Direction and distance deficits in path integration after unilateral vestibular loss depend on task complexity

Cognitive Brain Research 25 (2005) 862 – 872 www.elsevier.com/locate/cogbrainres

Research Report

Direction and distance deficits in path integration after unilateral vestibular loss depend on task complexity Patrick Pe´ruch a,*, Liliane Borel b, Jacques Magnan c, Michel Lacour b a

Laboratoire de Neurophysiologie et Neuropsychologie, INSERM and Universite´ de la Me´diterrane´e, Faculte´ de Me´decine de la Timone, 27 Bd Jean Moulin, 13385 Marseille Cedex 5, France b Laboratoire de Neurobiologie Inte´grative et Adaptative, CNRS and Universite´ de Provence, Centre Saint-Charles, Poˆle 3C, Case B, 3 Place Victor Hugo, 13331 Marseille Cedex 03, France c Service d’ORL et de Chirurgie Cervico-Faciale, Chemin des Bourrelly, CHU Marseille Nord, 13015 Marseille Cedex 20, France Accepted 20 September 2005 Available online 26 October 2005

Abstract The effects of peripheral vestibular disorders on the direction and distance components of the internal spatial representation were investigated. The ability of Menie`re’s patients to perform path integration was assessed in different situations aimed at differentiating the level of spatial processing (simple versus complex tasks), the available sensory cues (proprioceptive, vestibular, or visual conditions), and the side of the path (towards the healthy versus the lesioned side). After exploring two legs of a triangle, participants were required either to reproduce the exploration path, to follow the reverse path, or to take a shortcut to the starting point of the path (triangle completion). Patients’ performances were recorded before unilateral vestibular neurotomy (UVN) and during the time-course of recovery (1 week and 1 month) and were compared to those of matched control subjects tested at similar time intervals. Both the angular and linear path components of the trajectory were impaired for patients compared to controls. However, deficits were restricted to the complex tasks, which required a higher level of spatial processing. Most deficits were maximal 1 week after UVN, and some remained up to the first post-operative month. Spatial representation was differentially impaired according to the available sensory cues: deficits were absent in active locomotor blindfolded condition, appeared in conditions involving visual and vestibular information, and were maximal when visual cues alone were available. Finally, concerning the side of the path, unilateral vestibular loss led to global impairment of the internal spatial representation, yet some asymmetrical spatial performances were observed 1 week after UVN. On the whole, results suggest that the environment experienced by the patients is different after UVN and that a different internal spatial representation is constructed, especially for tasks requiring high levels of spatial processing. D 2005 Elsevier B.V. All rights reserved. Theme: Neural basis of behavior Topic: Learning and memory, systems and functions Keywords: Human navigation; Unilateral vestibular disease; Sensory system; Vestibular compensation; Internal spatial representation; Level of spatial processing

1. Introduction Spatial orientation and navigation involve different processes, such as sensing the environment, building up a mental spatial representation, and using it [28]. During navigation, one’s mental representation of the current * Corresponding author. Fax: +33 4 91 78 99 14. E-mail address: [email protected] (P. Pe´ruch). 0926-6410/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.cogbrainres.2005.09.012

position and orientation in the environment is updated. Spatial updating may be carried out either on the basis of exteroceptive information about the environment (piloting), on the basis of proprioceptive and vestibular information from self-movements through the environment (dead-reckoning or path integration), or on the basis of both [15,35,41]. Some species, including humans, are able to elaborate and use complex mental representations or ‘‘cognitive maps’’, which are well suited for navigation in large-scale environ-

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

ments. However, path integration is more adapted to smallscale navigation and is common to several species. Under normal conditions of navigation, visual, proprioceptive, and vestibular systems provide congruent information. Although the olfactory and auditory systems are extremely developed in some species, vision usually plays a predominant role, especially in humans. The optic flow provides information about the environment and about the pattern of motion of the observer [16,17,24,45]. Muscle and joint receptors give kinesthetic information about relative head and limb positions, whereas the vestibular inertial system specifies self-motion trajectory through angular and linear accelerations of the head [4,23,38]. The direction and distance components of the trajectories are differently processed by the sensory systems. While optic flow can be used for path integration over turns and distances [24], proprioceptive cues are better suited for the perception of rotations than of translations [12,40]. The contribution of the vestibular system in spatial orientation was first investigated by Worchel [46] and Beritoff [3]. Although there is wide support for the role of vestibular cues in the control of the direction component, the need for such sensory cues is debated for the distance component. The contribution of the vestibular system in angular displacement estimation has been reported for passive whole body rotations in healthy subjects [6,21] and in patients with labyrinthine disease [33]. The authors showed a deterioration of orientation after vestibular loss. More precisely, a unilateral loss of vestibular function induced an asymmetrical perception of space orientation [44]. Using active locomotion, Glasauer et al. [19] showed that vestibular loss led to impaired control of the direction of turns. Detection and memory of linear displacements by the vestibular otolithic receptors allow normal subjects to estimate passive translational displacements [4,7,22] and active walking [30,34,43]. Unilateral vestibular-defective patients have impaired linear path integration during active goal-directed locomotion, since they walk more slowly and veer earlier than controls [13]. In addition, the vestibular loss-induced deviations depend on the locomotion speed: deviations were greater for slow-speed than for high-speed locomotion [9]. However, in these studies patients were not required to estimate distance. Research dealing with distance estimation has shown that bilateral labyrinthinedefective subjects estimate the length of displacement under

863

blindfolded conditions as well as healthy subjects do in a goal-directed linear locomotion task [18], and in a locomotor navigation task along a triangular path [19,46]. The above studies, however, used simple tasks in which subjects had to acquire spatial knowledge during passive transport or during active walking through an environment. We designed an experiment contrasting simple and complex tasks, with path reproduction considered as a simple task, and path reversing and shortcutting (triangle completion) considered as complex tasks. Complex tasks such as shortcutting require the integration of distance and orientation information along the exploration path (they involve a survey-type mental representation), while simple tasks require only keeping in memory such information (they involve a route-type mental representation) [20,28]. The triangle-completion task has frequently been used to study the role of vestibular and proprioceptive information and, separately, the role of visual information in path integration [24,26,28,34,36,39]. Path reproducing or reversal is also found in a number of studies. But the three tasks had never been used in the same protocol with the same participants. Such a procedure would serve to disentangle the respective role of visual, vestibular, and proprioceptive inputs in situations susceptible to require the integration of spatial information (complex versus simple tasks). Consequently, we hypothesized that the consequences of unilateral vestibular loss on spatial performance would depend on task complexity. Based on our previous work [37], unilateral vestibular neurotomy (UVN) was expected not to alter patients’ performance for simple tasks, whatever the post-operative time, and for both turn and distance parameters. Indeed, we had shown that after unilateral vestibular loss, deficits were restricted to tasks requiring the highest level of spatial processing (spatial inference and route reversing) and concerned the direction component only. By contrast, in the present study one might expect spatial deficits for complex tasks for both parameters, with maximum impairments 1 week after UVN. Indeed, the internal spatial representation resulting from a multisensory integration process that combines visual, vestibular, and proprioceptive cues should be easier to elaborate in simple than in complex tasks. In addition, we presumed that the overall spatial deficits would predominate in experimental conditions with real motion (that stimulate the vestibular system) compared to navigation in a visual virtual environment [37]. Table 1

Table 1 Expected effects: no effect ( ), possible effect (T), and significant effect (+) of unilateral vestibular loss on direction and distance parameters as a function of task complexity (simple versus complex), testing periods (D 1: 1 day before UVN; D + 7: 1 week after UVN; D + 30: 1 month after UVN), and available sensory cues (Real: real motion cues; Virtual: visual motion cues) Direction

Distance

Simple tasks D Real Virtual

1

D+7

Complex tasks D + 30

D T

1

Simple tasks

D+7

D + 30

+ +

T

D

1

D+7

Complex tasks D + 30

D

1

D+7 + +

D + 30

864

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

summarizes the expected effects. To answer these questions, we analyzed the respective contributions of visual, proprioceptive, and remaining vestibular cues in path integration after unilateral vestibular loss. Finally, we investigated whether the internal spatial representation was globally or asymmetrically impaired after unilateral vestibular loss.

2.2. Sessions Patients and controls were submitted to three experimental sessions. For the patients, the first session was 1 day before UVN (D 1), the second after 1 week (D + 7, acute stage), and the third after 1 month (D + 30, compensatory stage). The intervals between the three sessions were the same for the control participants.

2. Materials and methods 2.3. Conditions 2.1. Participants Experiments were carried out on 7 unilateral (4 left, 3 right) vestibular-defective patients with intractable Menie`re’s disease and 7 healthy controls. Clinical diagnostic criteria for Menie`re’s disease are sudden attacks of vertigo, hearing loss, and tinnitus. Menie`re’s disease has its origin within the labyrinth. For the patients tested in this study, neurotomy of the vestibular nerve was used as treatment of intractable vertigo in Menie`re’s disease. Patients included 3 women and 4 men (mean age 50.6, SD 8.8). All patients had normal visual status and no specific motor or visuomotor disorders. The healthy group was matched in age (mean age 42.4, SD 9.7) and education level and selected on the basis of normal vestibular and visual functions. Patients and controls gave informed consent to the study, which was approved by the local ethics committee (CCPPRB Aix-Marseille I). Each patient described the classical triadic symptomatology of hearing loss, tinnitus, and recurrent vertigo and had been forced to stop their professional activity. They all underwent a thorough neurological investigation prior to therapy. The criteria for deciding on surgical treatment included drug treatment failure (since the patients became resistant to antivertigo substances), frequency of vertigo attacks, and vestibular and hearing loss [29]. UVN was used to eliminate vertigo and to preserve hearing. The unilateral vestibular deficit was determined by bithermal caloric irrigation with cold (30 -C) and warm (44 -C) water, for each ear. The induced vestibulo-ocular responses reflect the degree to which the vestibular system is responsive and the symmetry between left and right responses. All patients exhibited pure unilateral deficits with a vestibular deficit to the caloric test averaging 38.7 T 20.8% (range: 8– 75%). Audiological assessment indicated a mean hearing loss of 45 T 36% (range: 7– 100%) of the affected ear. The history of vertigo lasted from 2 to 20 years (mean: from 7 T 6 years). Five of the seven patients complained of a weekly occurrence, and the other two of monthly occurrence. The surgical procedure was a retrosigmoid vestibular nerve section. All patients were able to ambulate two or 3 days after surgery. During the post-operative period they received no drug that could have influenced their performance. One week after, UVN patients were able to walk, turn, and maintain balance. The caloric test showed a total lack of response on the lesioned side at this time as well as later on.

All participants were tested for spatial knowledge acquisition in three conditions requiring various sensory cues, which were performed in real and virtual environments. The virtual environment was presented via an immersive helmet-mounted display (see below). Each situation alternated exploration paths, during which the participants were instructed to memorize the visited locations, with test paths during which the participants were required to reach the locations from memory, following the experimenter’s instructions. The exploration path was as follows (see Fig. 1): from a starting location A, there was a first leg of 3 m to a second location B, from which there was a second leg of 3 m to a third location C; at B, the two legs of the path were at right angles, to the right or to the left. In test paths, from the end of the exploration path (at C, facing back location B) the participants were asked to navigate to a specified location. Three series of tests were conducted (see Figs. 1 and 3). Patients were required either to reproduce the exploration path, to follow the reverse path, or to take a shortcut to the starting point of the path (triangle completion). Path reproduction was defined as simple tasks: the participants (at C, at the end of the exploration path) had to consider they were at the starting point of the exploration path and were required to reproduce the exploration path from A to B and from B to C. Path reversing and shortcutting were defined as complex tasks: in reversing tests, the participants had to produce the reverse path from C to B and from B to A; in shortcutting tests, the participants had to return directly from C to A.

Fig. 1. Top-view of the exploration path (illustrated here to the right) and of the three kinds of test paths: reproduction (simple tasks), reversing, and shortcutting (complex tasks). See Materials and methods for more details.

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

865

When performing the test paths, the participants were told to respond first by orienting themselves towards a target location, and then to move in a straight line until they estimated they had arrived at that location. No feedback on performance and no time limits were given: the participants were only asked to respond as accurately as possible. 2.3.1. Proprio-vestibular (PRO-VEST) condition This locomotor condition was performed in a 12  8 m empty room. The participants were blindfolded and wore headphones with white noise. They explored the spatial layout by walking; only proprioceptive and vestibular cues were available. To reassure them, they were first trained to walk blindfolded while an experimenter held them by the shoulders. The experimental session started only when the participants felt confident. The exploration path was marked with patches on the floor. The participants were placed at the starting location A, in the reference position facing B. They were informed that they occupied this location. The experimenter guided the participants to location B. Upon arriving at B the participants were stopped for 3 s and informed that they occupied this location. Then they were informed that the next location to visit was C, before being rotated and translated to C. When arriving at C, they were stopped and informed that they occupied this location (see Fig. 1). For each movement, a pure rotation (average speed about 30 deg/s) towards a location always preceded a pure translation (average speed about 1 m/s) to this location, and a pause of 3 s preceded and followed each movement. During the test paths, to prevent any loss of balance and to reassure the participants, the experimenter followed the participants, taking care not to touch them. A second experimenter marked on the floor the participant’s position for each target location. At the end of a test path, the experimenter held the participants by the shoulders and brought them back to the starting location via various indirect paths. When at A, the participants were oriented to B and informed of their location and orientation. Then they were guided along the exploration path before performing the next test, and so on. 2.3.2. Visuo-vestibular (VIS-VEST) condition A graphic PC-based desktop workstation (Pentium II 450 MHz, 256 Mo RAM, Glyder TX Gold 16 Mo graphics card, resolution 800  600 in true colors) was used to simulate a three-dimensional environment, built using 3 D Studio Max software. The virtual environment was composed of three objects (red, blue, and green cones), respectively, for the starting (A), intermediate (B), and ending (C) location of the exploration path, with an orange cylinder of about 15 m of diameter serving as a circular background (see Fig. 2). The ground was textured in order to provide rotational and translational cues [24]. The virtual environment was identical to the real one, that is, the locations of the three

Fig. 2. Perspective view in the virtual environment from starting location A. The environment is limited by an orange circular wall (in dark gray), and the ground is textured. The intermediate location (B) is 3 m forward, and the ending location (C, not visible from the starting location) is on the right side for the right exploration path.

objects corresponded to the physical locations marked by patches in the PRO-VEST condition. A real-time computer program, using RenderWare software, produced perspective views or scenes simulating observer motion through the environment. The frame rate was about 20 images per second. The observer’s viewpoint was set at 1.8 m high. In the experimental session, the participant was seated on a rotating chair, and wore a helmet (Sony Virtual IO-Glasses, 30-  22physical field of view, 832  624 pixel resolution) equipped with a sensor (Ascension 3 D-Bird) recording body movements in heading and roll directions (the pitch was set to zero by the software). Movement was performed in two ways by the observer through the virtual environment. Translations were controlled via a joystick (Space Mouse) that provided forward –backward translations, with movement restricted to the horizontal plane. Rotations were produced by the participant’s rotating movements of the chair and recorded via the sensor. Thus, both visual and vestibular cues were available. More precisely, since participants physically rotated but visually translated, information on rotation was gained from the labyrinth and from the rotational optic flow, while information on distance was gained from the translational optic flow. Finally, the proprioceptive information available when rotating the chair with the feet was considered negligible since the body itself was not transported as in the PRO-VEST condition. At the beginning of each experimental session, the participants practiced on the device for 10 min in a virtual environment with a different arrangement of objects. They were trained to manipulate the Space Mouse and to rotate the chair with their feet, without moving the head on the trunk. They were required to translate in a straight line with the mouse and to turn 90- or 180- right and left with the chair. After this training, none of the participants reported any difficulty in using the Space Mouse and in controlling their body orientation.

866

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

As in the PRO-VEST condition, exploration paths alternated with test paths. The participants moved from A to B and to C following the experimenter’s instructions. The exploration path was comparable to that of the PRO-VEST condition: translations and rotations were carried out at the same speed and with the same pauses. When the participants occupied the location of an object, this object was not visible (with the exception of the object at the starting point, see Fig. 2). Each test path started at the end of the exploration path. A new scene was presented with the objects removed; only the ground and the limiting wall remained. The participants were informed that they were at C, having their back to B, and were required to maneuver according to the experimenter’s instructions. At the end of a test path the trajectory was recorded. The participants were positioned again at A and performed an exploration path. Then the objects were removed for the next test, and so on. 2.3.3. Visual (VIS) condition As in the VIS-VEST condition, the participants were seated on the rotating chair and wore the helmet. However, the chair was immobilized and the sensor was deactivated so that all movements, including left-right rotations, were produced via the Space Mouse. Thus, only visual cues were available. As in the previous condition, participants received preliminary training when starting the experimental session. 2.4. Design The conditions were carried out in balanced order across sessions. For each condition, the participants performed three exploration paths (on the same side) alternated with three test paths. Then they performed three exploration paths alternated with three test paths on the other side. The side (left or right) was balanced across sessions, and for each side the tests (reproduction, reversing, or shortcutting) were presented in random order.

Each experimental session lasted about 90 min, including the training periods. 2.5. Data collection and analysis The participants were required to perform the tests as accurately as possible, without time constraints. Since such instructions were supposed to be more difficult to respect in the PRO-VEST condition, preliminary training was also given to reassure them. Temporal parameters were not recorded since in a previous work [37] velocity did not correlate with accuracy, neither in locomotor nor in virtual conditions. The patients were able to walk in all sessions: when performing the response trials they never stumbled but they could veer slightly. Thus, errors were measured as if the participants had walked in a straight line from the starting location to the goal location. Four space-dependent measures were computed: absolute and signed turn error, and absolute and signed distance error. Turn error corresponds to the difference (in degrees) between the requested turn and the observed turn. Distance error corresponds to the difference (in cm) between the requested distance and the observed distance. Errors were averaged together in tasks involving two response path segments (path reproduction and path reversing). Main analyses of variance (ANOVAs) were conducted on absolute turn and distance errors in order to obtain a good indication of the error amplitude. In both cases they consisted of mixed ANOVAs with group (patients versus controls) as between-participant factor and with task (simple versus complex), condition (PRO-VEST, VIS-VEST, and VIS), session (D 1, D + 7, and D + 30), and side of the path (towards the healthy versus the lesioned side for the patients and right versus left for the controls) as within-participants factors. Turn error was also analyzed using circular statistics [2]. Since circular and linear methods yielded similar results, only the latter are reported here. Finally, signed values are also reported since they state

Fig. 3. Illustrations of representative trajectories of one control (top) and one patient (bottom) tested 1 week (D + 7) after right unilateral vestibular neurotomy for a right exploration path. The trajectories show signed turn and distance errors as a function of task complexity (simple versus complex) and condition (VIS, VIS-VEST, and PRO-VEST). While the trajectories of the patient are close to those of the control in the PRO-VEST condition, the performance is significantly impaired in the VIS-VEST and in the VIS conditions, in particular for the complex tasks.

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

the over- or undershooting of the direction and distance components of the trajectory (see Fig. 3).

3. Results 3.1. Absolute turn error The ANOVA indicated that group constituted a main effect for the variations of the mean turn error [ F(1,12) = 10.96; P < 0.01]. Turn error was significantly higher for patients than for controls (29.7- versus 22.4-). An overall effect of task was evidenced [ F(1,12) = 127.87; P < 0.0001], with higher turn error on complex than on simple tasks (37.3- versus 12.1-). The ANOVA also revealed a main effect of condition [ F(2,24) = 53.08; P < 0.0001]. Planned comparisons revealed that turn error was lower in PRO-VEST (14.2-) than in VIS-VEST (37.6-) [ F(1,12) = 73.45; P < 0.0001] and in VIS conditions (37.3-) [ F(1,12) = 59.52; P < 0.0001]; the error recorded for the last two conditions did not differ significantly [ F(1,12) = 0.29; P < 0.86]. Finally, there was no main effect of session and of side of the path, and no significant interaction between any factors. Detailed analyses contrasting performance between patients and controls are reported on Table 2. Data indicated that spatial performance depended on task complexity since turn error was impaired for patients compared to controls for complex tasks only. Moreover, performance was related to the available sensory informa-

Table 2 Mean (and CI) turn error for patients and controls as a function of task complexity (A), condition (B), and session (C) (A) Patients Controls F(1,12) P

(B) Patients Controls F(1,12) P

(C) Patients Controls F(1,12) P

Simple

Complex

13.14 T 2.10 11.16 T 1.72 1.19 0.29

49.03 T 4.29 31.23 T 3.19 10.56 0.01*

Pro-Vest

Vis-Vest

Vis

15.40 T 2.10 12.53 T 1.62 3.46 0.08

38.88 T 5.70 28.33 T 4.36 7.61 0.02*

38.88 T 5.96 27.65 T 4.18 7.20 0.02*

D

D+7

D + 30

26.86 T 4.87 21.30 T 3.31 4.85 0.05*

29.13 T 5.11 22.44 T 4.05 5.92 0.03*

1

32.31 T 5.16 28.46 T 3.78 2.84 0.12

Local significant differences ( P < 0.05) are marked by *. Turn error was higher in patients than in controls (A) in complex tasks, (B) in VIS-VEST and in VIS conditions, and (C) 1 week and 1 month post-operative (D + 7 and D + 30).

867

tion, with turn error higher for patients than for controls in both the VIS-VEST and VIS conditions while it remained similar for both groups in the blindfolded locomotor (PRO-VEST) condition. Finally, turn error recorded from Menie`re’s patients tested before surgery in the latent phase of their disease did not differ from those of the controls. By contrast, turn error was higher for patients 1 week after UVN and up to the first postoperative month. Fig. 4 gives detailed analyses of turn error computed for each level of task complexity, condition, and session for patients and controls. The results indicate that when performing complex tasks, turn error was higher for patients than for controls 1 week after UVN when both vestibular and visual information was available (VIS-VEST) [ F(1,12) = 5.73; P < 0.03]. Similar results were obtained when only visual cues were available (VIS) [ F(1,12) = 4.86; P < 0.05]. Note that in this condition, even patients tested before neurotomy, in the latent phase of the disease, as well as 1 month after, had poorer performance than controls [ F(1,12) = 16.55; P < 0.001 and F(1,12) = 4.78; P < 0.04, respectively]. On the contrary, turn error in simple tasks never differed between patients and controls. These data suggest that the more complex the task (the higher the level of spatial processing), the higher the error on the orientation component of the spatial representation. 3.2. Absolute distance error The ANOVA on distance error revealed an overall significant effect of group [ F(1,12) = 9.14; P < 0.01]; distance was impaired for patients compared to controls (97.4 cm versus 71.1 cm). There was a significant effect of task [ F(1,12) = 15.47; P < 0.001], with higher distance error on complex than on simple tasks (95.6 cm versus 71.1 cm). ANOVA showed a significant effect of Condition [ F(2,24) = 64.7; P < 0.0001]. Distance error was lower in the PROVEST condition (36 cm) than in both VIS-VEST (94.5 cm) [ F(1,12) = 145.82; P < 0.0001] and VIS (125.7 cm) [ F(1,12) = 74.34; P < 0.0001], and lower in VIS-VEST than in VIS [ F(1,12) = 16.08; P < 0.001]. Finally, ANOVA indicated no main effect of session and of side of the path, and no significant interaction. Detailed analyses contrasting performance between patients and controls are reported in Table 3. Spatial performance depended on task complexity: distance error was higher for patients than for controls in complex tasks and similar for both groups in simple tasks. In addition, distance error was higher for patients than for controls in VIS-VEST and VIS. Finally, distance error was not increased for patients tested before surgery in the latent phase of their disease, while deficits became obvious after UVN (D + 7 and D + 30). Fig. 5 gives detailed analyses of distance error computed for each level of task complexity, condition, and session for

868

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

Fig. 4. Effects of unilateral vestibular loss on turn error. Mean (and CI) absolute turn error (in degrees) for patients and controls as a function of task complexity (simple versus complex tasks), condition (PRO-VEST, VIS-VEST, and VIS), and session (D 1, D + 7, and D + 30). Local significant differences ( P < 0.05) are marked by *.

patients and controls. On complex tasks, distance error was higher for patients than for controls in the VIS-VEST condition [ F(1,12) = 4.98; P < 0.04] 1 week after UVN. Patients’ spatial performance was similar to that of the controls when participants relied on visual cues alone to compute and perform the trajectory. Again, distance error did not differ for patients and controls on simple tasks,

Table 3 Mean (and CI) distance error for patients and controls as a function of task complexity (A), condition (B), and session (C)

(A) Patients Controls F(1,12) P

(B) Patients Controls F(1,12) P

(C) Patients Controls F(1,12) P

Simple

Complex

81.95 T 8.07 64.31 T 7.68 3.61 0.08

109.36 T 8.54 77.92 T 3.70 9.10 0.01*

Pro-Vest

Vis-Vest

Vis

40.89 T 5.23 34.17 T 3.82 2.82 0.12

108.39 T 10.27 80.67 T 8.70 8.09 0.01*

145.91 T 10.18 105.61 T 9.50 4.44 0.05*

D

D+7

D + 30

94.34 T 10.56 67.79 T 7.51 4.43 0.05*

96.21 T 10.67 65.57 T 8.77 6.67 0.02*

1

104.63 T 10.68 84.09 T 9.81 3.16 0.10

Local significant differences ( P < 0.05) are marked by *. Turn error was higher in patients than in controls (A) in complex tasks, (B) in VIS-VEST and in VIS conditions, and (C) 1 week and 1 month post-operative (D + 7 and D + 30).

suggesting that it may depend on the level of spatial processing required for the task. 3.3. Signed turn and distance errors As illustrated in Fig. 3, both groups overshot the direction and undershot the distance. To determine whether unilateral vestibular loss led to symmetrical or asymmetrical direction deficits, detailed analyses based on the percentage of over- and undershooting indicated that the effect of side of the exploration path was significant for patients tested 1 week after UVN (D + 7) in shortcutting. As illustrated in Fig. 6, patients’ performance differed from that of the controls for exploration paths ipsilateral to the operated side in PRO-VEST (v 2 = 64.26, P < 0.001) and VIS-VEST (v 2 = 38.22, P < 0.001), and for exploration paths contralateral to the operated side in VIS (v 2 = 18.54, P < 0.001). In addition, data from the first leg of the reproducing path, which consisted of straight-line locomotion, showed that 1 week after UVN the majority of the patients’ responses were deviated towards the side of the lesion for exploration paths ipsilateral and contralateral to the operated side in PROVEST (85.7% and 57.2%, respectively) as well as in VISVEST (57.2% and 85.7%). On the contrary, VIS condition led to deviations towards the side contralateral to the lesion (85.7% and 57.2%).

4. Discussion This study investigated how vestibular information contributes to spatial representation. Unilateral vestibulardefective patients with Menie`re’s disease were tested before

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

869

Fig. 5. Effects of unilateral vestibular loss on distance error. Mean (and CI) absolute distance error (in cm) for patients and controls as a function of task complexity (simple versus complex tasks), condition (PRO-VEST, VIS-VEST, and VIS), and session (D 1, D + 7, and D + 30). Local significant differences ( P < 0.05) are marked by *.

and after total UVN. Their performance was compared to that of a control population of healthy subjects. To specify the consequences of unilateral vestibular loss on the internal spatial representation, we dissociated the orientation and distance components of the navigational performance, the level of spatial processing (simple versus complex tasks), the role of the different sensory cues, and the side of the exploration path. 4.1. Effect of vestibular lesion on the orientation component The data confirmed that unilateral vestibular loss impairs the orientation component of navigation. Patients tested

after UVN exhibited greater turn error than healthy participants. Moreover, the orientation component was differently impaired depending on task complexity and on the sensory cues available. Direction deficits were restricted to the complex tasks, which required higher levels of spatial processing. Indeed, reproduction of a path, which requires the simplest level of spatial processing probably based on the memory trace of a previously explored route [28], led to the same performance for patients and controls. Inversely, reversing a path and shortcutting, which need more complex processing such as forming and using a survey-type representation, induced higher turn error for patients than for controls. We

Fig. 6. Mean percentage of over- and undershooting of direction (respectively right and left) showing the effect of the side of the path (right versus left for controls and ipsilateral versus contralateral for patients) in Session 2 (D + 7) for shortcutting, as a function of condition (VIS, VIS-VEST, and PRO-VEST). Local significant differences ( P < 0.05) are marked by *.

870

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

emphasize that the more complex the task, the higher the weight of vestibular cues in building up an accurate internal spatial representation. However, the participants may have noticed that all the stimulus trajectories were the same and attempted to produce the same response, which would have increased their performance. Thus, it is possible that the use of a greater variety of stimulus trajectories would have exhibited deficits even in the simple tasks. Turn error was similar for patients and controls when proprioceptive and vestibular information resulting from locomotor activity was available (PRO-VEST condition). Error was higher for patients than for controls when visual and vestibular cues were available (VIS-VEST condition) 1 week after UVN. Finally, the performance of the patients was worse when visual cues alone were available (VIS condition) since the orientation component was impaired up to 1 month post-lesion and even before UVN. These data indicate that the deficit is inversely correlated with the available, egocentric (proprioceptive and vestibular) information. That the orientation component is impaired after vestibular lesion agrees with the results for passive turns [33,44] as well as active turns [19]. Interestingly, the lack of orientation deficits in patients performing path integration from proprioceptive information during active blindfolded locomotion (PRO-VEST condition) raises the question of the functional role of the vestibular inputs during active displacements. In our opinion, since performance was impaired in the other conditions, these data point out the strong role of the proprioceptive cues that compensate for vestibular loss during active locomotion. In addition, this impairment means that posturo-locomotor deficits resulting from vestibular loss had a poor effect on the global spatial performance. These results differ from those in our previous study [37] in which orientation deficits were also observed in locomotor navigation. In the present study it seems that right angles and half-turns are coded more easily than the in-between angles used in the study by Pe´ruch et al. [37]. On the contrary, visual navigation was more complex, which would account for the greater spatial deficits. Indeed, when visual cues alone were available, impairments were observed before and after UVN up to the first post-operative month in the present study, while these were restricted to the first week after UVN in our previous study. Contrary to our hypothesis, turn errors were higher when there was no variation in the vestibular stimulation, that is, in the VIS condition. This finding suggests that all the sensory cues are necessary to build up an accurate mental representation. Put differently, when one sensory cue is impaired, the environment may be experienced in a different way, and a different mental representation may be constructed. Multisensory integration of internal and external cues seem necessary to perform navigation tasks that require an internal spatial representation. Apparently, having no labyrinth on one side is not the same as having a functioning

labyrinth that is not currently registering accelerations; removing a cue (by removing the labyrinth) is not the same thing perceptually as holding a cue constant (by holding the head stationary in healthy participants). This notion highlights the importance, in healthy individuals, of vestibular information signaling that the head is stationary. Last, the results argue against a visual substitution process in vestibular compensation [27,42] when applied to the case of cognitive processing. A point of interest is that patients’ turn error did not significantly differ for ipsilateral and contralateral turns relative to the side of the lesion. That vestibular inputs from only one labyrinth do not mediate asymmetric (ipsi- or contralateral) spatial representation is supported by neuroanatomic data showing bilateral vestibular projections from the vestibular nuclei to the parietal and temporal cortex [10]. However, detailed analysis of the signed turn error showed significant differences between patients and controls for shortcutting 1 week after UVN only. Patients rotated significantly more towards the lesioned side in the PROVEST condition. The results concur with those of von Brevern et al. [44], who highlighted an asymmetrical perception of space orientation during perceptual estimation of self-rotation for patients seated on a rotating chair in darkness. As a rule, both patients and controls tended to overshoot the rotation. These data partially agree with those recorded during active displacement requiring vestibulo-proprioceptive perception of motion in nonvisual navigation [28], since participants overshot turns of amplitude lower than 120- and undershot turns of 180- and more. Similar results were found for the perception of active angular displacement in the horizontal plane [31], and under different combinations of visual, vestibular, and kinesthetic information [1]. 4.2. Effect of vestibular lesion on the distance component Unilateral vestibular loss impaired the distance component of the internal spatial representation, although to a lesser extent than for the orientation component. Indeed, distance impairment was evidenced in the VIS-VEST condition acutely after UVN. Distance error also depended on the level of spatial processing required to perform the task since it was higher for patients than for controls in the complex tasks only. To our knowledge, these data provide one of the first descriptions of impaired distance estimation after vestibular loss. But why has impaired distance estimation not been described before? The main reason might be that distance assessment did not require a high level of spatial processing. Indeed, in tasks where labyrinthine-defective participants were required to walk a previously seen triangular path, directional but not distance errors were reported [19]. The effects of unilateral vestibular loss on distance do not depend on the side (ipsi- or contralateral) of the exploration

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

path. As concerns straight-line locomotion (first leg of the reproduction path), 1 week after UVN most patients deviated towards the lesioned side during active blindfolded locomotion (PRO-VEST condition). Typically, such deviations are symptomatic of asymmetric vestibular inputs [14]. Such an asymmetrical perception of self-motion in darkness with a locomotion trajectory deviated towards the side ipsilateral to the lesion has been reported for vestibulardefective patients after acute unilateral acoustic neuroma resection [13] and during the chronic stage after vestibular loss [9]. In addition, the present data indicate that when only visual cues were available (VIS condition) patients deviated towards the side contralateral to the lesion. These data corroborate those described for the same type of patients in goal-directed locomotion [8]. Finally, both patients and controls tended to undershoot the distance, with patients undershooting more than controls. Undershoot of distances from 6 m onwards has been reported by Berthoz et al. [4] and Marlinsky [30] for control subjects after passive linear transportation. In a study on linear horizontal displacements along the interaural axis in darkness, subject’s displacement estimation was highly related to the linear acceleration intensity [7] sensed by the otolith system. Since converging inputs from the two vestibular labyrinths are essential in shaping the response sensitivity of otolith-related central vestibular neurons [11], the higher undershooting of distance for patients after UVN could result from the missing vestibular inputs from one side. Spatial performance of Me´nie`re’s patients after UVN shows perturbations of both the direction and the distance components. However, contrary to [25,28,32,46], which found a direct proportionality between linear and angular errors, such perturbations were not linked in a proportional way in our study. An opposite theory defended by Berthoz et al. [5] suggested that direction and distance components were processed by separate mechanisms. Since the present data point to some discrepancies between direction and distance errors, they can be taken as an argument in support of this theory. In summary, we conclude that vestibular information participates in spatial knowledge at a high sensory integration level and that the environment experienced by the patients is different after UVN. That vestibular information is necessary to elaborate an accurate internal spatial representation is highlighted by the higher deficits in direction and distance for complex tasks, that is, for tasks requiring the highest level of spatial processing. Spatial representation was differentially impaired according to the available sensory cues. Deficits were absent in active locomotor blindfolded condition, appeared in conditions involving visual and vestibular information, and were maximal when visual cues alone were available. Finally, our data indicate that asymmetrical vestibular peripheral loss results in global impairment of the internal spatial representation.

871

Acknowledgments This study was supported by grants from CNRS and Ministe` re de´ le´ gue´ a` la Recherche et aux Nouvelles Technologies (UMR 6149), from INSERM (EMI-U 9926), and from IFR 131 ‘‘Sciences du Cerveau et de la Cognition’’. We thank patients and controls who participated in the experiments, Aileen McGonigal for making editing suggestions, and anonymous reviewers for providing helpful comments.

References [1] N.H. Bakker, P.J. Werkhoven, P.O. Passenier, The effects of proprioceptive and visual feedback on geographical orientation in virtual environments, Presence 8 (1999) 36 – 53. [2] E. Batschelet, Circular Statistics in Biology, Academic Press, New York, 1981. [3] J.S. Beritoff, Neural mechanisms of higher vertebrates behavior, in: W.T. Liberson (Ed.), Trans. and Ed., Little, Brown, and Co, Boston, 1965. [4] A. Berthoz, I. Israe¨l, P. Georges-Franc¸ois, R. Grasso, T. Tzuzuku, Spatial memory of body linear displacement: what is being stored? Science 269 (1995) 95 – 98. [5] A. Berthoz, M.A. Amorim, S. Glasauer, R. Grasso, Y. Takei, I. ViaudDelmon, Dissociation between distance and direction during locomotor navigation, in: R.G. Golledge (Ed.), Wayfinding Behavior. Cognitive Mapping and other Spatial Processes, Johns Hopkins, Baltimore, 1999, pp. 328 – 348. [6] J. Bloomberg, G. Melvill Jones, B.N. Segal, S. McFarlane, J. Soul, Vestibular-contingent voluntary saccades based on cognitive estimate of remembered vestibular information, Adv. Oto-Rhino-Laryngol. 41 (1988) 71 – 75. [7] L. Borel, B. Le Goff, O. Charade, A. Berthoz, Gaze strategies during linear motion in head free humans, J. Neurophysiol. 72 (1994) 2451 – 2466. [8] L. Borel, F. Harlay, C. Lopez, J. Magnan, A. Chays, M. Lacour, Walking performance of vestibular-defective patients before and after unilateral vestibular neurotomy, Behav. Brain Res. 150 (2004) 191 – 200. [9] T. Brandt, Vestibulopathic gait. Walking and running, in: E. Ruzicka, M. Hallett, J. Jankovic (Eds.), Gait Disorders. Advances in Neurology, Lippincott, Williams and Wilkins, Philadelphia, 2001, pp. 165 – 172. [10] T. Brandt, M. Dieterich, The vestibular cortex. Its localisations, functions and disorders, Ann. N. Y. Acad. Sci. 871 (1999) 293 – 312. [11] Y.S. Chan, C.H. Lai, D.K.Y. Shum, Bilateral otolith contribution to spatial coding in the vestibular system, J. Biomed. Sci. 9 (2002) 574 – 586. [12] S.S. Chance, F. Gaunet, A.C. Beall, J.M. Loomis, Locomotion mode affects the updating of objects encountered during travel: the contribution of vestibular and proprioceptive inputs to path integration, Presence 7 (1998) 168 – 178. [13] H.S. Cohen, Vestibular disorders and impaired path integration along a linear trajectory, J. Vestib. Res. 10 (2000) 7 – 15. [14] I.S. Curthoys, G.M. Halmagyi, Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss, J. Vestib. Res. 5 (1995) 67 – 107. [15] C.R. Gallistel, The Organization of Learning, MIT Press, Cambridge, MA, 1990. [16] J.J. Gibson, The Senses Considered as a Perceptual System, Houghton Mifflin, Boston, MA, 1966. [17] J.J. Gibson, The Ecological Approach to Visual Perception, Houghton Mifflin, Boston, MA, 1979.

872

P. Pe´ruch et al. / Cognitive Brain Research 25 (2005) 862 – 872

[18] S. Glasauer, M.A. Amorim, E. Vitte, A. Berthoz, Goal-directed linear locomotion in normal and labyrinthine-defective subjects, Exp. Brain Res. 98 (1994) 323 – 335. [19] S. Glasauer, M.A. Amorim, I. Viaud-Delmon, A. Berthoz, Differential effects of labyrinthine dysfunction on distance and direction during blindfolded walking of a triangular path, Exp. Brain Res. 145 (2002) 489 – 497. [20] R.G. Golledge, Environmental cognition, in: D. Stokols, I. Altman (Eds.), Handbook of Environmental Psychology, vol. 1, Wiley, New York, 1987, pp. 131 – 174. [21] F.E. Guedry, Psychophysics of vestibular sensation, in: H.H. Kornhuber (Ed.), Handbook of Sensory Physiology, Vestibular System: Part 2. Psychophysics, Applied Aspects and General Interpretations, vol. VI/2, Springer, Berlin, 1974, pp. 3 – 154. [22] I. Israe¨l, A. Berthoz, Contribution of the otoliths to the calculation of linear displacement, J. Neurophysiol. 62 (1989) 247 – 263. [23] I. Israe¨l, N. Chapuis, S. Glasauer, O. Charade, A. Berthoz, Estimation of passive horizontal linear whole-body displacements in humans, J. Neurophysiol. 70 (1993) 1271 – 1273. [24] M.J. Kearns, W.H. Warren, A.P. Duchon, M.J. Tarr, Path integration from optic flow and body senses in a homing task, Perception 31 (2002) 349 – 374. [25] R.L. Klatzky, J.M. Loomis, R.G. Golledge, J.G. Cicinelli, S. Doherty, J.W. Pellegrino, Acquisition of route and survey knowledge in the absence of vision, J. Mot. Behav. 22 (1990) 19 – 43. [26] R.L. Klatzky, J.M. Loomis, R.G. Golledge, Encoding spatial representations through nonvisually guided locomotion: tests of human path integration, in: D. Medin (Ed.), The Psychology of Learning and Motivation, Academic Press, San Diego, 1997, pp. 41 – 84. [27] M. Lacour, Restoration of nerve function: models and concepts, in: M. Lacour, M. Toupet, P. Denise, Y. Christen (Eds.), Vestibular Compensation: Facts, Theories and Clinical Perspectives, Elsevier, Paris, 1989, pp. 11 – 34. [28] J.M. Loomis, R.L. Klatzky, R.G. Golledge, J.G. Cicinelli, J.W. Pellegrino, P.A. Fry, Nonvisual navigation by blind and sighted: assessment of path integration ability, J. Exp. Psychol. Gen. 122 (1993) 73 – 91. [29] J. Magnan, Vestibular neurotomy by the retrosigmoid approach, in: O. Sterkers, E. Ferrary, R. Dauman, J.P. Sauvage, P. Tran Ba Huy (Eds.), Menie`re’s Disease. Update, The Hague, Kugler, 2000, pp. 793 – 797. [30] V.V. Marlinsky, Vestibular and vestibulo-proprioceptive perception of motion in the horizontal plane in blindfolded man-I. Estimations of linear displacement, Neuroscience 90 (1999) 389 – 394. [31] V.V. Marlinsky, Vestibular and vestibulo-proprioceptive perception of motion in the horizontal plane in blindfolded man-II. Estimations

[32]

[33]

[34] [35]

[36] [37]

[38]

[39]

[40]

[41] [42]

[43] [44]

[45]

[46]

of rotations about the earth-vertical axis, Neuroscience 90 (1999) 395 – 401. V.V. Marlinsky, Vestibular and vestibulo-proprioceptive perception of motion in the horizontal plane in blindfolded man-III. Route inference, Neuroscience 90 (1999) 403 – 411. T. Metcalfe, M. Gresty, Self controlled reorienting movements in response to rotational displacements in normal subjects and patients with labyrinthine diseases, in: D.L. Tomko, B. Cohen, F.E. Guedry (Eds.), Sensing Motion, Annals of the Academy of Sciences, New York, 1992, pp. 695 – 698. H. Mittelstaedt, S. Glasauer, Idiothetic navigation in gerbil and humans, Zool. Jahrb. Physiol. 95 (1991) 427 – 435. H. Mittelstaedt, M.L. Mittelstaedt, Homing by path integration, in: F. Papi, H.G. Wallraff (Eds.), Avian Navigation, Springer, New York, 1982, pp. 290 – 297. P. Pe´ruch, M. May, F. Wartenberg, Homing in virtual environments: effects of field of view and path layout, Perception 26 (1997) 301 – 311. P. Pe´ruch, L. Borel, F. Gaunet, C. Thinus-Blanc, J. Magnan, M. Lacour, Spatial performance of unilateral vestibular defective patients in nonvisual versus visual navigation, J. Vestib. Res. 9 (1999) 37 – 47. M. Potegal, Vestibular and neostriatal contributions to spatial orientation, in: M. Potegal (Ed.), Spatial Abilities. Development and Physiological Foundations, Academic Press, London, 1982, pp. 361 – 387. B. Riecke, H.A.H.C. van Veen, H.H. Bu¨lthoff, Visual homing is possible without landmarks: a path integration study in virtual reality, Presence 11 (2002) 443 – 473. J.J. Rieser, Access to knowledge of spatial structure at novel points of observation, J. Exper. Psychol., Learn., Mem., Cogn. 15 (1989) 1157 – 1165. J.J. Rieser, A.E. Garing, Spatial orientation, Encyclop. Hum. Behav. 14 (1994) 287 – 295. P.F. Smith, C.L. Darlington, I.S. Curthoys, The effect of visual deprivation on vestibular compensation in the guinea pig, Brain Res. 364 (1986) 195 – 198. J.A. Thomson, How do we use visual information to control locomotion? Trends Neurosci. 3 (1980) 247 – 250. M. von Brevern, M.E. Faldon, G.B. Brookes, M.A. Gresty, Evaluating 3D semicircular canal function by perception of rotation, Am. J. Otol. 18 (1997) 484 – 493. W.H. Warren, M.W. Morris, M. Kalish, Perception of translational heading from optical flow, J. Exp. Psychol. Hum. Percept. Perform. 14 (1988) 646 – 660. P. Worchel, The role of vestibular organs in spatial orientation, J. Exp. Psychol. 44 (1952) 4 – 10.