| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Laboratoire de Physiologie de la Perception et de l'Action, Centre National de la Recherche Scientifique, Collège de France, 75005 Paris, France
 |
ABSTRACT |
|---|
 Abstract
 Introduction
Methods
Results
Discussion
References
|
|---|
Israël, I., R. Grasso, P. Georges-François, T. Tsuzuku, and A. Berthoz. Spatial memory and path integration studied by self-driven passive linear displacement. I. Basic properties. J. Neurophysiol. 77: 3180-3192, 1997. According to path integration, the brain is able to compute the distance of a traveled path. In this research we applied our previously reported method for studying memory of linear distance, a crucial mechanism in path integration; our method is based on the overt reconstruction of a passive transport. Passive transport is a special case of navigation in which no active control is performed. Blindfolded subjects were first asked to travel 2 m forward, in darkness, by driving with a joystick the robot on which they were seated. The results show that all subjects but two undershot this distance, i.e., overestimated their own displacement. Then, subjects were submitted to a passive linear forward displacement along 2, 4, 6, 8, or 10 m, and had to reproduce the same distance, still blindfolded. The results show that the distance of the stimulus was accurately reproduced, as well as stimulus duration, peak velocity, and velocity profile. In this first condition, the imposed velocity profile was triangular and therefore stimulus distance and duration were correlated. In a second condition, it was shown that distance was correctly reproduced also when the information about stimulus duration was kept constant. Here, different velocity profiles were used as stimuli, and most subjects also reproduced the velocity profile. Statistical analyses indicated that distance was not reproduced as a consequence of duration, peak velocity, or velocity profile reproduction, but was uniquely correlated to stimulus distance. The previous hypothesis of a double integration of the otolith signal to provide a distance estimate can explain our results. There was a large discrepancy between the accuracy with which the subjects matched the velocity profiles and that of distance reproduction. It follows that, whereas the dynamics of passive motion are stored and available to further use, distance is independently estimated. It is concluded that vestibular and somatosensory signals excited by passive transport can be used to build a dynamic as well as a static representation of the traveled path. We found a close quantitative similarity between the present findings on distance reproduction and those obtained from active locomotion experiments in which the same paradigm was used. This resemblance suggests that the two types of navigation tasks draw on common physiological processes and extends the relevance of our results to naturally occurring path integration.
Idiothetic signals (Mittelstaedt and Mittelstaedt 1973 Experimental setup
A mobile robot, the Robuter (Robosoft SA, Bayonne, France), with a race car seat fixed on it was used for this experiment (Fig. 1A). In this device, two motor wheels driven by two 300-W DC permanent magnet independent motors ensure propulsion of a 120-kg maximal mass at a maximal linear velocity of 1.2 m/s, with a maximal acceleration of 1 m/s2. Steering is obtained by controlling the relative speed of the two driving wheels. The robot can be controlled by a remote microcomputer (PC) through wireless modems, or by a joystick connected to the robot itself. The joystick controls the robot's linear velocity in steps of 0.05 m/s (robot velocity directly proportional to joystick angle) with a delay of 0.2 s. Such a delay originates from the hardware and software implementation of the joystick mode control of robot motion and is not due to the mechanical inertia of the robot mass. Positioning accuracy and linearity of trajectory is ensured by proportional integral derivative control loops employing optical encoding of position (resolution of 1 mm and 0.01 s) and a trajectory generation and control system operating at 250 Hz. Odometry (position on the X-axis and timing) was recorded by the robot during motion at a 50-Hz sampling rate (Fig. 1B).
Experimental procedure
Fifteen healthy volunteers, with ages ranging from 20 to 50 yr and with no history of vestibular disorder, gave their informed consent to take part in the experiment, which was approved by the local ethical committee.
CALIBRATION.
The preliminary phase of the experiment, called "calibration," was performed for several reasons: we wished 1) to force subjects to pay attention to the amplitude of displacement rather than to other contingent factors such as duration or peak velocity; 2) to avoid effects due to uncertainty in controlling a nonfamiliar, although relatively slow, transport vehicle in darkness; and 3) to obtain information about subjects' ability to estimate distance of passive transport. The subjects were requested to drive the robot a distance of exactly 2 m in complete darkness. The experimenter then told the subject the exact distance just traveled, and another attempt was made. This exercise was repeated until the response was stabilized at ~2 m, but a minimum of 10 trials was imposed even when apparently not necessary.
CONDITION 1: TRIANGULAR VELOCITY PROFILE.
The subject was passively randomly displaced along 2, 4, 6, 8, or 10 m with the headphones and the black goggles on. Velocity profiles of most stimuli (13 of 16) were triangular, i.e., with equal values of accelerations and decelerations in the range of 0.06-0.5 m/s2. Peak velocity ranged from 0.6 to 1 m/s (Table 1). This profile was chosen to produce a continuous stimulation of the otoliths by linear acceleration. Three stimuli with constant velocity profiles (0.4, 0.6, and 0.8 m/s) were also applied over distances of 4, 6, and 8 m, with acceleration and deceleration at 0.8 m/s2. In contrast with the triangular profile, this provided only brief stimulation of the otoliths at the beginning and at the end of the trajectories.
CONDITION 2: CONSTANT DURATION PROFILES.
In the first condition, the total distance and duration of the passive transport were not independent. Therefore, to prevent the subjects from using the duration of transport as a cue to reproduce distance, we devised a second condition in which different velocity profiles of same duration (16 s) for all distances were used.
Data analysis
REPRODUCTION OF VELOCITY PROFILES.
Inspired by a two-dimensional cross-correlation analysis, a method was developed to provide an index of resemblance between the stimulus and response velocity profiles. Our aim was to obtain a comparison of shapes regardless of errors in distance, duration, or peak velocity reproduction. The first step in the procedure was a normalization of the time scales of both stimulus and response profiles, separately, from 0 to 100%. The number of samples of the profiles was reduced to 100 by averaging adjacent points. Because the number of points constituting a profile initially ranged from 1,000 to 2,000, it follows that from 10 to 20 adjacent points were averaged; this corresponds to a cutoff frequency of 5-10 Hz for a moving average filter. Because the profiles were previously filtered at 5 Hz to eliminate high-frequency, low-amplitude noise, this additional filtering did not markedly alter the relevant characteristics of the signals. Then, all of the normalized trials from the same subject or from the same stimulus were averaged, so as to reduce noise/random variability stemming from the manipulation of the joystick. Finally, the root mean square (RMS) of the differences between the averaged stimulus and response velocity profiles was taken as a quantitative index of mutual resemblance.
STATISTICAL ANALYSIS.
Appropriate analysis of variance (ANOVA) designs were used to compare the data from individual trials between different conditions, with either response total magnitude (distance or duration) or algebraic error (response Calibration
The average traveled distance of the very first trial of the calibration test was 1.55 m, i.e., this first trial induced on average a 22.5% undershoot error with respect to the required 2-m distance, and interindividual variability was ±0.52 (SD) m. The distance was much closer to 2 m (1.90 m, i.e., 5% undershoot error) and the interindividual SD was lower (±0.31 m) at the end (the 10th trial) of this preliminary exercise. It can be seen (Fig. 3) that a plateau in performance was already reached by the fifth trial (1.95 ± 0.27 m, mean ± SE), and successive trials exhibited about the same error. The difference between the 1st and the 10th trial distance was significant [F(1,14) = 5.44, P = 0.035], as was the difference between the 1st and the 5th trials [F(1,14) = 6.63, P = 0.022]. The difference was also significant between the 1st trial and each of the trials after the 5th, whereas there was no significant difference between the 5th and the 10th trials.
Triangular velocity condition
DISTANCE REPRODUCTION.
Subjects were able to reproduce the distances (Fig. 4) with an average overall accuracy of 25% (SD of the pooled relative errors, n = 232). The linear regression between stimulus and response distance was calculated for each subject with all the 16 trials (an example is shown in Fig. 4B). Regressions from the individual subjects are presented in Fig. 4A, inset. The average of the individual regression lines (Table 3) is shown in Fig. 4A, together with the means and SEs of the reproduced distances. The correlation coefficient r was highly significant for all subjects (P < 0.0001).
DURATION REPRODUCTION.
As mentioned in METHODS, with the triangular velocity profile, stimulus duration and stimulus distance were interdependent. Therefore the duration of the stimulus could provide some information assisting its reproduction. Indeed, the subjects also reproduced the duration of the stimulus (Fig. 5, Table 3), although the instruction was to reproduce the distance. The value of r was highly significant for each subject (P < 0.0001, except for 1: subject EC obtained P < 0.0013). Only subject EC displayed a "step strategy," i.e., with joystick manipulations of short duration and displacement at high velocity; this subject was nevertheless as accurate as the others in reproducing distance.
VELOCITY REPRODUCTION.
There was no correlation between stimulus peak velocity and distance, and therefore stimulus peak velocity could not be of any help for the subjects to reproduce the distance. However, most subjects did reproduce stimulus peak velocity. The value of r was significant for all subjects (P < 0.01) but four (subjects LC, EC, II, and MB). The average determination coefficient (Table 3) was therefore lower than that of distance and duration.
INTERDEPENDENCE AMONG DISTANCE, DURATION, AND VELOCITY.
To examine whether stimulus duration or peak velocity had been used by the subjects to reproduce distance, we applied a multiple regression analysis to our data, with reproduced distance as the dependent variable and stimulus distance, duration, and peak velocity as independent variables. The results indicate that the response distance can only be attributed to the stimulus distance (Table 4A), and neither to stimulus duration nor peak velocity. The response is correlated with stimulus duration (Table 4A), but this correlation results from the existing correlation between stimulus distance and duration.
VELOCITY PROFILE.
Whereas the peak velocity was not a relevant parameter for judging and reproducing distance, subjects frequently reproduced the stimulus velocity profile (Fig. 1C). Only subject LC produced very asymmetric triangular profiles, whereas subject EC systematically used a rectangular velocity profile, reaching the maximal velocity of the robot on short duration. Subjects II and MB exhibited variable combinations of velocity profiles. Nevertheless, distance reproduction was not markedly different from that of the other subjects, who produced mostly triangular responses.
Constant duration condition
The multiple regression analysis applied on the triangular velocity profile trials allowed us to establish that duration was not the main cue used by the subjects. Furthermore, there was some indication that subjects also reproduced the velocity profile of the passive transport. We then designed a second condition with another set of stimuli, characterized by three velocity profiles of identical duration (Table 2). We wanted to check whether duration was indeed not necessary to reproduce the corresponding distance, and whether subjects would also reproduce velocity profiles when they are not triangular.
DISTANCE REPRODUCTION.
As expected, although stimulus duration was not a valid predictor of its distance, subjects did reproduce the imposed distance (Fig. 6) as well as in the first condition: overall accuracy (as measured by the SD of the relative error) was 35% (n = 132), with 25% (n = 44) for the triangular profile, 28% for the trapezoid profile, and 47% for the rectangular profile. The average of the individual regression lines (each line computed on the basis of 5 measures) for each velocity profile as well as for all three pooled profiles (15 measures; Fig. 6A) is given in Table 5. For the rectangular profile, r was significant for all subjects but subject EC. The determination coefficient (r2) obtained from the rectangular profile was lower than that resulting from the other profiles, but a two-factor repeated-measures ANOVA (profile type × distance) on the reproduced distance showed no effect [F(2,16) = 0.67, P = 0.52] or interaction [F(8,64) = 0.62, P = 0.75] due to the velocity profile.
DURATION REPRODUCTION.
In this condition stimulus duration did not vary and the average response duration was very close to that of the stimulus: 14.14 ± 1.21 s (n = 132). There was no significant difference between the duration errors for the three profiles. The average error was VELOCITY REPRODUCTION.
In this condition, in which stimulus duration and distance were not correlated, stimulus maximal velocity could have been used to provide some information about distance. Stimulus peak velocity and distance of the five trials were indeed strongly interdependent for all velocity profiles.
VELOCITY PROFILE.
Subjects reproduced the velocity profile of the stimuli more closely for longer distances (Fig. 7A). A global overshoot at the onset of the reproduction can be seen, principally in the triangular profiles. This was probably due to the relatively long delay of the joystick control(0.2 s).
A passive displacement can be represented in static as well as in dynamic terms. That is to say that we could refer to an experienced travel either as a 10-m, 10-s linear displacement or as a motion at a gradually increasing speed followed by a deceleration up to a stop. These two representations might coexist in short-term memory or, alternatively, only one might be stored. In this latter case, if the dynamic representation is the one available, static estimates could be derived by reprocessing it. On the other hand, motion dynamics would be lost if only static parameters are stored.
Calibration task
In this initial experiment, subjects were asked to drive the robot in darkness over a 2-m linear path with the joystick. Klatzky et al. (1990) Reproduction task
REPRODUCTION OF DISTANCE.
The present work brought contrasting evidence about the mechanisms of distance perception because 1) the strategy selected by most subjects to reproduce distance (the assigned task) was to reproduce the velocity profile, i.e., the spatiotemporal dynamics of the passive transport, but 2) regression analyses indicated that distance reproduction was not correlated with the accuracy of duration, peak velocity, or velocity profile reproduction. Thus the results suggest that whereas the dynamics of passive motion are stored and available to further use, total distance is probably independently estimated.
REPRODUCTION OF DISTANCE WITH DURATION AND PEAK VELOCITY.
The different statistical analyses indicated that no motion parameter (including the velocity profile) significantly contributed to the accuracy of reproduction of distance. On the other hand, reproduction of duration appeared secondary to distance. The indication given by this method was confirmed by the constant duration experiment, in which the duration of the stimulus was kept constant. Indeed, the accuracy in reproducing distance was the same as when duration varied proportionally to distance. Therefore we conclude that distance was not estimated from related magnitudes. This is not surprising, because we have previously shown (Israël and Berthoz 1989 RANGE EFFECT.
Whereas during calibration an undershoot of the requested 2 m was observed, in the reproduction task the subjects overshot 2-m trials but undershot larger distances. These distortions in the reproduction task can be interpreted as a manifestation of the "range effect," also known as "regression to the mean effect" or "central tendency effect" (overshoot of small distances and undershoot of large distances of a given set) (Poulton 1979 COMPARISON WITH LOCOMOTION EXPERIMENTS.
There is a close resemblance between our results and those obtained by Loomis et al. (1993) How are the motion dynamics matched during the reproduction?
An important finding of this (and the previous) work is that motion dynamics are stored during the passive displacement and played back during the reproduction phase. There are many ways such a behavior can be modeled. Figure 8 shows a simple schema that summarizes our concept. The schema is made of two parts: 1) the passive transport phase and 2) the active transport phase. The actual acceleration drives the otoliths (and somatosensory system), the output of which is stored in a dynamic short-term memory. Then memory feeds a comparator of a negative feedback controller. The block labeled "robot control" represents the feedback gain. The robot acceleration profile provides the input to the otoliths, whose output is in turn compared with the memorized input profile. This generates an error signal driving the active reproduction of passive motion dynamics.
General remarks
A careful quantitative analysis of the results of the present experiment allows us to conclude that vestibular and somatosensory signals generated by passive transport can be used to build a dynamic as well as a static representation of the traveled path. Recent studies have already provided some neurophysiological background to understand the present findings: by transporting monkeys on a robot-mounted platform in complete darkness, O'Mara et al. (1994)
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
) are the sensory signals generated by the displacement of a subject: optic flow, proprioception, efference copies, and inertial signals. Mittelstaedt and Mittelstaedt (1980, 1982) hypothesized the use of these idiothetic signals for spatial orientation in the "path integration" process. Through path integration the position of a moving subject is continuously updated with respect to the starting point, and therefore the subject is able to compute the homing direction at any time. Recent studies in humans (Bloomberg et al. 1991; Glasauer et al. 1994; Israël and Berthoz 1989; Klatzky et al. 1990; Loomis et al. 1993; Mittelstaedt and Glasauer 1991; Thomson 1983) have shown that subjects can indeed estimate the traveled path solely from self-generated information, i.e., without external signals (visual or acoustic landmarks).
and Etienne et al. (1988) found that rodents could correctly home after passive rotations in darkness, but not after passive linear displacements. Although in a more recent study, Mittelstaedt and Glasauer (1991) showed that linear inertial forces imposed to active homing trajectories are taken into account by rodents, the former results did cast some doubt on the use of linear inertial information in the path integration process. However, passive linear displacement estimation in humans has been studied with a number of different paradigms
through verbal estimates (Guedry and Harris 1963), saccadic eye movements (Israël and Berthoz 1989), or button-pushing responses (Israël et al. 1993; Mittelstaedt and Glasauer 1991)and all of these studies showed that the amplitude of passive linear motion can be correctly estimated.
; Maurer and Séguinot 1995 for critical reviews), with or without distance estimation, the neural mechanisms involved in the process are still to be clarified. Spatial memory plays a key role here inasmuch as an internal coding of the distance and direction of the perceived motion has to be built and stored by the brain.
) we provided qualitative evidence about the type of memory encoding of simple whole body passive linear displacements in darkness. Subjects required to reproduce the distance of an imposed passive motion also reproduced its velocity profile. This implies that all the spatiotemporal properties of movement are stored and that reproduction is based on the dynamic comparison of the incoming sensory input with the stored one. However, such a process does not exclude the possibility that static parameters of motion may also be either independently stored or retrieved from spatial memory.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
View larger version (37K):
[in a new window]
FIG. 1.
A: subject is seated on robot, with black goggles, headphones, and bite bar in place, and is using joystick. Two modems (1 at top of robot seat and the other close to microcomputer) can also be seen. B: stimulus and response position for trial of 10-m distance and 1-m/s peak velocity in 1st (triangular velocity) condition for 15 subjects. C: stimulus and response velocity for trials in B (derivation after 5-Hz low-pass filtering of position traces). D-F: some examples of stimulus and response velocity in a previous test in which subjects had to reproduce velocity of stimulus.
View this table:
TABLE 1.
Triangular velocity condition stimuli
) corresponding to each profile is shown in Fig. 2. With the triangular profile it was not possible to travel the 2- and 10-m stimuli in 16 s, given the limited velocity range of the robot: the durations were 13.33 and 20 s for the 2- and 10-m stimuli, respectively.
View this table:
TABLE 2.
Constant duration condition stimuli
View larger version (23K):
[in a new window]
FIG. 2.
Otolith response to acceleration profiles of 2nd condition, simulated with the use of the transfer function developed by Ormsby and Young (1977) . Dashed lines: result of simulation (MOD). Solid lines: input signal. Thin lines: data from "artificial" (ideal) profiles (ART). Heavier lines: data recorded and derivated from robot odometry (REC) after 3-Hz low-pass filtering. All 3 profiles generated a 6-m distance.
stimulus) as dependent variables. The relative error (response stimulus)/stimulus was used to quantify overall accuracy. Linear regressions of individual trials were performed to quantify the stimulus-response relationship from the subjects. A probability level of 0.05 was considered significant. Multiple regression analysis was performed to estimate the relative importance of the respective stimulus parameters in determining the response.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
View larger version (13K):
[in a new window]
FIG. 3.
Calibration. Performance of subjects during calibration test: average and SE for all 15 subjects shown with respect to trial number.
View larger version (16K):
[in a new window]
FIG. 4.
Distance reproduction (1st condition). A: average (- - -) of all individual lines of 15 subjects, and average ± SE of each reproduced distance. Average determination coefficient r2 was 0.85. Inset: individual regression lines between stimulus and response distance for 15 subjects. B: responses of subject BJ, with corresponding regression line (- - -).
View this table:
TABLE 3.
Linear regressions: R = A*S + B, triangular velocity
View larger version (19K):
[in a new window]
FIG. 5.
Duration reproduction. A: individual regression lines between stimulus and response duration for 15 subjects. B: responses of subject BJ with corresponding regression line.
0.04 ± 0.04 m/s in the triangular trials.
View this table:
TABLE 4.
Multiple regression on distance reproduction and duration reproduction in the triangular velocity condition
View larger version (18K):
[in a new window]
FIG. 6.
Distance reproduction (2nd condition). A: average (- - -) of all individual lines of top left inset, and average and SE of each reproduced distance. Top left inset: individual regression lines between stimulus and response distance of 3 profiles pooled (n = 15) for 9 subjects. Bottom right inset: average regression lines between stimulus and response distance for 3 profiles. B: responses of subject BJ with corresponding regression line.
View this table:
TABLE 5.
Linear regressions: R = A*S + B, constant duration
1.41 ± 0.93 s (n = 9) with the rectangular velocity profile, 0.65 ± 0.84 s with the trapezoid profile, and 2.17 ±0.63 s with the triangular profile: response duration was shorter than stimulus duration in all cases.
7.40 s, whereas the error of the six remaining subjects was0.52 ± 0.36 s; the difference was larger than in the first condition (4.91 s for subject EC vs. 0.59 ± 0.76 s for the 6 remaining subjects). Subject EC apparently applied the step strategy with still more conviction when deprived of temporal information correlated to distance, without losing accuracy in fulfilling the task.
View larger version (55K):
[in a new window]
View larger version (38K):
[in a new window]
FIG. 7.
Velocity reproduction (2nd condition). A: all velocity responses to all trials of all subjects (except subject EC) are shown for each profile and each distance. Heavy line: stimulus. B: normalized response (velocity and duration) averaged over all trials of same velocity profile for 3 subjects (RG, YT, and BJ), mean ± SD, with cumulated velocity error. Dotted line: stimulus. Heavy line: mean velocity. Thin lines: mean ± SD.
View this table:
TABLE 6.
Velocity profile reproduction
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
), to address the relationship between motion perception and path integration. Blindfolded subjects were asked to reproduce the perceived distance of a linear passive displacement by directing another passive motion.
used the same distance to "train" their subjects in an experiment on locomotion. It is indeed reasonable to assume that humans should have some meaningful representation of such a short length. The results showed that all subjects but two undershot this distance (i.e., subjects overestimated their own self-traveled distance) by 22% in the first trial with an interindividual variability >25%. Such a considerable undershoot and variability suggest that either subjects have a very variable representation of the required length, or the vestibular and somatosensory inputs are not calibrated to correspond to a metrical representation of distance.
in another linear displacement task. Subjects, blindfolded and with ears plugged, sitting on a sled that moved along the X-axis, had to push a button when they thought that the sled passed a previously seen target (the distance here was 2.4 m): the button was pushed at 1.57 ± 0.37 m during the displacement. Despite methodological differences (the displacement was passive and not self controlled; the task was goal directed and not amplitude coded; and the expected response was at 2.4 m, not 2.0 m), the error is quantitatively similar. Because the target was seen by the subjects in this former experiment, the previous hypothesis of a variable metrical representation of the 2-m length is weakened. Another explanation can be suggested for both cases: in the former experiment the undershoot was explained as a consequence of a double integration over time of otolith discharge, including the initial overshoot that is induced by an acceleration step (see Berthoz and Droulez 1982 for a review). It is possible that such a process occurred also in the present experiment.
; Israël et al. 1993; Mittelstaedt and Glasauer 1991), and the relative accuracy in total distance reproduction do not favor, in our opinion, this last hypothesis. Subject EC must have retained or reconstructed some internal static estimate of the imposed path and disregarded the dynamic information in the reproduction task.
) that the otoliths are necessary to estimate a passive linear whole body displacement with respect to an earth-fixed memorized visual target, and to acquire this target with eye saccades.
; Stevens and Greenbaum 1966). The effect was observed both for the reproduced distance and for the duration in the triangular velocity condition, whereas it almost disappeared in the constant duration condition. Because this effect is characteristic of judgments of sensory magnitude (Poulton 1979), the subjects might have implicitly estimated both distance and duration, although the instruction was about distance only. The absence of range effect in the constant duration condition suggests that this effect can be mainly ascribed to the estimation of duration.
. In the experiment of Loomis et al., blindfolded subjects were first led by the experimenter while walking along a path 2-10 m long (the same distances as in the present experiment), and the subjects then had to reproduce the same distance while blindfolded and without aid. The reported results are strikingly similar to the present ones: the 2-m distance was overshot by 0.26 m (0.31 ± 0.12 m in the present test) and the 10-m distance was undershot by 1.02 m (0.79 ± 0.33 m here). This resemblance suggests that there are important parallels between active locomotion and the self-controlled passive displacement we have used in the present study. It should be noted that the motion parameters (speed and acceleration) selected for passive motion were much in the physiological range of normal locomotion.
) might participate in the updating of position during motion.
: those authors found that subjects passively transported in darkness toward a previously seen target tended to underestimate (in the range of linear velocity and distance used in the present experiment) the traveled distance, whereas the opposite happened during active locomotion. Mittelstaedt and Glasauer proposed the idea that a leaky path integrator, loaded with the visually estimated distance, processes incoming inertial signals: the reference distance is differently included in the processing during passive transport and active locomotion, respectively. If we applied the same rule to the present experiment, we would obtain a large undershoot of reproduced versus imposed distances, which was not the case. The similarity between the passive and active transport phases in our experiment might have caused the same processing of inertial signals to occur in both phases. Because of the important methodological differences between both experiments (i.e., the visually acquired reference distance and the proprioceptive locomotion-related signals of the above quoted experiment), further comparison would be pointless.
; de Graaf et al. 1994; Hlavacka et al. 1992). Tactile cues may complement vestibular information, providing 1) a signal related to the body linear acceleration (pressure on the back, visceral shifts, etc.) and 2) a signal generated by robot vibrations. The subjects could have correlated all of these signals with visually perceived velocity during the very preliminary training (before the calibration task). However, the training phase was unlikely to influence the strategy of reproduction, because the performance of the subjects who participated in the constant duration condition was not different from that displayed in the first condition, although no training was performed before the second condition. Therefore it is highly improbable that the somatosensory input generated by vibrations (which are peculiarly linked to the robot and ground characteristics) was calibrated.
). This result does not rule out the participation of tactile cues to the estimation process, but it confirms the importance of the otolith signals.
View larger version (8K):
[in a new window]
FIG. 8.
Simple schema of distance reproduction paradigm. Graph labeled "stimulus" includes all dynamic properties of passive motion. OTOLITHS actually includes all idiothetic signals available in present experiment (i.e., those due to vestibular and somatosensory systems), and box labeled "robot control" covers all robot and joystick parameters.
; Shelhamer and Young 1994; Young and Meiry 1968) revealed that integration over time of the otolith-induced neural discharge occurs over the whole frequency range of the stimuli employed in the present study, leading to a close relationship between the perceived and the actual linear velocity (Young 1984). On the grounds of these latter findings it can be proposed that feedback control is carried out on linear speed rather than acceleration. As mentioned above, a second time integration of sensory input may occur (Israël et al. 1993) and feedback control could be theoretically performed on instantaneous position. This last possibility corresponds to the true path integration hypothesis (Mittelstaedt and Mittelstaedt 1982), which is a very attractive one because it would attribute to one and the same process both the static and the dynamic characteristics of the subjects' responses. In such a case, the static estimate of distance would correspond moment by moment to the current stored value of the dynamic profile and no reprocessing of recorded signals should be needed.
found hippocampal neurons responding to linear motion and others responding to axial rotation; cells belonging to the rat hippocampal formation that code head direction in space have now long been known (McNaughton et al. 1983); changes in rat hippocampal theta activity correlated to the velocity of angular rotation in the yaw plane have been demonstrated (Gavrilov et al. 1996). The improving description of neural ascending pathways (Grüsser et al. 1992; Muller et al. 1996) bringing multisensory motion-related information to the cortex led to the identification of computational (Wan et al. 1994) and biological (McNaughton et al. 1996) models of a corticothalamohippocampal navigation system that work by updating position and direction in space in real time.
) suggests that these two types of navigation tasks draw on common physiological processes and extend the relevance of our results to more ecological behaviors of path integration.
| |
ACKNOWLEDGEMENTS |
|---|
We are grateful to A. Treffel for the mechanical adaptation of the Robuter, and to S. Glasauer for the design of the Robuter-experimenter interface software.
This work was supported by the Commission of European Communities programs Esprit Basic Research project 6615 (MUCOM) and Biomed BMH1-CT94-1133. R. Grasso was supported by the Fondation pour la Recherche Médicale and the Training and Mobility of Researchers program of the CEC. T. Tsuzuku was supported by the Fondation Fyssen (France).
| |
FOOTNOTES |
|---|
Address for reprint requests: I. Israël, Laboratoire de Physiologie de la Perception et de l'Action, CNRS, Collège de France, 11, place Marcelin Berthelot, 75005 Paris, France.
Received 17 July 1996; accepted in final form 20 February 1997.
| |
REFERENCES |
|---|
|
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
enreize.
Fortschr. Zool.
21: 46-58, 1973.This article has been cited by other articles:
|
|
 |
|
  N. Dominici, E. Daprati, D. Nico, G. Cappellini, Y. P. Ivanenko, and F. Lacquaniti Changes in the Limb Kinematics and Walking-Distance Estimation After Shank Elongation: Evidence for a Locomotor Body Schema? J Neurophysiol, March 1, 2009; 101(3): 1419 - 1429. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Marlinski and R. A. McCrea Activity of Ventroposterior Thalamus Neurons During Rotation and Translation in the Horizontal Plane in the Alert Squirrel Monkey J Neurophysiol, May 1, 2008; 99(5): 2533 - 2545. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. M. Klier, B. J. M. Hess, and D. E. Angelaki Human Visuospatial Updating After Passive Translations in Three-Dimensional Space J Neurophysiol, April 1, 2008; 99(4): 1799 - 1809. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. M. Seemungal, S. Glasauer, M. A. Gresty, and A. M. Bronstein Vestibular Perception and Navigation in the Congenitally Blind J Neurophysiol, June 1, 2007; 97(6): 4341 - 4356. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. A. Yong, G. D. Paige, and S. H. Seidman Multiple Sensory Cues Underlying the Perception of Translation and Path J Neurophysiol, February 1, 2007; 97(2): 1100 - 1113. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Glasauer, E. Schneider, R. Grasso, and Y. P. Ivanenko Space-Time Relativity in Self-Motion Reproduction J Neurophysiol, January 1, 2007; 97(1): 451 - 461. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R.A.A. Vingerhoets, W. P. Medendorp, and J.A.M. Van Gisbergen Time Course and Magnitude of Illusory Translation Perception During Off-Vertical Axis Rotation J Neurophysiol, March 1, 2006; 95(3): 1571 - 1587. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. M. Merfeld, S. Park, C. Gianna-Poulin, F. O. Black, and S. Wood Vestibular Perception and Action Employ Qualitatively Different Mechanisms. I. Frequency Response of VOR and Perceptual Responses During Translation and Tilt J Neurophysiol, July 1, 2005; 94(1): 186 - 198. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Li, M. Wei, and D. E. Angelaki Primate Memory Saccade Amplitude After Intervened Motion Depends on Target Distance J Neurophysiol, July 1, 2005; 94(1): 722 - 733. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. W. Stackman, E. J. Golob, J. P. Bassett, and J. S. Taube Passive Transport Disrupts Directional Path Integration by Rat Head Direction Cells J Neurophysiol, November 1, 2003; 90(5): 2862 - 2874. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. P. Medendorp, D. B. Tweed, and J. D. Crawford Motion Parallax Is Computed in the Updating of Human Spatial Memory J. Neurosci., September 3, 2003; 23(22): 8135 - 8142. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
