Biomedical subjects

Dora E Angelaki

Publications and source records attributed to Dora E Angelaki.

At least 19 recordsLinked to original sources

PubMed2004

Similar kinematic properties for ocular following and smooth pursuit eye movements.

Ocular following (OFR) is a short-latency visual stabilization response to the optic flow experienced during self-motion. It has been proposed that it represents the early component of optokinetic nystagmus (OKN) and that it is functionally linked to the vestibularly driven stabilization reflex during translation (translational vestibuloocular reflex, TVOR). Because no single eye movement can eliminate slip from the whole retina during translation, the OFR and the TVOR appear to be functionally related to maintaining visual acuity on the fovea. Other foveal-specific eye movements, like smooth pursuit and saccades, exhibit an eye-position-dependent torsional component, as dictated by what is known as the "half-angle rule" of Listing's law. In contrast, eye movements that stabilize images on the whole retina, such as the rotational vestibuloocular reflex (RVOR) and steady-state OKN do not. Consistent with the foveal stabilization hypothesis, it was recently shown that the TVOR is indeed characterized by an eye-position-dependent torsion, similar to pursuit eye movements. Here we have investigated whether the OFR exhibits three-dimensional kinematic properties consistent with a foveal response (i.e., similar to the TVOR and smooth pursuit eye movements) or with a whole-field stabilization function (similar to steady-state OKN). The OFR was elicited using 100-ms ramp motion of a full-field random dot pattern that moved horizontally at 20, 62, or 83 degrees/s. To study if an eye-position-dependent torsion is generated during the OFR, we varied the initial fixation position vertically within a range of +/-20 degrees . As a control, horizontal smooth pursuit eye movements were also elicited using step-ramp target motion (10, 20, or 30 degrees/s) at similar eccentric positions. We found that the OFR followed kinematic properties similar to those seen in pursuit and the TVOR with the eye-position-dependent torsional tilt of eye velocity having slopes that averaged 0.73 +/- 0.16 for OFR and 0.57 +/- 0.12 (means +/- SD) for pursuit. These findings support the notion that the OFR, like the TVOR and pursuit, are foveal image stabilization systems.

Animals↗

PubMed2004

Properties of cerebellar fastigial neurons during translation, rotation, and eye movements.

The most medial of the deep cerebellar nuclei, the fastigial nucleus (FN), receives sensory vestibular information and direct inhibition from the cerebellar vermis. We investigated the signal processing in the primate FN by recording single-unit activities during translational motion, rotational motion, and eye movements. Firing rate modulation during horizontal plane translation in the absence of eye movements was observed in all non-eye-movement-sensitive cells and 26% of the pursuit eye-movement-sensitive neurons in the caudal FN. Many non-eye-movement-sensitive cells recorded in the rostral FN of three fascicularis monkeys exhibited convergence of signals from both the otolith organs and the semicircular canals. At low frequencies of translation, the majority of these rostral FN cells changed their firing rates in phase with head velocity rather than linear acceleration. As frequency increased, FN vestibular neurons exhibited a wide range of response dynamics with most cells being characterized by increasing phase leads as a function of frequency. Unlike cells in the vestibular nuclei, none of the rostral FN cells responded to rotational motion alone, without simultaneously exhibiting sensitivity to translational motion. Modulation during earth-horizontal axis rotation was observed in more than half (77%) of the neurons, although with smaller gains than during translation. In contrast, only 47% of the cells changed their firing rates during earth-vertical axis rotations in the absence of a dynamic linear acceleration stimulus. These response properties suggest that the rostral FN represents a main processing center of otolith-driven information for inertial motion detection and spatial orientation.

Action Potentials↗

PubMed2004

Neurons compute internal models of the physical laws of motion.

A critical step in self-motion perception and spatial awareness is the integration of motion cues from multiple sensory organs that individually do not provide an accurate representation of the physical world. One of the best-studied sensory ambiguities is found in visual processing, and arises because of the inherent uncertainty in detecting the motion direction of an untextured contour moving within a small aperture. A similar sensory ambiguity arises in identifying the actual motion associated with linear accelerations sensed by the otolith organs in the inner ear. These internal linear accelerometers respond identically during translational motion (for example, running forward) and gravitational accelerations experienced as we reorient the head relative to gravity (that is, head tilt). Using new stimulus combinations, we identify here cerebellar and brainstem motion-sensitive neurons that compute a solution to the inertial motion detection problem. We show that the firing rates of these populations of neurons reflect the computations necessary to construct an internal model representation of the physical equations of motion.

Animals↗

PubMed2004

Multiple reference frames for motion in the primate cerebellum.

Knowledge of body motion through space is necessary for spatial orientation, self-motion perception, and postural control. Yet, sensory afferent signals may not directly provide such information to the brain. Because motion detected by the vestibular end organs is encoded in a head-fixed frame of reference, a coordinate transformation is thus required to encode body motion. In this study, we investigated whether cerebellar motion-sensitive neurons encode the translation of the body through space. We systematically changed both the direction of motion relative to the body and the static orientation of the head relative to the trunk. The activities of motion-sensitive neurons in the most medial of the deep cerebellar nuclei, the rostral fastigial nucleus, were compared with those in the brainstem vestibular nuclei. We found a distributed representation of reference frames for motion in the rostral fastigial nucleus, in contrast to cells in the vestibular nuclei, which primarily encoded motion in a head-fixed reference frame. This differential representation of motion-related information implies potential differences in the functional roles of these areas.

Acceleration↗

PubMed2004

An integrative neural network for detecting inertial motion and head orientation.

The ability to navigate in the world and execute appropriate behavioral responses depends critically on the contribution of the vestibular system to the detection of motion and spatial orientation. A complicating factor is that otolith afferents equivalently encode inertial and gravitational accelerations. Recent studies have demonstrated that the brain can resolve this sensory ambiguity by combining signals from both the otoliths and semicircular canal sensors, although it remains unknown how the brain integrates these sensory contributions to perform the nonlinear vector computations required to accurately detect head movement in space. Here, we illustrate how a physiologically relevant, nonlinear integrative neural network could be used to perform the required computations for inertial motion detection along the interaural head axis. The proposed model not only can simulate recent behavioral observations, including a translational vestibuloocular reflex driven by the semicircular canals, but also accounts for several previously unexplained characteristics of central neural responses such as complex otolith-canal convergence patterns and the prevalence of dynamically processed otolith signals. A key model prediction, implied by the required computations for tilt-translation discrimination, is a coordinate transformation of canal signals from a head-fixed to a spatial reference frame. As a result, cell responses may reflect canal signal contributions that cannot be easily detected or distinguished from otolith signals. New experimental protocols are proposed to characterize these cells and identify their contributions to spatial motion estimation. The proposed theoretical framework makes an essential first link between the computations for inertial acceleration detection derived from the physical laws of motion and the neural response properties predicted in a physiologically realistic network implementation.

Acceleration↗

PubMed2004

Viewing distance dependence of the vestibulo-ocular reflex during translation: extra-otolith influences.

Despite nearly perfect gaze stability during natural head movements, the amplitude of the vestibulo-ocular reflex during passive head and body translation (TVOR) has been consistently reported to be undercompensatory during near target viewing. Here we have compared the rhesus monkey TVOR during pure head and body translation with the eye movements generated during eccentric yaw rotations, where both semicircular canal and otolith signals are activated. We found a significant increase in both the near target TVOR amplitude and its viewing distance dependence during eccentric rotations, as compared to pure translations. We conclude that the simultaneous activation of the horizontal semicircular canals result in an improvement of the viewing distance-dependence of the rhesus monkey TVOR.

Animals↗

PubMed2004

Control of eye orientation: where does the brain's role end and the muscle's begin?

Our understanding of how the brain controls eye movements has benefited enormously from the comparison of neuronal activity with eye movements and the quantification of these relationships with mathematical models. Although these early studies focused on horizontal and vertical eye movements, recent behavioural and modelling studies have illustrated the importance, but also the complexity, of extending previous conclusions to the problems of controlling eye and head orientation in three dimensions (3-D). An important facet in understanding 3-D eye orientation and movement has been the discovery of mobile, soft-tissue sheaths or 'pulleys' in the orbit which might influence the pulling direction of extraocular muscles. Appropriately placed pulleys could generate the eye-position-dependent tilt of the ocular rotation axes which are characteristic for eye movements which follow Listing's law. Based on such pulley models of the oculomotor plant it has recently been proposed that a simple two-dimensional (2-D) neural controller would be sufficient to generate correct 3-D eye orientation and movement. In contrast to this apparent simplification in oculomotor control, multiple behavioural observations suggest that the visuo-motor transformations, as well as the premotor circuitry for saccades, pursuit eye movements and the vestibulo-ocular reflexes, must include a neural controller which operates in 3-D, even when considering an eye plant with pulleys. This review summarizes the most recent work and ideas on this controversy. In addition, by proposing directly testable hypotheses, we point out that, in analogy to the previously successful steps towards elucidating the neural control of horizontal eye movements, we need a quantitative characterization first of motoneuron and next of premotor neuron properties in 3-D before we can succeed in gaining further insight into the neural control of 3-D motor behaviours.

Animals↗

PubMed2004

Eyes on target: what neurons must do for the vestibuloocular reflex during linear motion.

A gaze-stabilization reflex that has been conserved throughout evolution is the rotational vestibuloocular reflex (RVOR), which keeps images stable on the entire retina during head rotation. An ethological newer reflex, the translational or linear VOR (TVOR), provides fast foveal image stabilization during linear motion. Whereas the sensorimotor processing has been extensively studied in the RVOR, much less is currently known about the neural organization of the TVOR. Here we summarize the computational problems faced by the system and the potential solutions that might be used by brain stem and cerebellar neurons participating in the VORs. First and foremost, recent experimental and theoretical evidence has shown that, contrary to popular beliefs, the sensory signals driving the TVOR arise from both the otolith organs and the semicircular canals. Additional unresolved issues include a scaling by both eye position and vergence angle as well as the temporal transformation of linear acceleration signals into eye-position commands. Behavioral differences between the RVOR and TVOR, as well as distinct differences in neuroanatomical and neurophysiological properties, raise multiple functional questions and computational issues, only some of which are readily understood. In this review, we provide a summary of what is known about the functional properties and neural substrates for this oculomotor system and outline some specific hypotheses about how sensory information is centrally processed to create motor commands for the VORs.

Animals↗

PubMed2003

Does head rotation contribute to gaze stability during passive translations?

Active translations of human subjects are nearly perfectly compensated by a combined rotation of both the eyes and the head. Because vestibuloocular reflex (VOR) gain is less than perfect during passive translations with near targets in head-fixed subjects, there is a possibility that the compensatory head rotation observed during natural behavior represents a vestibularly driven head reflex [translational vestibulocollic reflex (TVCR)]. The TVCR could elicit a horizontal rotation of the head during lateral linear acceleration that contributes to gaze stabilization. To investigate this hypothesis, we examined whether a horizontal rotation of the head contributes to gaze stability during passive lateral translation in rhesus monkeys whose head was free to rotate in the horizontal plane. Motion frequency was varied between 0.5 and 5 Hz while animals fixated targets at distances of 12-102 cm. We did not find evidence supporting the existence of a TVCR. Specifically, during motion at frequencies between 0.5 and 2 Hz, horizontal head rotation was negligible. During 4- and 5-Hz oscillations, there was a clear and consistent horizontal rotation of the head, but responses were always anticompensatory to gaze stabilization; that is, the head rotated in the same direction as head translation and oppositely to the direction of gaze rotation. Furthermore, there was no difference in gaze stability between the head-free and head-fixed conditions. Thus we conclude that the compensatory head rotation observed in human studies of active gaze movements could represent a strategy and/or a motor command contribution to gaze stabilization, rather than a simple vestibularly driven reflex.

Acceleration↗

PubMed2003

Dynamics of vestibular neurons during rotational motion in alert rhesus monkeys.

The temporal processing in the encoding of head rotation was investigated by comparing the dynamics of vestibular nuclei neurons with those of the regularly and irregularly firing semicircular canal afferents in alert rhesus monkeys. During earth-vertical axis rotations, neurons without eye movement sensitivity differed in their response dynamics from both regularly and irregularly firing semicircular canal afferents. At high frequencies, central responses increased in sensitivity and maintained phase leads of nearly 30 degrees relative to head velocity. These persistent high-frequency phase leads resembled those of irregularly firing (but not regularly firing) semicircular canal afferents. However, at low frequencies, central responses exhibited significantly smaller phase leads than those of irregularly firing semicircular canal afferents, and dynamics resembled more those of the regularly firing afferents. The response dynamics of central non-eye movement cells were significantly different from those of position-vestibular-pause and eye-head neurons (collectively referred to as eye movement cells). In contrast to the persistent phase leads of non-eye movement neurons, all eye movement cells modulated closely in phase with head velocity at all frequencies down to 0.05 Hz during visual suppression tasks. Vertical canal non-eye movement neurons that were insensitive to both translations and static head tilts led head velocity by approximately 5-30 degrees during high-frequency earth-horizontal axis rotations. Unlike the earth-vertical axis responses that led head velocity at low frequencies by as much as 20-40 degrees, vertical canal neurons only slightly led or even lagged behind head velocity during low-frequency earth-horizontal axis rotations. Posterior canal central non-eye movement cells lagged behind head velocity significantly more than anterior canal neurons. These frequency dependencies of central vestibular neurons in comparison with those of the afferents suggest that both low- and high-pass filtering might be necessary to convert primary semicircular canal afferent response dynamics to central neuron ones.

Action Potentials↗

PubMed2003

Spatial tuning and dynamics of vestibular semicircular canal afferents in rhesus monkeys.

Rotational head motion in vertebrates is detected by the three semicircular canals of the vestibular system whose innervating primary afferent fibers encode movement information in specific head planes. In order to further investigate the nature of vestibular central processing of rotational motion in rhesus monkeys, it was first necessary to quantify afferent information coding in this species. Extracellular recordings were performed to determine the spatial and dynamic properties of semicircular canal afferents to rotational motion in awake rhesus monkeys. We found that the afferents innervating specific semicircular canals had maximum sensitivity vectors that were mutually orthogonal. Similar to other species, afferent response dynamics varied, with regular firing afferents having increased long time constants ( t(1)), decreased cupula velocity time constants ( t(v)), and decreased fractional order dynamic operator values ( s(k)) as compared to irregular firing afferents.

Action Potentials↗

PubMed2003

Resolution of sensory ambiguities for gaze stabilization requires a second neural integrator.

The ability to simultaneously move in the world and maintain stable visual perception depends critically on the contribution of vestibulo-ocular reflexes (VORs) to gaze stabilization. It is traditionally believed that semicircular canal signals drive compensatory responses to rotational head disturbances (rotational VOR), whereas otolith signals compensate for translational movements [translational VOR (TVOR)]. However, a sensory ambiguity exists because otolith afferents are activated similarly during head translations and reorientations relative to gravity (i.e., tilts). Extra-otolith cues are, therefore, necessary to ensure that dynamic head tilts do not elicit a TVOR. To investigate how extra-otolith signals contribute, we characterized the temporal and viewing distance-dependent properties of a TVOR elicited in the absence of a lateral acceleration stimulus to the otoliths during combined translational/rotational motion. We show that, in addition to otolith signals, angular head position signals derived by integrating sensory canal information drive the TVOR. A physiological basis for these results is proposed in a model with two distinct integration steps. Upstream of the well known oculomotor velocity-to-position neural integrator, the model incorporates a separate integration element that could represent the "velocity storage integrator," whose functional role in the oculomotor system has so far remained controversial. We propose that a key functional purpose of the velocity storage network is to temporally integrate semicircular canal signals, so that they may be used to extract translation information from ambiguous otolith afferent signals in the natural and functionally relevant bandwidth of head movements.

Animals↗

PubMed2003

Do visual cues contribute to the neural estimate of viewing distance used by the oculomotor system?

Perceived shape and depth judgments that require knowledge of viewing distance are strongly influenced by both vergence angle and the pattern of vertical disparities across large visual fields. On the basis of this established contribution of visual cues to the neural estimate of viewing distance, we hypothesized that the oculomotor system would also make use of high-level visual cues to distance. To address this hypothesis, we investigated how compensatory eye movements during whole-body translation scale with viewing distance. Monkeys viewed large-field (85 x 68 degrees ) random-dot stereograms that were rear projected onto a fixed screen and simulated either a textured wall or pyramid at different viewing distances. In these stereograms, we independently manipulated vergence angle, horizontal and vertical disparity gradients, relative horizontal disparities, and textural cues to viewing distance. For comparison, random-dot patterns were also projected onto a moveable screen placed at different physical distances from the animal. Several cycles of left-right sinusoidal motion of the monkey at 5 Hz were interleaved with several cycles of motion in darkness, and the relationship between eye movement responses and viewing distance was quantified. As expected from previous work, the amplitude of compensatory eye movements depended strongly on vergence angle. Although visual cues to distance had a statistically significant effect on eye movements, these effects were approximately 20-fold weaker than the effect of vergence angle. We conclude that sensory and motor systems do not share a common neural estimate of viewing distance and that the oculomotor system relies far less on visual cues than the perceptual system.

Animals↗

PubMed2003

Vestibular contributions to gaze stability during transient forward and backward motion.

The accuracy with which the vestibular system anticipates and compensates for the visual consequences of translation during forward and backward movements was investigated with transient motion profiles in rhesus monkeys trained to fixate targets on an isovergence screen. Early during motion when visuomotor reflexes remain relatively ineffective and vestibular-driven mechanisms have an important role for controlling the movement of the eyes, a large asymmetry was observed for forward and backward heading directions. During forward motion, ocular velocity gains increased steeply and reached near unity gains as early as 40-50 ms after motion onset. In addition, instantaneous directional errors also remained <10 degrees for forward headings. In contrast, backward motion was characterized by smaller vestibular gains and larger directional errors during the first 70 ms of the movement. To evaluate the accumulated retinal slip and vergence errors during the early epochs of motion when vestibular-driven mechanisms dominate gaze stability, the movement of a virtual fixation point defined by the intersection of the two gaze lines was quantitatively compared with the respective movement of the extinguished target in head coordinates. Both conjugate retinal slip and vergence errors were <0.2 degrees during the first 70 ms of the movement, with forward motion conjugate errors typically being smaller as compared with backward motion directions. Thus vestibularly driven gaze stabilization mechanisms can effectively minimize conjugate retinal slip errors as well as keep binocular disparity errors low during the open loop interval of head movement.

Animals↗

PubMed2003

Premotor neurons encode torsional eye velocity during smooth-pursuit eye movements.

Responses to horizontal and vertical ocular pursuit and head and body rotation in multiple planes were recorded in eye movement-sensitive neurons in the rostral vestibular nuclei (VN) of two rhesus monkeys. When tested during pursuit through primary eye position, the majority of the cells preferred either horizontal or vertical target motion. During pursuit of targets that moved horizontally at different vertical eccentricities or vertically at different horizontal eccentricities, eye angular velocity has been shown to include a torsional component the amplitude of which is proportional to half the gaze angle ("half-angle rule" of Listing's law). Approximately half of the neurons, the majority of which were characterized as "vertical" during pursuit through primary position, exhibited significant changes in their response gain and/or phase as a function of gaze eccentricity during pursuit, as if they were also sensitive to torsional eye velocity. Multiple linear regression analysis revealed a significant contribution of torsional eye movement sensitivity to the responsiveness of the cells. These findings suggest that many VN neurons encode three-dimensional angular velocity, rather than the two-dimensional derivative of eye position, during smooth-pursuit eye movements. Although no clear clustering of pursuit preferred-direction vectors along the semicircular canal axes was observed, the sensitivity of VN neurons to torsional eye movements might reflect a preservation of similar premotor coding of visual and vestibular-driven slow eye movements for both lateral-eyed and foveate species.

Animals↗

PubMed2003

Foveal versus full-field visual stabilization strategies for translational and rotational head movements.

Because we view the world from a constantly shifting platform when our head and body move in space, vestibular and visuomotor reflexes are critical to maintain visual acuity. In contrast to the phylogenetically old rotational vestibulo-ocular reflex (RVOR), it has been proposed that the translational vestibulo-ocular reflex (TVOR) represents a newly developed vestibular-driven mechanism that is important for foveal vision and stereopsis. To investigate the hypothesis that the function of the TVOR is indeed related to foveal (as opposed to full-field) image stabilization, we compared the three-dimensional ocular kinematics during lateral translation and rotational movements with those during pursuit of a small moving target in four rhesus monkeys. Specifically, we tested whether TVOR rotation axes tilt with eye position as in visually driven systems such as pursuit, or whether they stay relatively fixed in the head as in the RVOR. We found a significant dependence of three-dimensional eye velocity on eye position that was independent of viewing distance and viewing conditions (full-field, single target, or complete darkness). The slopes for this eye-position dependence averaged 0.7 +/- 0.07 for the TVOR, compared with 0.6 +/- 0.07 for visually guided pursuit eye movements and 0.18 +/- 0.09 for the RVOR. Because the torsional tilt versus vertical gaze slopes during translation were slightly higher than those during pursuit, three-dimensional eye movements during translation could partly reflect a compromise between the two different solutions for foveal gaze control, that of Listing's law and minimum velocity strategies. These results with respect to three-dimensional kinematics provide additional support for a functional difference in the two vestibular-driven mechanisms for visual stability during rotations and translations and establish clearly the functional goal of the TVOR as that for foveal visual acuity.

Animals↗

PubMed2003

Accuracy of saccades to remembered targets as a function of body orientation in space.

A vertical asymmetry in memory-guided saccadic eye movements has been previously demonstrated in humans and in rhesus monkeys. In the upright orientation, saccades generally land several degrees above the target. The origin of this asymmetry has remained unknown. In this study, we investigated whether the asymmetry in memory saccades is dependent on body orientation in space. Thus animals performed memory saccades in four different body orientations: upright, left-side-down (LSD), right-side-down (RSD), and supine. Data in all three rhesus monkeys confirm previous observations regarding a significant upward vertical asymmetry. Saccade errors made from LSD and RSD postures were partitioned into components made along the axis of gravity and along the vertical body axis. Up/down asymmetry persisted only in body coordinates but not in gravity coordinates. However, this asymmetry was generally reduced in tilted positions. Therefore the upward bias seen in memory saccades is egocentric although orientation in space might play a modulatory role.

Animals↗

PubMed2003

Gravity modulates Listing's plane orientation during both pursuit and saccades.

Previous studies have shown that the spatial organization of all eye orientations during visually guided saccadic eye movements (Listing's plane) varies systematically as a function of static and dynamic head orientation in space. Here we tested if a similar organization also applies to the spatial orientation of eye positions during smooth pursuit eye movements. Specifically, we characterized the three-dimensional distribution of eye positions during horizontal and vertical pursuit (0.1 Hz, +/-15 degrees and 0.5 Hz, +/-8 degrees) at different eccentricities and elevations while rhesus monkeys were sitting upright or being statically tilted in different roll and pitch positions. We found that the spatial organization of eye positions during smooth pursuit depends on static orientation in space, similarly as during visually guided saccades and fixations. In support of recent modeling studies, these results are consistent with a role of gravity on defining the parameters of Listing's law.

Animals↗