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Biomedical subjects

Dora E Angelaki

Publications and source records attributed to Dora E Angelaki.

At least 19 recordsLinked to original sources
PubMed2006

Deficits and recovery in visuospatial memory during head motion after bilateral labyrinthine lesion.

To keep a stable internal representation of the environment as we move, extraretinal sensory or motor cues are critical for updating neural maps of visual space. Using a memory-saccade task, we studied whether visuospatial updating uses vestibular information. Specifically, we tested whether trained rhesus monkeys maintain the ability to update the conjugate and vergence components of memory-guided eye movements in response to passive translational or rotational head and body movements after bilateral labyrinthine lesion. We found that lesioned animals were acutely compromised in generating the appropriate horizontal versional responses necessary to update the directional goal of memory-guided eye movements after leftward or rightward rotation/translation. This compromised function recovered in the long term, likely using extravestibular (e.g., somatosensory) signals, such that nearly normal performance was observed 4 mo after the lesion. Animals also lost their ability to adjust memory vergence to account for relative distance changes after motion in depth. Not only were these depth deficits larger than the respective effects on version, but they also showed little recovery. We conclude that intact labyrinthine signals are functionally useful for proper visuospatial memory updating during passive head and body movements.

Animals↗
PubMed2006

Scaling of the fore-aft vestibulo-ocular reflex by eye position during smooth pursuit.

An eye position signal scales the amplitude of compensatory eye velocity in the translational vestibulo-ocular reflex (TVOR). To investigate the origin of such a modulatory signal, we studied the kinematics of the fore-aft TVOR as rhesus monkeys pursued a horizontally moving target at velocities between 0.5 and 30 degrees /s. We found that the "V-shaped" curve of the fore-aft TVOR amplitude as a function of eye position was shifted opposite to the direction of pursuit eye movement. As a result, the tip of the V-shaped curve that occurred close to zero eye position during steady-state fixation was shifted to the right during leftward pursuit and to the left during rightward pursuit eye movements. The faster the pursuit velocity the larger the observed shift. These results suggest that the scaling of the TVOR can precede actual eye position changes by several tens of milliseconds, which averaged 169 +/- 87 ms in three rhesus monkeys. Thus, central motor commands, rather than low-level efference copy or proprioceptive information, may be the signals scaling TVOR amplitude.

Algorithms↗
PubMed2006

Three-dimensional kinematics at the level of the oculomotor plant.

Motor systems often require that superfluous degrees of freedom be constrained. For the oculomotor system, a redundancy in the degrees of freedom occurs during visually guided eye movements and is solved by implementing Listing's law and the half-angle rule, kinematic constraints that limit the range of eye positions and angular velocities used by the eyes. These constraints have been attributed either to neurally generated commands or to the physical mechanics of the eye and its surrounding muscles and tissues (i.e., the ocular plant). To directly test whether the ocular plant implements the half-angle rule, critical to the maintenance of Listing's law, we microstimulated the abducens nerve with the eye at different initial vertical eye positions. We report that the electrically evoked eye velocity exhibits the same eye position dependence as seen in visually guided smooth-pursuit eye movements. These results support an important role for the ocular plant in providing a solution to the degrees-of-freedom problem during eye movements.

Abducens Nerve↗
PubMed2006

Neural correlates of the dependence of compensatory eye movements during translation on target distance and eccentricity.

To stabilize objects of interest on the fovea during translation, vestibular-driven compensatory eye movements [translational vestibulo-ocular reflex (TVOR)] must scale with both target distance and eccentricity. To identify the neural correlates of these properties, we recorded from different groups of eye movement-sensitive neurons in the prepositus hypoglossi and vestibular nuclei of macaque monkeys during lateral and fore-aft displacements. All neuron types exhibited some increase in modulation amplitude as a function of target distance during high-frequency (4 Hz) lateral motion in darkness, with slopes that were correlated with the cell's pursuit gain, but not eye position sensitivity. Vergence angle dependence was largest for burst-tonic (BT) and contralateral eye-head (EH) neurons and smallest for ipsilateral EH and position-vestibular-pause (PVP) cells. On the other hand, the EH and PVP neurons with ipsilateral eye movement preferences exhibited the largest vergence-independent responses, which would be inappropriate to drive the TVOR. In addition to target distance, the TVOR also scales with target eccentricity, as evidenced during fore-aft motion, where eye velocity amplitude exhibits a "V-shaped " dependence and phase shifts 180 degrees for right versus left eye positions. Both the modulation amplitude and phase of BT and contralateral EH cells scaled with eye position, similar to the evoked eye movements during fore-aft motion. In contrast, the response modulation of ipsilateral EH and PVP cells during fore-aft motion was characterized by neither the V-shaped scaling nor the phase reversal. These results show that distinct premotor cell types carry neural signals that are appropriately scaled by vergence angle and eye position to generate the geometrically appropriate compensatory eye movements in the translational vestibulo-ocular reflex.

Accommodation, Ocular↗
PubMed2006

Foveal visual strategy during self-motion is independent of spatial attention.

Translational self-motion disturbs the stability of retinal images by inducing a pattern of retinal optic flow that cannot be compensated globally by a single eye movement. The eyes must rotate by different amounts, depending on which spatial location needs to be stabilized on the retina. However, compensatory eye movements during steady fixation are always such as to maintain visual acuity on the fovea at the expense of significant image slip on the peripheral retina. We investigated whether such a foveal visual strategy during translation is hard-wired or whether it embeds enough flexibility to also allow for behaviorally relevant objects outside the foveae to be stabilized preferentially on the retinas. Monkeys were moved forward or backward and leftward or rightward passively in darkness while planning a saccade or bar release to peripheral dimmed targets. By comparing the eye movements made during these tasks with those under conditions of steady fixation, we found that the motion-induced eye movements depended only on current fixation. This was true even during the last milliseconds just before a saccade to the peripheral target. We conclude that the foveal stabilization strategy is invariant and solely dependent on current eye position, a strategy that is optimal for both processing speed and efficiency in the extraction of heading information from retinal flow during self-motion.

Adaptation, Physiological↗
PubMed2006

Visual and nonvisual contributions to three-dimensional heading selectivity in the medial superior temporal area.

Robust perception of self-motion requires integration of visual motion signals with nonvisual cues. Neurons in the dorsal subdivision of the medial superior temporal area (MSTd) may be involved in this sensory integration, because they respond selectively to global patterns of optic flow, as well as translational motion in darkness. Using a virtual-reality system, we have characterized the three-dimensional (3D) tuning of MSTd neurons to heading directions defined by optic flow alone, inertial motion alone, and congruent combinations of the two cues. Among 255 MSTd neurons, 98% exhibited significant 3D heading tuning in response to optic flow, whereas 64% were selective for heading defined by inertial motion. Heading preferences for visual and inertial motion could be aligned but were just as frequently opposite. Moreover, heading selectivity in response to congruent visual/vestibular stimulation was typically weaker than that obtained using optic flow alone, and heading preferences under congruent stimulation were dominated by the visual input. Thus, MSTd neurons generally did not integrate visual and nonvisual cues to achieve better heading selectivity. A simple two-layer neural network, which received eye-centered visual inputs and head-centered vestibular inputs, reproduced the major features of the MSTd data. The network was trained to compute heading in a head-centered reference frame under all stimulus conditions, such that it performed a selective reference-frame transformation of visual, but not vestibular, signals. The similarity between network hidden units and MSTd neurons suggests that MSTd may be an early stage of sensory convergence involved in transforming optic flow information into a (head-centered) reference frame that facilitates integration with vestibular signals.

Action Potentials↗
PubMed2005

Differences in the accuracy of human visuospatial memory after yaw and roll rotations.

Our ability to keep track of objects in the environment, even as we move, has been attributed to various cues including efference copies, vestibular signals, proprioception, and gravitational cues. However, the presence of some cues, such as gravity, may not be used to the same extent by different axes of motion (e.g., yaw vs. roll). We tested whether changes in gravitational cues can be used to improve visuospatial updating performance for yaw rotations as previously shown for roll. We found differences in updating for yaw and roll rotations in that yaw updating is not only associated with larger systematic errors but is also not facilitated by gravity in the same way as roll updating.

Adult↗
PubMed2005

Updating visual space during motion in depth.

Whether we are riding in a car or walking, our internal map of the environment must be continuously updated to maintain spatial constancy. Using a memory eye movement task, we examined whether nonhuman primates can keep track of changes in the distance of nearby objects when moved toward or away from them. We report that memory-guided eye movements take into account the change in distance traveled, illustrating that monkeys can update retinal disparity information in order to reconstruct three-dimensional visual space during motion in depth. This ability was compromised after destruction of the vestibular labyrinths, suggesting that the extraretinal signals needed for updating can arise from vestibular information signaling self-motion through space.

Analysis of Variance↗
PubMed2005

Sensory convergence solves a motion ambiguity problem.

Our inner ear is equipped with a set of linear accelerometers, the otolith organs, that sense the inertial accelerations experienced during self-motion. However, as Einstein pointed out nearly a century ago, this signal would by itself be insufficient to detect our real movement, because gravity, another form of linear acceleration, and self-motion are sensed identically by otolith afferents. To deal with this ambiguity, it was proposed that neural populations in the pons and midline cerebellum compute an independent, internal estimate of gravity using signals arising from the vestibular rotation sensors, the semicircular canals. This hypothesis, regarding a causal relationship between firing rates and postulated sensory contributions to inertial motion estimation, has been directly tested here by recording neural activities before and after inactivation of the semicircular canals. We show that, unlike cells in normal animals, the gravity component of neural responses was nearly absent in canal-inactivated animals. We conclude that, through integration of temporally matched, multimodal information, neurons derive the mathematical signals predicted by the equations describing the physics of the outside world.

Animals↗
PubMed2005

Sensory vestibular contributions to constructing internal models of self-motion.

The ability to navigate in the world and execute appropriate behavioral and motor responses depends critically on our capacity to construct an accurate internal representation of our current motion and orientation in space. Vestibular sensory signals are among those that may make an essential contribution to the construction of such 'internal models'. Movement in a gravitational environment represents a situation where the construction of internal models becomes particularly important because the otolith organs, like any linear accelerometer, sense inertial and gravitational accelerations equivalently. Otolith afferents thus provide inherently ambiguous motion information, as they respond identically to translation and head reorientation relative to gravity. Resolution of this ambiguity requires the nonlinear integration of linear acceleration and angular velocity cues, as predicted by the physical equations of motion. Here, we summarize evidence that during translations and tilts from upright the firing rates of brainstem and cerebellar neurons encode a combination of dynamically processed semicircular canal and otolith signals appropriate to construct an internal model representation of the computations required for inertial motion detection.

Adaptation, Physiological↗
PubMed2005

Do motoneurons encode the noncommutativity of ocular rotations?

As we look around, the orientation of our eyes depends on the order of the rotations that are carried out, a mathematical feature of rotatory motions known as noncommutativity. Theorists and experimentalists continue to debate how biological systems deal with this property when generating kinematically appropriate movements. Some believe that this is always done by neural commands to a simplified eye plant. Others have postulated that noncommutativity is implemented solely by the mechanical properties of the eyeball. Here we directly examined what the brain tells the muscles, by recording motoneuron activities as monkeys made eye movements. We found that vertical recti and superior/inferior oblique motoneurons, which drive sensory-generated torsional eye movements, do not modulate their firing rates according to the noncommutative-driven torsion during pursuit. We conclude that part of the solution for kinematically appropriate eye movements is found in the mechanical properties of the eyeball, although neural computations remain necessary and become increasingly important during head movements.

Action Potentials↗
PubMed2005

Primate memory saccade amplitude after intervened motion depends on target distance.

To keep a stable internal representation of the visual world as our eyes, head, and body move around, humans and monkeys must continuously adjust neural maps of visual space using extraretinal sensory or motor cues. When such movements include translation, the amount of body displacement must be weighted differently in the updating of far versus near targets. Using a memory-saccade task, we have investigated whether nonhuman primates can benefit from this geometry when passively moved sideways. We report that monkeys made appropriate memory saccades, taking into account not only the amplitude and nature (rotation vs. translation) of the movement, but also the distance of the memorized target: i.e., the amplitude of memory saccades was larger for near versus far targets. The scaling by viewing distance, however, was less than geometrically required, such that memory saccades consistently undershot near targets. Such a less-than-ideal scaling of memory saccades is reminiscent of the viewing distance-dependent properties of the vestibuloocular reflex. We propose that a similar viewing distance-dependent vestibular signal is used as an extraretinal compensation for the visuomotor consequences of the geometry of motion parallax by scaling both memory saccades and reflexive eye movements during motion through space.

Animals↗
PubMed2005

Roles of gravitational cues and efference copy signals in the rotational updating of memory saccades.

Primates are able to localize a briefly flashed target despite intervening movements of the eyes, head, or body. This ability, often referred to as updating, requires extraretinal signals related to the intervening movement. With active roll rotations of the head from an upright position it has been shown that the updating mechanism is 3-dimensional, robust, and geometrically sophisticated. Here we examine whether such a rotational updating mechanism operates during passive motion both with and without inertial cues about head/body position in space. Subjects were rotated from either an upright or supine position, about a nasal-occipital axis, briefly shown a world-fixed target, rotated back to their original position, and then asked to saccade to the remembered target location. Using this paradigm, we tested subjects' abilities to update from various tilt angles (0, +/-30, +/-45, +/-90 degrees), to 8 target directions and 2 target eccentricities. In the upright condition, subjects accurately updated the remembered locations from all tilt angles independent of target direction or eccentricity. Slopes of directional errors versus tilt angle ranged from -0.011 to 0.15, and were significantly different from a slope of 1 (no compensation for head-in-space roll) and a slope of 0.9 (no compensation for eye-in-space roll). Because the eyes, head, and body were fixed throughout these passive movements, subjects could not use efference copies or neck proprioceptive cues to assess the amount of tilt, suggesting that vestibular signals and/or body proprioceptive cues suffice for updating. In the supine condition, where gravitational signals could not contribute, slopes ranged from 0.60 to 0.82, indicating poor updating performance. Thus information specifying the body's orientation relative to gravity is critical for maintaining spatial constancy and for distinguishing body-fixed versus world-fixed reference frames.

Adult↗
PubMed2005

Pursuit--vestibular interactions in brain stem neurons during rotation and translation.

Under natural conditions, the vestibular and pursuit systems work synergistically to stabilize the visual scene during movement. How translational vestibular signals [translational vestibuloocular reflex (TVOR)] are processed in the premotor pathways for slow eye movements continues to remain a challenging question. To further our understanding of how premotor neurons contribute to this processing, we recorded neural activities from the prepositus and rostral medial vestibular nuclei in macaque monkeys. Vestibular neurons were tested during 0.5-Hz rotation and lateral translation (both with gaze stable and during VOR cancellation tasks), as well as during smooth pursuit eye movements. Data were collected at two different viewing distances, 80 and 20 cm. Based on their responses to rotation and pursuit, eye-movement-sensitive neurons were classified into position-vestibular-pause (PVP) neurons, eye-head (EH) neurons, and burst-tonic (BT) cells. We found that approximately half of the type II PVP and EH neurons with ipsilateral eye movement preference were modulated during TVOR cancellation. In contrast, few of the EH and none of the type I PVP cells with contralateral eye movement preference modulated during translation in the absence of eye movements; nor did any of the BT neurons change their firing rates during TVOR cancellation. Of the type II PVP and EH neurons that modulated during TVOR cancellation, cell firing rates increased for either ipsilateral or contralateral displacement, a property that could not be predicted on the basis of their rotational or pursuit responses. In contrast, under stable gaze conditions, all neuron types, including EH cells, were modulated during translation according to their ipsilateral/contralateral preference for pursuit eye movements. Differences in translational response sensitivities for far versus near targets were seen only in type II PVP and EH cells. There was no effect of viewing distance on response phase for any cell type. When expressed relative to motor output, neural sensitivities during translation (although not during rotation) and pursuit were equivalent, particularly for the 20-cm viewing distance. These results suggest that neural activities during the TVOR were more motorlike compared with cell responses during the rotational vestibuloocular reflex (RVOR). We also found that neural responses under stable gaze conditions could not always be predicted by a linear vectorial addition of the cell activities during pursuit and VOR cancellation. The departure from linearity was more pronounced for the TVOR under near-viewing conditions. These results extend previous observations for the neural processing of otolith signals within the premotor circuitry that generates the RVOR and smooth pursuit eye movements.

Action Potentials↗
PubMed2005

Self-motion-induced eye movements: effects on visual acuity and navigation.

Self-motion disturbs the stability of retinal images by inducing optic flow. Objects of interest need to be fixated or tracked, yet these eye movements can infringe on the experienced retinal flow that is important for visual navigation. Separating the components of optic flow caused by an eye movement from those due to self-motion, as well as using optic flow for visual navigation while simultaneously maintaining visual acuity on near targets, represent key challenges for the visual system. Here we summarize recent advances in our understanding of how the visuomotor and vestibulomotor systems function and interact, given the complex task of compensating for instabilities of retinal images, which typically vary as a function of retinal location and differ for each eye.

Adaptation, Physiological↗
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↗