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1Department of Neurobiology, Washington University School of Medicine, St. Louis, Missouri; and 2Department of Neurology, Zurich University Hospital, Zurich, Switzerland
Submitted 2 October 2007; accepted in final form 4 February 2008
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Goldberg and Bruce 1990; Sommer and Wurtz 2002, 2006), there is much we do know about the extraretinal signals necessary for spatial updating to occur.
For example, both humans and non-human primates can update for rotations associated with actively generated changes in eye, head, and body position. This has been shown with variants of the double-step saccade paradigm in which a peripheral target is briefly flashed and must be later foveated after intervening movements of the eyes (Hallett and Lightstone 1976; Herter and Guitton 1998; McKenzie and Lisberger 1986; Ohtsuka 1994; Schlag et al. 1990; Zivotofsky et al. 1996) and head/body (Medendorp et al. 2002). These findings, based on self-generated movements, have led many to speculate that efference copy signals of the outgoing motor command are critical for spatial updating.
The necessity of such efference copies has been investigated by studies that examined the efficacy of spatial updating during passive rotations of the eyes and head/body. For the former, changes in eye position via stimulation of the superior colliculus and burst neurons in the paramedian pontine reticular formation have shown that information from these brain stem areas can be utilized to maintain spatial constancy (Sparks and Mays 1983). For the latter, passive whole-body rotations have shown that humans can take intervening yaw (Klier et al. 2006) and roll (Klier et al. 2005, 2006) rotations into account, although there were substantial individual differences and updating for roll was better, on average, than updating for yaw.
In the real world, our bodies not only rotate but translate in space either actively (i.e., when we walk or run) or passively (i.e., when we sit in a car or ride on a moving sidewalk). But updating for translation is more complicated than updating for rotations for two reasons: first, rotations only require the amplitude and direction of the intervening movement to be taken into account, whereas translations additionally require the consequences of motion parallax to be accounted for. Because objects that are located closer to our eyes move larger distances across our retinas than farther objects, greater changes in version are required for near targets and smaller changes in version are required for far targets (given the same translational amplitude). Second, while rotations do not change the distance of an object from the observer, translations do (especially those along the forward/backward axis). Thus the brain must also generate changes in vergence angles after intervening translational movements.
Previous studies have evaluated the ability of humans to estimate the amplitude of passive, linear self-motion, also known as path integration (Mittelstaedt and Mittelstaedt 1980). Several studies have shown that humans can accurately judge the distance traveled toward a target (Berthoz et al. 1995; Glasauer and Brandt 2007; Israel et al. 1993, 1997; Siegler et al. 2000). However, while path integration could be a signal that is used for accurate spatial updating, these studies did not dissociate the visual location of the target from the motor command necessary to foveate it accurately. Notably, accurate path integration does not necessarily imply accurate updating ability. For the latter, there is an additional computational step (i.e., updating the retinal error for a motor command).
A single human study has demonstrated that subjects can take actively generated translations into account for lateral (i.e., side-to-side) visuospatial updating (Medendorp et al. 2003). Recently a number of animal studies have shown that monkeys can also update after lateral (Li et al. 2005) and fore-aft (Li and Angelaki 2005) translations. In addition, labyrinthectomized animals lose their ability to update in both the lateral and forward/backward directions, but interestingly, deficits in the forward/backward dimension are more pronounced and show less recovery (Wei et al. 2006). Again, these results point to a significant role of the vestibular system, especially the otolith organs, in translational spatial updating.
To determine whether spatial updating is not simply a product of primate overtraining or learning, we designed the current experiment to quantify human updating capabilities for passive translation. For the first time, we analyze updating along all three axes—forward/backward, rightward/leftward, and upward/downward. We found that subjects perform well after forward/backward, lateral and upward translations but consistently undershoot the target after downward translations. Preliminary results of this work have appeared in abstract form (Klier et al. 2007b).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Six subjects (4 female and 2 male) ranging in age from 28 to 48 yr old were recruited to participate in the experiment. All but one (EK) were naïve to the purpose of the experiment, all had normal or corrected-to-normal vision, and none had any known neuromuscular or neurological deficits. All subjects gave informed consent to the experimental protocol, and the eye movement recording procedures were approved by the Ethics Committee of the Canton of Zurich, Switzerland.
Measuring three-dimensional eye position
Three-dimensional eye positions of both eyes were measured using the magnetic search coil technique and three-dimensional Skalar search coils (Skalar Instruments, Delft, The Netherlands). The magnetic field system consisted of three mutually orthogonal magnetic fields, generated by a cubic frame with side lengths of 0.5 m, operating at frequencies of 80, 96, and 120 Hz. Three-dimensional eye position was calibrated using an algorithm that simultaneously determined the orientation of the coil on the eye and offset voltages based on nine target fixations in close-to-primary and secondary gaze positions (Klier et al. 2005). These targets were projected via a projector (LC-XG210, EIKI Deutschland GmbH, Germany) onto a tangent screen (150 x 190 cm) located at a distance of 2 m in front of the subjects.
Experimental equipment
Subjects sat on a 6 df moveable platform (E-Cue 624x1800, Simulator Systems B.V.) capable of linear translations in three-dimensions: lateral = right/left, vertical = up/down, and forward/backward. A wooden chair complete with a foam head-rest and aviation harness was located in the center of the platform. During each experiment, each subject's head was fixed to the chair by a personalized, thermoplastic mask that was molded to the face and bolted to the chair around the subject's head. In addition, the subject's body was fixed to the chair via seatbelts around the pelvis and torso, and with evacuation pillows that filled the spaces between the subject and the sides of the chair.
The space-fixed, visual targets consisted of five red light-emitting diodes (LEDs) located at 23, 33, 43, 63, and 150 cm away from the subjects’ cyclopean eye (Fig. 1A). The relative distances of these targets were chosen such that they spanned the range of vergence angles that human subjects are capable of achieving (Fig. 1B). These space-fixed targets were mounted between a homemade, U-shaped, Plexiglas apparatus with four thin wires bridging the two long arms (resembling railroad tracks). Four of the space-fixed targets were located in the center of the four spanning wires, while the furthest target (150 cm) was placed on the end of another Plexiglas rod that extended, away from the subject, from the middle of the short arm of the first apparatus. As these targets were required to be space-fixed, the entire Plexiglas apparatus was suspended from the ceiling with a wooden pole, and the height of the five targets was adjusted for each subject by placing them at eye level. One LED, which functioned as the head-fixed fixation target, was mounted via a vertical, metal rod that was clamped to the motion platform at a distance of 53 cm from the subjects’ eyes (Fig. 1A –boxed "F"). Thus this latter LED moved with the platform and with the subjects. To avoid the fixation LED from running into the space-fixed targets at 63 and 43 cm when the chair moved 10 cm forward and backward, respectively, it was placed 
2 mm below eye level. This offset did not affect updating measurements during lateral translations where performance is measured by changes in horizontal version or forward/backward translations where performance is measured by changes in vergence angle. Moreover, this small offset was also negligible during vertical translations where subjects had to update for amplitudes of 100 mm.
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Experimental procedure
CALIBRATION. Each experiment began and ended with a calibration task. Using the aforementioned projector and screen, nine targets were back projected, one at a time in a counterclockwise pattern, and the subjects had to fixate each of these targets for three seconds. The first target was located directly in front of the subjects, while the other eight were in the cardinal directions at amplitudes of 10 and 14°.
FIXATION TRIALS. To determine the appropriate version and vergence angles of the two eyes for each of the five space-fixed targets in depth, we illuminated and had subjects fixate each target for 3 s. This was done with the subjects at center (where the 5 space-fixed targets where lined up directly in front of the cyclopean eye—Fig. 1A), and with the subjects statically positioned at 10 cm to the right, left, down, and up of this center position.
STATIONARY TRIALS. How accurately subjects acquired these space-fixed targets during a memory saccade was determined during stationary trials where subjects either remained at center (Fig. 2A) or were moved 10 cm rightward, leftward, downward, or upward (Fig. 2B, rightward movement). Once this position was attained, the ambient light was then turned on, followed by the head-fixed LED 0.5 s later. The subject had to fixate the head-fixed LED, and, 1.5 s after it was turned on, one of the space-fixed targets was briefly flashed for 100 ms. The subjects had to maintain fixation on the head-fixed LED but remember the location of the flashed space-fixed target. After the space-fixed target and the ambient light were extinguished, a delay period of 1.5 s followed, after which time the head-fixed LED was extinguished. This cued the subjects to make a memory saccade to the remembered location of the flashed space-fixed target and hold that final position for 2 s until they heard an auditory tone which instructed them to relax and prepare for the next trial. The final eye position was held for 2 s so that the entire vergence movement could be completed. Note that the space-fixed targets were not turned back on at the end of each trial, and so subjects were not provided any visual feedback and thus they could not learn the task.
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Importantly, in the motion trials, subjects were always moved from the center, initial position (Figs. 1A and 2A) to any one of six final positions (e.g., Fig. 2, B and C). Corresponding stationary trials were specifically selected such that there was one stationary trial for the initial position and one stationary trial for the final position for each motion trial. Thus the main goal was to determine if the subjects’ updated movements in the motion trials corresponded better with the memory movements in the initial stationary trials (i.e., no updating) or with the memory movements in the final stationary trials (i.e., perfect updating; Fig. 2C). Note that it was not necessary to collect final stationary trials for the forward/backward motion trials. This is because the three nearest space-fixed targets (at 23, 33, and 43 cm) were each spaced 10 cm apart from one another and thus could serve as final stationary trials for one another. For example, when the 33-cm space-fixed target was flashed and the subject was moved forward, the stationary trial of the 23-cm space-fixed target functioned as the final stationary trial. Similarly, when the 33-cm space-fixed target was flashed and the subject was moved backward, the stationary trial of the 43-cm space-fixed target functioned as the final stationary trial.
There were a total of four forward/backward motion trials—two with forward motion (33-cm target flash with 10-cm forward motion and 43-cm target flash with 10-cm forward motion) and two with backward motion (23-cm target flash with 10-cm backward motion and 33-cm flash with 10-cm backward motion). Only three of the five space-fixed targets were used for forward/backward motion (23, 33, and 43 cm) because the necessary changes in vergence for the two farthest targets (at 63 and 150 cm) would have been extremely small, ranging from 0.14° for a 10-cm backward movement when the target at 150 cm is flashed to 1.03° for a 10-cm forward movement when the target at 63 cm is flashed (these vergence angles were computed using an intraocular distance of 6 cm). Thus updating ability would have been too difficult to accurately measure for these very small vergence changes. For the same reason, the target at 43 cm was only associated with forward motion (requiring 2.41° of vergence change) but not backward motion that would only require 1.50° of vergence change. Finally, the closest target at 23 cm was only associated with backward motion because forward motion would require a final vergence angle of 25.99°, which is too large for humans to make.
Data analysis
Raw data from each subject's left and right eyes, sampled at 833 Hz, was first converted into rotation vectors, which indicate the horizontal, vertical, and torsional positions of the eye. These positions were subsequently transformed into eye velocity by taking the derivative of eye position (dE/dt, where E is 3-dimensional eye position). Finally, angular eye velocity (
) was computed from the previous two values by the equation = 2 (dE/dt + E x dE/dt)/(1 + |E|2) (where x designs the cross-vector product). Version eye position was computed as the average of left and right eye position: (R + L)/2, whereas the vergence angle was computed as the difference between right and left eye position: R –L. All saccade trajectories to the remembered target locations were automatically selected using the following criteria: the start of a saccade was selected when the square root of the sum of squares of the horizontal, vertical and torsional angular velocities exceeded 10°/s for both eyes. The end of a saccade occurred when the same value decreased below 10°/s for both eyes. The end of the memory period was taken at a point 250 ms before the auditory tone. Two postsaccadic periods, saccade end and memory end, were measured because it has been shown that vergence responses often take longer than vergence responses to reach completion (Westheimer 1954; Yarbus 1967). These data, along with the actual locations of the targets in space allowed us to plot saccade trajectories and endpoints, and conduct statistical analyses on our data.
Updating ratios
To quantify how well subjects were able to take their intervening movements into account when computing the updated eye movement to the remembered target location, we computed updating ratios for both version and vergence. Perfect updating would be indicated by motion trial version and vergence angles that are equal to final stationary trial version and vergence angles (Fig. 2C, rightmost panel, circled "F"). In contrast, no updating would be indicated by motion trial version and vergence angles that are equal to initial stationary trial version and vergence angles (Fig. 2C, rightmost panel, circled "I"). Thus the following updating ratio was computed separately for version and vergence values (Vmotion –MVstat.initial /(MVstat.final –MVstat.initial), where Vmotion is version or vergence angle for an individual motion trial, MVstat.initial is the mean version or vergence angle from the initial stationary trials, and MVstat.final is the mean version or vergence angle for the final stationary trials. A value of 1 indicates perfect updating (i.e., the subjects’ eyes were directed to the space-fixed location of the LED), whereas a value of 0 indicates no updating (i.e., the subjects’ eyes were directed to the head-fixed location of the LED). Note that for horizontal and vertical translations, the version updating ratio is important for determining updating ability as this is the main variable that must change if updating occurs. In contrast, initial and final vergence angles are nearly identical and thus the corresponding updating ratio is useless. In contrast, for forward/backward updating, the vergence updating ratio is key because the main change in eye position after forward/backward motion is a vergence movement. Here, the initial and final version angles are too similar to derive any meaningful data (this will be demonstrated in Fig. 5). Updating ratios were computed for each subject separately for the two experimental days and then these two values were averaged for the final updating ratio. This was done to control for varying levels of arousal, motivation and fatigue that sometimes led to differences in version and (especially) vergence for each individual target across the two different experimental days.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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We first analyzed the subjects’ performances during the stationary trials to obtain a measure of their performance in memory trials when no updating was required. The stationary trials were conducted in both the initial (Fig. 2A) and final (Fig. 2B) positions of the motion trials (Fig. 2C). An example of a final stationary trial for a rightward 10-cm translation is shown in Fig. 3 for both the nearest target (23 cm) that was in front of the fixation point (53 cm) and the farthest target (150 cm) that was behind the fixation point (53 cm). For the near target (left), the required memory saccade was composed of a large, conjugate, horizontal movement to the left (top traces) and a large increase in vergence (bottom trace). In contrast, for the far target (right), the memory saccade consisted of a much smaller leftward version movement (top traces) and a decrease in vergence (bottom trace).
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The opposite pattern is true for forward/backward movements. Figure 5B illustrates a 10-cm forward motion trial in which a target at 33 cm was flashed. Here differences in version movements between the initial and final stationary trials are negligible (notice close proximity of red and blue traces) because the targets were aligned with the subject's cyclopean eye and thus also with the motion axis. However, because the subject was moved forward and was therefore now closer to the previously flashed target, they had to make an eye movement with increased vergence to the remembered location of the space-fixed target. This can be seen by the higher vergence angle of the final stationary trial (red trace) as compared with the initial stationary trial (blue trace). The actual vergence movement of the subject (black trace) was closer to the final stationary trial (red trace) after the eye movement was made.
To quantify these observations across all subjects, all targets and all movement directions, we plotted the subjects’ version (Fig. 6, top) and vergence (bottom) performances in the motion memory trials as a function of their version and vergence performances in the final stationary memory trials for lateral (left), vertical (middle), and forward/backward (right) translations. Data from each subject are shown by a different symbol (see Fig. 1B, inset), and each target is indicated by a different color (see inset). The unity slope is indicated by the dashed black lines and the average slope across all subjects is shown by the solid black lines. As already mentioned, the version comparison is relevant for lateral and vertical movements and the vergence comparison is relevant for forward/backward movements. The average version comparison slope [±95% confidence intervals] was 0.82 [0.69, 0.94] for lateral motion and 0.81 [0.63, 0.99] for vertical motion. Because these slopes were slightly <1, there was only partial updating for lateral and vertical translations. For forward/backward motion, vergence slopes [±95% confidence intervals] averaged 1.17 [0.77, 1.50] and thus were not different from a slope of 1. Data for each individual subject's slopes in all conditions are given in Table 2.
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The average vergence updating ratio for the forward/backward motion trials was 1.12 ± 0.45. However, we did not further compare potential direction and target differences because the observed power was relatively low (0.42 compared with 0.70 for lateral and 1.00 for vertical translations). The lower power was due to a number of factors including 1) the smaller number of space-fixed targets used (3 instead of 5) and the fact that only one direction of motion (instead of 2) was used for two of the three space-fixed targets (see METHODS section for details) and 2) the larger intrasubject variability for vergence compared with version movements (Henriques et al. 2003; Medendorp et al. 2003).
To get a better idea of the intrasubject variability present in the current experiment, Fig. 7B plots the average SD for each subject, in all conditions. The variability of the SDs was clearly lower than that of the actual updating ratio means (Fig. 7A). However, notice that here too there was a trend in which more variability was observed for farther targets. This trend is likely due to motion parallax where smaller version/vergence changes are required for far targets than for near targets.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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, 2006). Intrasubject variability was low for near target updating but increased as a function of target distance (Fig. 7B). Finally, because version and vergence accuracy in the stationary memory trials were identical to those during fixation (Fig. 4), the observed updating errors likely arise from the processes associated with spatial updating and not from mislocalization of the original location of the target (Medendorp et al. 2003) or from decay of memory storage (White et al. 1994).
These findings show that in addition to efference copy signals of the outgoing motor command (that are generated during active displacements), extra-retinal sensory information (e.g., vestibular and/or proprioceptive cues) are also useful for translational updating in humans as has been shown previously for rotational updating (Klier et al. 2005, 2006, 2007b). Among these sensory signals, strong evidence points to the vestibular system as a key player in spatial updating. Wei et al. (2006) attempted to eliminate vestibular signals by labyrinthectomizing animals that were trained to perform translational updating paradigms. They found that both lateral and forward/backward translational updating was compromised after the lesions but that the effects were much more severe and permanent for forward/backward motion. Lateral updating ratios fell from 0.71 to 0.49 and recovered to near normal levels after 10 wk, implying that proprioception/somatosensory cues also contribute to updating during lateral and yaw updating. In contrast, forward/backward updating ratios fell from 0.96 to nearly zero and did not recover much even after 16 wk. Thus while vestibular signals appear to play a vital role in spatial updating, they may be more crucial in certain directions of motion than in others, or alternatively, this may reflect a difference between the version and vergence systems.
Previous studies have demonstrated that humans can correctly gauge the amount of distance traveled after passive whole-body translations (Berthoz et al. 1995; Glasauer and Brandt 2007; Israel et al. 1993, 1997; Siegler et al. 2000). Functionally, this could arise via temporal integration of velocity and/or acceleration information derived from the vestibular system and stored in spatial memory (Berthoz et al. 1995; Israel and Berthoz 1989; Israel et al. 1997). Such path integration signals may be used to update visual maps of space after translations. Alternatively, however, the signals used for updating may arise from efference copies of the cancellation signal used to suppress translational vestibuloocular reflex (TVOR). The latter is actually more likely because updating is only necessary when the TVOR is suppressed during self-motion (otherwise, if the TVOR is intact, the final motor error is equivalent to the initial retinal error). Finally, note that this efference copy signal is quite different from an efference copy of the motor command associated with voluntary movements. For example, the TVOR cancellation efference copy signal is only available during the passive motion and can therefore not be used for predictive remapping (Duhamel et al. 1992), while the efference copy of the outgoing motor command is available before the movement is executed.
Monkey versus man
As mentioned, Wei et al. (2006) reported average lateral translational updating ratios of 0.71 ± 0.21 (mean ± SD) and average forward/backward ratios of 0.96 ± 1.10 across their two animals. Thus monkeys were better at updating for forward/backward motion than lateral motion. We can compare these monkey parameters to the human parameters found in the current study. Our average updating ratio across all subjects, targets and directions of motion was 0.84 ± 0.28 for lateral motion and 1.12 ± 0.45 for forward/backward motion. Thus humans and non-human primates had similar updating abilities, with forward/backward updating having higher ratios, but more variability, than lateral updating.
These similarities are interesting given the differences in the updating paradigms. First, in the monkey experiments, at the end of each motion and stationary trial, the space-fixed target was turned on again, allowing the monkey to make a corrective saccade and permitting learning to occur. Humans have been shown to improve performance on spatial updating tasks when visual feedback is provided (Israel et al. 1999); however, none was permitted in the current study. Yet this lack of learning did not seem to affect our subjects’ performance as compared with the animals that did receive visual feedback. Second, the monkeys were trained to perform these tasks thousands of times over several months, sometimes a year. And once ready for testing, >1,000 trials were collected for analysis from each animal (Li et al. 2005). Humans were only given a handful of trial runs before the experiment began, and in each experiment, only six trials of every target/motion combination could be collected. Thus here, as in all human experiments, the subjects had much less experience with the required tasks and much less data were collected. This latter point should affect the final variability of the data from a purely statistical standpoint as less data leads to greater variability in measurements. This does not seem to have been the case here. Finally, the monkeys had a direct, physiologically relevant reward (i.e., juice) for completing the experiment, whereas the human volunteers did not.
Near versus far targets
The observed trend, that for lateral and vertical updating the average updating ratio increased with increased target depth, might have partially depended on the fact that subjects had their heads fixed. The large version movements required to accurately update near targets is typically accomplished, in natural circumstances, by combined movements of the eyes and head. In fact, the head typically increases its relative contribution with increased gaze shift amplitude (Freedman and Sparks 1997; Klier et al. 2001; Martinez-Trujillo et al. 2003). Thus the relatively lower updating ratios seen with the nearer targets may be improved if this study were to be repeated with the head free to move. Alternatively, if the suppressed TVOR command (which occurs when the head-fixed target is fixated during translation) is used as the updating signal, then differences between near and far TVOR gains may explain the differences between updating ratios for targets in depth. This is because while TVOR gain is near unity for far targets, it is consistently undercompensatory for near targets (Schwarz and Miles 1991). This lower TVOR gain for near targets could thus result in the lower updating ratios we observed.
Source of extra-retinal signals
If vestibular signals are used to update the locations of targets in space (as speculated in the preceding text), then one issue that remains to be resolved is the location at which these vestibular signals are used. Accumulating evidence from saccadic studies have implicated the posterior parietal cortex (Colby and Goldberg 1999; Duhamel et al. 1992) and extrastriate visual areas (Nakamura and Colby 2002) as well as the frontal cortex (Goldberg and Bruce 1990; Umeno and Goldberg 1997) as updating centers for intervening saccadic eye movements. These studies have found evidence for remapping, a phenomenon in which the representation of a visual target is moved or remapped at the time of an eye movement by an amount equivalent to the amplitude and direction of the intervening eye movement. For example, when a saccadic eye movement brings the receptive field of a cell on the location of a previously flashed target, and the target is no longer present, the cell responds as if the target was still present. Thus visual information is shifted from the coordinates of the initial eye position, to the coordinates of the final eye position, thereby maintaining spatial constancy. Several other studies support the notion that target locations are indeed stored in an eye-centered reference frame (Baker et al. 2003; Batista et al. 1999; Colby and Goldberg 1999; Henriques et al. 1998; Snyder 2000).
But does a similar remapping mechanism exist for changes in head/body position that are detected by vestibular stimulation (either rotational or translation motion)? Here the location of a cell's receptive field would need to be shifted by the amplitude and direction of the intervening head or whole-body movement. The parameters of these movements could be derived, in eye coordinates, either directly from the suppressed rotational or translational VOR or indirectly from the path integration of the vestibular signal. Some cortical evidence exists for such signals including visuomotor areas like the frontal eye fields (Fukushima et al. 2000). But whether these signals are actually used to remap visual receptive fields is still unknown.
If vestibular signals derived from the brain stem are used for vestibular spatial updating in the cortex, then one must also delineate the pathways by which these signals travel from the vestibular-related brain stem areas to the cortical areas that have been implicated in spatial updating. Two possible pathways, both involving the thalamus, are currently known to exist that may transfer vestibular signals to the visuomotor cortical areas. The first involves vestibular projections to the ventrolateral thalamus (Lang et al. 1979; Meng et al. 2007) which then projects onto areas 2v, 3a, and parieto-insular vestibular cortex (PIVC) (Akbarian et al. 1992). PIVC, in turn, has connections to the frontal eye fields (Guldin et al. 1992; Huerta et al. 1987). The second involves prepositus and vestibular nuclei projections to the intralaminar nuclei of the thalamus (Asanuma et al. 1983; Lang et al. 1979; Warren et al. 2003), which then project to both the frontal and parietal cortex (Huerta and Kaas 1990; Huerta et al. 1986; Kaufman and Rosenquist 1985; Shook et al. 1990, 1991). In fact, part of this latter pathway (from mediodorasl thalamus to the frontal eye fields) has already been implicated in transmitting eye-movement-related signals for spatial updating after saccades (Sommer and Wurtz 2004, 2006).
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: E. M. Klier, Dept. of Neurobiology, Box 8108, Washington University School of Medicine, 660 S. Euclid Ave., St. Louis, MO 63110 (E-mail: eliana{at}cabernet.wustl.edu)
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Asanuma C, Thach WT, Jones EG. Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res 286: 237–265, 1983.[Medline]
Baker JT, Harper TM, Snyder LH. Spatial memory following shifts of gaze. I. Saccades to memorized world-fixed and gaze-fixed targets. J Neurophysiol 89: 2564–2576, 2003.
Batista AP, Buneo CA, Snyder LH, Andersen RA. Reach plans in eye-centered coordinates. Science 285: 257–260, 1999.
Berthoz A, Israel I, Georges-Francois P, Grasso R, Tsuzuku T. Spatial memory of body linear displacement: what is being stored? Science 269: 95–98, 1995.
Colby CL, Goldberg ME. Space and attention in parietal cortex. Annu Rev Neurosci 22: 319–349, 1999.[CrossRef][Web of Science][Medline]
Duhamel JR, Colby CL, Goldberg ME. The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255: 90–92, 1992.
Freedman EG, Sparks DL. Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J Neurophysiol 77: 2328–2348, 1997.
Fukushima K, Sat T, Fukushima J, Shinmei Y, Kaneko CR. Activity of smooth pursuit-related neurons in the monkey periarcuate cortex during pursuit and passive whole-body rotation. J Neurophysiol 83: 563–587, 2000.
Glasauer S, Brandt T. Noncummutative updating of perceived self-orientation in three dimensions. J Neurophysiol 97: 2958–2964, 2007.
Goldberg ME, Bruce CJ. Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. J Neurophysiol 64: 489–508, 1990.
Guldin WO, Akbarian S, Grüsser OJ. Cortico-cortical connections and cytoarchitectonics of the primate vestibular cortex: a study in squirrel monkeys (Saimiri sciureus). J Comp Neurol 326: 375–401, 1992.[CrossRef][Web of Science][Medline]
Hallett PE, Lightstone AD. Saccadic eye movements to flashed targets. Vision Res 16: 107–114, 1976.[CrossRef][Web of Science][Medline]
Henriques DY, Klier EM, Smith MA, Lowy D, Crawford JD. Gaze-centered remapping of remembered visual space in an open-loop pointing task. J Neurosci 18: 1583–1594, 1998.
Henriques DYP, Medendorp WP, Gielen CCAM, Crawford JD. Geometric computations underlying eye-hand coordination: orientations of the two eyes and the head. Exp Brain Res 152: 70–78, 2003.[CrossRef][Web of Science][Medline]
Herter TM, Guitton D. Human head-free gaze saccades to targets flashed before gaze-pursuit are spatially accurate. J Neurophysiol 80: 2785–2789, 1998.
Huerta MF, Kaas JH. Supplementary eye field as defined by intracortical microstimulation: connections in macaques. J Comp Neurol 293: 299–330, 1990.[CrossRef][Web of Science]
Huerta MF, Krubitzer LA, Kaas JH. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. I. Subcortical connections. J Comp Neurol 253: 415–439, 1986.[CrossRef][Web of Science][Medline]
Huerta MF, Krubitzer LA, Kaas JH. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. J Comp Neurol 265: 332–361, 1987.[CrossRef][Web of Science][Medline]
Israel I, Berthoz A. Contribution of the otoliths to the calculation of linear displacement. J Neurophysiol 62: 247–263, 1989.
Israel I, Chapuis N, Glasauer S, Charade O, Berthoz A. Estimation of passive horizontal linear whole-body displacement in humans. J Neurophysiol 70: 1270–1273, 1993.
Israel I, Grasso R, Georges-Francois P, Tsuzuku T, Berthoz A. Spatial memory and path integration studied by self-driven passive linear displacement. I. Basic properties. J Neurophysiol 77: 3180–3192, 1997.
Israel I, Sievering D, Koenig E. Self-rotation estimate about the vertical axis. Acta Otolaryngol 115: 3–8, 1995.[Medline]
Israel I, Ventre-Dominey J, Denise P. Vestibular information contributes to update retinotopic maps. Neuroreport 10: 3479–3483, 1999.[Web of Science][Medline]
Kaufman EF, Rosenquist AC. Efferent projections of the thalamic intralaminar nuclei in the cat. Brain Res 335: 257–279, 1985.[CrossRef][Web of Science][Medline]
Klier EM, Angelaki DE, Hess BJM. Roles of gravitational cues and efference copy signals in the rotational updating of memory saccades. J Neurophysiol 94: 468–478, 2005.
Klier EM, Angelaki DE, Hess BJM. Human visuospatial updating after non-commutative rotations. J Neurophysiol 98: 537–544, 2007a.
Klier EM, Hess BJM, Angelaki DE. Differences in the accuracy of human visuospatial memory after yaw and roll rotations. J Neurophysiol 95: 2692–2697, 2006.
Klier EM, Hess BJM, Angelaki DE. Spatial updating performance after lateral, vertical and. fore/aft translations in humans. Soc Neurosci Abstr 508.10, 2007.
Klier EM, Wang H, Crawford JD. The superior colliculus encodes gaze commands in retinal coordinates. Nat Neurosci 4: 627–632, 2001.[CrossRef][Web of Science][Medline]
Lang W, Büttner-Ennever JA, Büttner U. Vestibular projections to the monkey thalamus: an autoradiographic study. Brain Res 177: 3–17, 1979.[CrossRef][Web of Science][Medline]
Li N, Angelaki DE. Updating visual space during motion in depth. Neuron 48: 149–158, 2005.[CrossRef][Web of Science][Medline]
Li N, Wei M, Angelaki DE. Primate memory saccade amplitude after intervened motion depends on target distance. J Neurophysiol 94: 722–733, 2005.
Martinez-Trujillo JC, Klier EM, Wang H, Crawford JD. Contribution of head movement to gaze command coding in monkey frontal cortex and superior colliculus. J Neurophysiol 90: 2770–2776, 2003.
McKenzie A, Lisberger SG. Properties of signals that determine the amplitude and direction of saccadic eye movements in monkeys. J Neurophysiol 56: 196–207, 1986.
Medendorp WP, Smith MA, Tweed DB, Crawford JD. Rotational remapping in human spatial memory during eye and head motion. J Neurosci 22: RC196, 2002.
Medendorp WP, Tweed DB, Crawford JD. Motion parallax is computed in the updating of human spatial memory. J Neurosci 23: 8135–8142, 2003.
Meng H, May PJ, Dickman JD, Angelaki DE. Vestibular signals in primate thalamus: properties and origins. J Neurosci 27: 13590–13602, 2007.
Middelstaedt ML, Mittelstaedt H. Homing path integration in a mammal. Naturwissenschaften 67: 566–567, 1980.[CrossRef][Web of Science]
Nakamura K, Colby CL. Updating of the visual representation in monkey striate and extrastriate cortex during saccades. Proc Natl Acad Sci USA 99: 4026–4031, 2002.
Ohtsuka K. Properties of memory-guided saccades toward targets flashed during smooth pursuit in human subjects. Invest Ophthalmol Vis Sci 35: 509–514, 1994.
Schlag J, Schlag-Rey M, Dassonville P. Saccades can be aimed at the spatial location of targets flashed during pursuit. J Neurophysiol 64: 575–581, 1990.
Schwarz U, Miles FA. Ocular responses to translation and their dependence on viewing distance. I. Motion of the observer. J Neurophysiol 66: 851–864, 1991.
Siegler I, Viaud-Delmon I, Israel I, Berthoz A. Self-motion perception during a sequence of whole-body rotation in darkness. Exp Brain Res 134: 66–73, 2000.[CrossRef][Web of Science][Medline]
Shook BL, Schlag-Rey M, Schlag J. Primate supplementary eye field. I. Comparative aspects of mesencephalic and pontine connections. J Comp Neurol 301: 618–642, 1990.[CrossRef][Web of Science][Medline]
Shook BL, Schlag-Rey M, Schlag J. Primate supplementary eye field. II. Comparative aspects of connections with the thalamus, corpus striatum, and related forebrain nuclei. J Comp Neurol 307: 562–583, 1991.[CrossRef][Web of Science][Medline]
Snyder LH. Coordinate transformations for eye and arm movements in the brain. Curr Opin Neurobiol 10: 747–754, 2000.[CrossRef][Web of Science][Medline]
Sommer MA, Wurtz RH. A pathway in primate brain for internal monitoring of movements. Science 296: 1480–1482, 2002.
Sommer MA, Wurtz RH. What the brain tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J Neurophysiol 91: 1403–1423, 2004.
Sommer MA, Wurtz RH. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 222: 374–377, 2006.
Sparks DL, Mays LE. Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. J Neurophysiol 49: 45–63, 1983.
Umeno MM, Goldberg ME. Spatial processing in the monkey frontal eye field. I. Predictive visual responses. J Neurophysiol 78: 1373–1383, 1997.
Warren S, Dickman JD, Angelaki DE, May PJ. Convergence of vestibular and somatosensory inputs with gaze signals in macaque thalamus. Soc Neurosci Abstr 29: 391.7, 2003.
Wei M, Li N, Newlands D, Dickman JD, Angelaki DE. Deficits and recovery in visuospatial memory during head motion after bilateral labyrinthine lesion. J Neurophysiol 96: 1676–1682, 2006.
Westheimer G. Mechanisms of saccadic eye movements. AMA Arch Ophthalmol 52: 710–724, 1954.[Medline]
White JM, Sparks DL, Stanford TR. Saccades to remembered target locations: an analysis of systematic and variable errors. Vision Res 34: 79–92, 1994.[CrossRef][Web of Science][Medline]
Yarbus AL. Eye Movements and Vision. New York: Plenum, 1967.
Zivotofsky AZ, Rottach KG, Averbuch-Heller L, Kori AA, Thomas CW, Dell'Osso LF, Leigh RJ. Saccades to remembered targets: the effects of smooth pursuit and illusory stimulus motion. J Neurophysiol 76: 3671–3632, 1996.
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