccadic peak velocity is a sensitive and robust biomarker of benzodiazepine effects. However, lorazepam has pronounced effects also on other parameters of horizontal saccades. Sex-dependent drug effects on spatial consistency may reflect cerebellar mechanisms, given the role of the cerebellum in saccadic spatial accuracy.
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