"Active" and "passive" learning of three-dimensional object structure within an immersive virtual reality environment.

We used a fully immersive virtual reality environment to study whether actively interacting with objects would effect subsequent recognition, when compared with passively observing the same objects. We found that when participants learned object structure by actively rotating the objects, the objects were recognized faster during a subsequent recognition task than when object structure was learned through passive observation. We also found that participants focused their study time during active exploration on a limited number of object views, while ignoring other views. Overall, our results suggest that allowing active exploration of an object during initial learning can facilitate recognition of that object, perhaps owing to the control that the participant has over the object views upon which they can focus. The virtual reality environment is ideal for studying such processes, allowing realistic interaction with objects while maintaining experimenter control.

Eye position sense contributes to the judgement of slant.

We measured monocular judgements of the slant of a cube face while varying eye position in the absence of stereoscopic and external lighting cues. Errors were found to be small, only 10% on average of the cube's eccentricity. Two factors appear to have contributed approximately equally to this error: an underestimate of cube slant as seen by the eye and an underestimate of eye position. When prism adaptation altered the sensed eye position, the pattern of slant judgements changed to reflect the altered sense of eye position.

Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements.

In humans, functional imaging studies have demonstrated a homologue of the macaque motion complex, MT+ [suggested to contain both middle temporal (MT) and medial superior temporal (MST)], in the ascending limb of the inferior temporal sulcus. In the macaque monkey, motion-sensitive areas MT and MST are adjacent in the superior temporal sulcus. Electrophysiological research has demonstrated that while MT receptive fields primarily encode the contralateral visual field, MST dorsal (MSTd) receptive fields extend well into the ipsilateral visual field. Additionally, macaque MST has been shown to receive extraretinal smooth-pursuit eye-movement signals, whereas MT does not. We used functional magnetic resonance imaging (fMRI) and the neural properties that had been observed in monkeys to distinguish putative human areas MT from MST. Optic flow stimuli placed in the full field, or contralateral field only, produced a large cluster of functional activation in our subjects consistent with previous reports of human area MT+. Ipsilateral optic flow stimuli limited to the peripheral retina produced activation only in an anterior subsection of the MT+ complex, likely corresponding to putative MSTd. During visual pursuit of a single target, a large portion of the MT+ complex was activated. However, during nonvisual pursuit, only the anterolateral portion of the MT+ complex was activated. This subsection of the MT+ cluster could correspond to putative MSTl (lateral). In summary, we observed three distinct subregions of the human MT+ complex that were arranged in a manner similar to that seen in the monkey.

Functional MRI activity in the thalamus and occipital cortex of anesthetized dogs induced by monocular and binocular stimulation.

The neuroanatomy of the mammalian visual system has received considerable attention through electrophysiological study of cats and non-human primates, and through neuroimaging of humans. Canine neuroanatomy, however, has received much less attention, limiting our understanding of canine vision and visual pathways. As an early step in applying blood oxygenation level dependant (BOLD) functional magnetic resonance imaging (fMRI) for veterinary use, we compared visual activity in the thalamus and occipital cortex of anesthetized dogs presented with binocular and monocular visual stimuli. Activity in the left and right thalamus and occipital cortex during monocular stimulation was also compared. Six beagles were presented with a vertical grating visual stimulus and scanned at 4 Tesla. Each dog was scanned twice under each of 3 anesthetic protocols (isoflurane, propofol, and fentanyl/midazolam). We found: 1) significant BOLD activation in the lateral geniculate nucleus (LGN) of the thalamus and the occipital cortex; 2) a significantly larger area of activation in the LGN during monocular stimulation than during binocular stimulation; and 3) that activity in the hemisphere contralateral to the stimulus was not significantly greater than that ipsilateral to it.

A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing.

An anti-saccade, which is a saccade directed toward a mirror-symmetrical position in the opposite visual field relative to the visual stimulus, involves at least three separate operations: covert orienting, response suppression, and coordinate transformation. The distinction between pro- and anti-saccades can also be applied to pointing. We used fMRI to compare patterns of brain activation during pro- and anti-movements, to determine whether or not additional areas become active during the production of anti-movements. In parietal cortex, an inferior network was active during both saccades and pointing that included three foci along the intraparietal sulcus: 1) a posterior superior parietal area (pSPR), more active during the anti-tasks; 2) a middle inferior parietal area (mIPR), active only during the anti-tasks; and 3) an anterior inferior parietal area (aIPR), equally active for pro- and anti-movement. A superior parietal network was active during pointing but not saccades and included the following: 1) a medial region, active during anti- but not pro-pointing (mSPR); 2) an anterior and medial region, more active during pro-pointing (aSPR); and 3) an anterior and lateral region, equally active for pro- and anti-pointing (lSPR). In frontal cortex, areas selectively active during anti-movement were adjacent and anterior to areas that were active during both the anti- and pro-tasks, i.e., were anterior to the frontal eye field and the supplementary motor area. All saccade areas were also active during pointing. In contrast, foci in the dorsal premotor area, the anterior superior frontal region, and anterior cingulate were active during pointing but not saccades. In summary, pointing with central gaze activates a frontoparietal network that includes the saccade network. The operations required for the production of anti-movements recruited additional frontoparietal areas.

Eye position signal modulates a human parietal pointing region during memory-guided movements.

Using functional magnetic resonance imaging, we examined the signal in parietal regions that were selectively activated during delayed pointing to flashed visual targets and determined whether this signal was dependent on the fixation position of the eyes. Delayed pointing activated a bilateral parietal area in the intraparietal sulcus (rIPS), rostral/anterior to areas activated by saccades. During right-hand pointing to centrally located targets, the left rIPS region showed a significant increase in activation when the eye position was rightward compared with leftward. As expected, activation in motor cortex showed no modulation when only eye position changed. During pointing to retinotopically identical targets, the left rIPS region again showed a significant increased signal when the eye position was rightward compared with leftward. Conversely, when pointing with the left arm, the right rIPS showed an increase in signal when eye position was leftward compared with rightward. The results suggest that the human parietal hand/arm movement region (rIPS), like monkey parietal areas (Andersen et al., 1985), exhibits an eye position modulation of its activity; modulation that may be used to transform the coordinates of the retinotopically coded target position into a motor error command appropriate for the wrist.

Curvature of visual space under vertical eye rotation: implications for spatial vision and visuomotor control.

Most models of spatial vision and visuomotor control reconstruct visual space by adding a vector representing the site of retinal stimulation to another vector representing gaze angle. However, this scheme fails to account for the curvatures in retinal projection produced by rotatory displacements in eye orientation. In particular, our simulations demonstrate that even simple vertical eye rotation changes the curvature of horizontal retinal projections with respect to eye-fixed retinal landmarks. We confirmed the existence of such curvatures by measuring target direction in eye coordinates in which the retinotopic representation of horizontally displaced targets curved obliquely as a function of vertical eye orientation. We then asked subjects to point (open loop) toward briefly flashed targets at various points along these lines of curvature. The vector-addition model predicted errors in pointing trajectory as a function of eye orientation. In contrast, with only minor exceptions, actual subjects showed no such errors, showing a complete neural compensation for the eye position-dependent geometry of retinal curvatures. Rather than bolstering the traditional model with additional corrective mechanisms for these nonlinear effects, we suggest that the complete geometry of retinal projection can be decoded through a single multiplicative comparison with three-dimensional eye orientation. Moreover, because the visuomotor transformation for pointing involves specific parietal and frontal cortical processes, our experiment implicates specific regions of cortex in such nonlinear transformations.

Recovery of fMRI activation in motion area MT following storage of the motion aftereffect.

We used functional magnetic resonance imaging (fMRI) during storage of the motion aftereffect (MAE) to examine the relationship between motion perception and neural activity in the human cortical motion complex MT+ (including area MT and adjacent motion-selective cortex). MT+ responds not only to physical motion but also to illusory motion, as in the MAE when subjects who have adapted to continuous motion report that a subsequent stationary test stimulus appears to move in the opposite direction. In the phenomenon of storage, the total decay time of the MAE is extended by inserting a dark period between adaptation and test phases. That is, when the static test pattern is presented after a storage period equal in duration to the normal MAE, the illusory motion reappears for almost as long as the original effect despite the delay. We examined fMRI activation in MT+ during and after storage. Seven subjects viewed continuous motion, followed either by an undelayed stationary test (immediate MAE) or by a completely dark storage interval preceding the test (stored MAE). Like the perceptual effect, activity in MT+ dropped during the storage interval then rebounded to reach a level much higher than after the same delay without storage. Although MT+ activity was slightly enhanced during the storage period following adaptation to continuous motion (compared with a control sequence in which the adaptation grating oscillated and no MAE was perceived), this enhancement was much less than that observed during the perceptual phenomenon. These results indicate that following adaptation, activity in MT+ is pronounced only with the presentation of an appropriate visual stimulus, during which the MAE is perceived.

Visual test of Listing's law during vergence.

A simple visual test was used to measure how much Listing's plane rotates as a function of the vergence angle. This test measured the elevation-dependent torsional disparity of horizontal and vertical lines during three tasks: vergence on a near target, vergence through prisms that remained fixed, and through prisms that rotated with eye elevation. Consistent with our previous search-coil measurements, the results here suggest that the angle between the Listing's planes of the two eyes is somewhat less than the vergence angle.

Neural constraints on eye motion in human eye-head saccades.

We examined two ways in which the neural control system for eye-head saccades constrains the motion of the eye in the head. The first constraint involves Listing's law, which holds ocular torsion at zero during head-fixed saccades. During eye-head saccades, does this law govern the eye's motion in space or in the head? Our subjects, instructed to saccade between space-fixed targets with the head held still in different positions, systematically violated Listing's law of the eye in space in a way that approximately, but not perfectly, preserved Listing's law of the eye in head. This finding implies that the brain does not compute desired eye position based on the desired gaze direction alone but also considers head position. The second constraint we studied was saturation, the process where desired-eye-position commands in the brain are "clipped" to keep them within an effective oculomotor range (EOMR), which is smaller than the mechanical range of eye motion. We studied the adaptability of the EOMR by asking subjects to make head-only saccades. As predicted by current eye-head models, subjects failed to hold their eyes still in their orbits. Unexpectedly, though, the range of eye-in-head motion in the horizontal-vertical plane was on average 31% smaller in area than during normal eye-head saccades, suggesting that the EOMR had been reduced by effort of will. Larger reductions were possible with altered visual input: when subjects donned pinhole glasses, the EOMR immediately shrank by 80%. But even with its reduced EOMR, the eye still moved into the "blind" region beyond the pinhole aperture during eye-head saccades. Then, as the head movement brought the saccade target toward the pinhole, the eyes reversed their motion, anticipating or roughly matching the target's motion even though it was still outside the pinhole and therefore invisible. This finding shows that the backward rotation of the eye is timed by internal computations, not by vision. When subjects wore slit glasses, their EOMRs shrank mostly in the direction perpendicular to the slit, showing that altered vision can change the shape as well as the size of the EOMR. A recent, three-dimensional model of eye-head coordination can explain all these findings if we add to it a mechanism for adjusting the EOMR.

Using a synoptophore to test Listing's law during vergence in normal subjects and strabismic patients.

The synoptophore was used to measure torsional interocular disparity. This, in turn, was used to compute how much the angle between the Listing's plane (LP) of the two eyes changes as a function of the vergence angle. The ratio of these two angles was defined as G. We measured G in normals and in patients suffering from intermittent horizontal strabismus. Consistent with previous search-coil experiments and with our previous visual test measures, the results using the synoptophore suggest that, for normals, G is less than 1. In the patient group the mean G was similar in magnitude but more variable. The variations in G did not appear to be related to the patient's measurement of ocular deviation. This result suggests that the vergence-related rotation of LP in these patients may be related to other factors besides the effort required to fuse the lines of sight.

Task-dependent changes in the shape and thickness of Listing's plane.

We examined the 2D surface formed by 3D eye positions of normal subjects to determine whether the shape and thickness changed in tasks that differed in saccadic directions: random, horizontal, vertical, radial, clockwise and counter-clockwise. Eye positions during the random task did not lie precisely on Listing's plane but on a surface with a small twist. This twist was present before, during, and after saccades. The degree of twist changed with the task; becoming less twisted for horizontal tasks and more twisted in the vertical tasks. The surface thickness changed with the task becoming thicker for multidirectional tasks. This greater thickness may occur because surfaces obtained in multidirectional tasks are the composite of surfaces with slightly different shapes.

Differences in perceived shape from shading correlate with activity in early visual areas.

The perception of shape from shading depends on the orientation of the shading gradient [1] [2] [3] [4]. Displays composed of elements with vertically oriented shading gradients of opposite polarity produce a strong and stable percept of 'concave' and 'convex' elements. If the shading gradients are rotated 90 degrees , the depth percept is reduced and appears much more ambiguous. Results from psychophysical [1] [2] [3] [4] [5] [6], neuropsychological [7] and computational studies [8] [9] suggest that the perception of shape from shading engages specific mechanisms in early cortical visual areas. In a three-dimensional functional magnetic resonance imaging (fMRI) study at 1.5 Tesla using a three-dimensional, interleaved-echoplanar imaging technique and a surface radio frequency (RF) coil placed under the visual cortex, we investigated the activity in these early visual areas associated with viewing shape from shading displays at two different orientations. We found significantly greater activation in area V1 and neighbouring low-level visual areas of cortex when subjects viewed displays that led to weak and unstable depth percepts than when they viewed displays that led to strong and stable depth percepts.

Interaction of smooth pursuit and the vestibuloocular reflex in three dimensions.

1. What is the neural mechanism of vestibuloocular reflex (VOR) cancellation when a subject fixates a target moving with the head? One theory is that the moving target evokes pursuit eye movements that add to and cancel the VOR. A recent finding with implications for this theory is that eye velocity vectors of both pursuit and the VOR vary with eye position, but in different ways, because pursuit follows Listing's law whereas the VOR obeys a "half-Listing" strategy. As a result, pursuit cannot exactly cancel the VOR in most eye positions, and so the pursuit superposition theory predicts an eye-position-dependent pattern of residual eye velocities during cancellation. To test these predictions, we measured eye velocity vectors in humans during VOR, pursuit, and cancellation in response to torsional, vertical, and horizontal stimuli with the eyes in different positions. 2. For example, if a subject is rolling clockwise (CW, frequency 0.3 Hz, maximum speed 37.5 deg/s) while looking 20 deg up, the VOR generates an eye velocity that is mainly counterclockwise (CCW), but also leftward. If we then turn on a small target light, located 20 deg up and moving with the subject, then pursuit superposition predicts that the CCW component of eye velocity will shrink and the horizontal component will reverse, from leftward to rightward. This pattern was seen in all subjects. 3. Velocities depended on eye position in the predicted way; e.g., when subjects looked 20 deg down, instead of 20 deg up, during CW roll, the reversal of horizontal eye velocity went the other way, from rightward to leftward. And when gaze was 20 deg right or left, analogous reversals occurred in the vertical eye velocity, again as predicted. 4. Analogous predictions for horizontal and vertical stimulation were also borne out by the data. For example, when subjects rotated rightward while looking 20 deg up, the VOR response was leftward and CCW. When the target light switched on, the torsional component of the response reversed, becoming CW. And analogous predictions for other eye positions and for vertical stimulation also held. 5. For all axes of stimulation and all eye positions, eye velocity during cancellation was roughly parallel with the gaze line. This alignment is predicted by pursuit superposition and has the effect of reducing retinal image slip over the fovea. 6. The fact that the complex dependence of eye velocity on the stimulation axis and eye position predicted by pursuit superposition was seen in all subjects and conditions suggests strongly that the VOR indeed is canceled additively by pursuit. However, eye velocities during cancellation were consistently smaller than predicted. This shrinkage indicates that a second mechanism, besides pursuit superposition, attenuates eye velocities during cancellation. The results can be explained if VOR gain is reduced by approximately 30%, and if, in addition, pursuit is driven by retinal slip rather than reconstructed target velocity in space.

Rotation of Listing's plane by horizontal, vertical and oblique prism-induced vergence.

We examined the changes in Listing's plane resulting from prismatically induced vergence. The three-dimensional angular positions of the two eyes were compared in normal subjects wearing search coils and gazing at targets 1.9 m away with and without prisms. For horizontal base-out prisms each degree of convergence in one eye yielded 0.72 deg of temporal rotation of Listing's plane in that eye. The results from vertical prisms were not what was expected from the horizontal results. A base-up prism on the right eye induced a downward and temporal rotation of Listing's plane. A base-down prism on the right eye induced an upward and nasal rotation of Listing's plane. The effects of oblique prisms were those expected from combining the effects of horizontal and vertical prisms. Thus in addition to producing a horizontal or vertical misalignment of the gaze line, prisms induce an unexpected position-dependent torsional disparity.

Eye-head coordination during large gaze shifts.

1. Three-dimensional (3D) eye and head rotations were measured with the use of the magnetic search coil technique in six healthy human subjects as they made large gaze shifts. The aims of this study were 1) to see whether the kinematic rules that constrain eye and head orientations to two degrees of freedom between saccades also hold during movements; 2) to chart the curvature and looping in eye and head trajectories; and 3) to assess whether the timing and paths of eye and head movements are more compatible with a single gaze error command driving both movements, or with two different feedback loops. 2. Static orientations of the eye and head relative to space are known to resemble the distribution that would be generated by a Fick gimbal (a horizontal axis moving on a fixed vertical axis). We show that gaze point trajectories during eye-head gaze shifts fit the Fick gimbal pattern, with horizontal movements following straight "line of latitude" paths and vertical movements curving like lines of longitude. However, horizontal (and to a lesser extent vertical) movements showed direction-dependent looping, with rightward and leftward (and up and down) saccades tracing slightly different paths. Plots of facing direction (the analogue of gaze direction for the head) also showed the latitude/longitude pattern, without looping. In radial saccades, the gaze point initially moved more vertically than the target direction and then curved; head trajectories were straight. 3. The eye and head components of randomly sequenced gaze shifts were not time locked to one another. The head could start moving at any time from slightly before the eye until 200 ms after, and the standard deviation of this interval could be as large as 80 ms. The head continued moving for a long (up to 400 ms) and highly variable time after the gaze error had fallen to zero. For repeated saccades between the same targets, peak eye and head velocities were directly, but very weakly, correlated; fast eye movements could accompany slow head movements and vice versa. Peak head acceleration and deceleration were also very weakly correlated with eye velocity. Further, the head rotated about an essentially fixed axis, with a smooth bell-shaped velocity profile, whereas the axis of eye rotation relative to the head varied throughout the movement and the velocity profiles were more ragged. 4. Plots of 3D eye orientation revealed strong and consistent looping in eye trajectories relative to space.(ABSTRACT TRUNCATED AT 400 WORDS)

Three-dimensional eye, head, and chest orientations after large gaze shifts and the underlying neural strategies.

1. The fixation orientations adopted by the eye, head, and chest were examined when all three were allowed to participate in gaze shifts to visual targets. The objective was to discover whether there are invariant, neurally determined laws governing these orientations that might provide clues to the processes of perception and motor control. This is an extension of the classical studies of eye-only saccades that determined that there is only one eye orientation for each gaze direction (Donders' law) and that the rotations necessary to take the eye from a reference orientation to all other orientations adopted are about axes that lie in a plane (Listing's law). 2. The three-dimensional orientations of the static eyes, head, and chest were measured after each gaze shift to a visual target, the targets having been fixed at positions ranging from 0 to 135 degrees to the left and right of center and 45 degrees up and down. These measurements were taken of seven human subjects by means of the search coil technique with coils attached to the sternum, head, and right eye. Orientations were plotted as quaternion vectors so that those orientations obeying Donders' law formed a surface and those obeying Listing's law formed a plane. 3. The orientations adopted by the eye, head, and chest were found to be a small subset of those possible under the biomechanical and task-imposed constraints. Thus there is a neurally implemented restriction, specifically of the rotation of the eye relative to space (i.e., the orientation variable es) and to the head (eh); also of the rotation of the head relative to space (hs) and to the chest (hc), and the rotation of the chest relative to space (cs). Plotted as quaternion vectors, the data for each orientation variable formed a characteristic surfacelike shape. In the case of es, hs, and hc these were twisted surfaces, whereas for eh the surface was planar and for cs it was nearly linear. Thus to a first approximation each of the orientation variables conformed to Donders' law. 4. The eye adopted a pointing (gaze) direction that has the ratio of vertical to horizontal components generally greater than one when fixating each of the corner targets. The chest, by contrast, moved almost entirely in the horizontal direction, whereas the head performed an intermediate role. 5. The es-, hs-, and hc-fitted surfaces and cs-fitted lines were titled remarkably little from the vertical axis (i.e., the gravity direction) despite larger tilts being possible.(ABSTRACT TRUNCATED AT 400 WORDS)

The influence of gravity on Donders' law for head movements.

Three-dimensional (3-D) head rotations were examined in seven human subjects when their bodies were inclined +/- 45 degrees in pitch and roll. The selection of 3-D orientations of the head while subjects looked at visual targets was similar to that seen previously for the eye: there was a small static counter pitch and counter roll of approx. 10%. Thus rotations of the head relative to the trunk are largely independent of the trunk's position relative to gravity and the head's torsional orientation is primarily dependent on its horizontal and vertical position relative to the trunk.

Modularity and parallel processing in the oculomotor integrator.

The neural signals that hold eye position originate in a brainstem structure called the neural integrator, so-called because it is thought to compute these position signals using a process equivalent to mathematical integration. Most previous experiments have assumed that the neural integrator reacts to damage like a single mathematical integrator: the eye is expected to drift towards a unique resting point at a simple exponential rate dependent on current eye position. Physiologically, this would require a neural network with uniformly distributed internal connections. However, Cannon et al. (1983) proposed a more robust modular internal configuration, with dense local connections and sparse remote connections, computationally equivalent to a parallel array of independent sub-integrators. Damage to some sub-integrators would not affect function in the others, so that part of the position signal would remain intact, and a more complex pattern of drift would result. We evaluated this parallel integrator hypothesis by recording three-dimensional eye positions in the light and dark from five alert monkeys with partial neural integrator failure. Our previous study showed that injection of the inhibitory gamma aminobutyric acid agonist muscimol into the mesencephalic interstitial nucleus of Cajal (INC) causes almost complete failure of the integrators for vertical and torsional eye position after approximately 30 min. This study examines the more modest initial effects. Several aspects of the initial vertical drift could not be accounted for by the single integrator scheme. First, the eye did not initially drift towards a single resting position; rapid but brief drift was observed towards multiple resting positions. With time after the muscimol injection, this range of stable eye positions progressively narrowed until it eventually approximated a single point. Second, the drift had multiple time constants. Third, multiple regression analysis revealed a significant correlation between drift rate and magnitude of the previous saccade, in addition to a correlation between drift rate and position. This saccade dependence enabled animals to stabilize gaze by making a series of saccades to the same target, each with less post-saccadic drift than its predecessor. These observations were predicted and explained by a model in which each of several parallel integrators generated a fraction of the eye-position command.(ABSTRACT TRUNCATED AT 400 WORDS)