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Unilateral vestibular loss impairs external space representation.

Borel L, Redon-Zouiteni C, Cauvin P, Dumitrescu M, Devèze A, Magnan J, Péruch P - PLoS ONE (2014)

Bottom Line: These individuals were also required to estimate their body pointing direction.Performance varied according to the time elapsed after neurotomy: deficits were stronger during the early stages, while gradual compensation occurred subsequently.These findings provide the first demonstration of the critical role of vestibular signals in the representation of external space and of body pointing direction in the early stages after unilateral vestibular loss.

View Article: PubMed Central - PubMed

Affiliation: Aix-Marseille Université, Marseille, France ; CNRS, UMR 7260 Laboratoire de Neurosciences Intégratives et Adaptatives, Marseille, France.

ABSTRACT
The vestibular system is responsible for a wide range of postural and oculomotor functions and maintains an internal, updated representation of the position and movement of the head in space. In this study, we assessed whether unilateral vestibular loss affects external space representation. Patients with Menière's disease and healthy participants were instructed to point to memorized targets in near (peripersonal) and far (extrapersonal) spaces in the absence or presence of a visual background. These individuals were also required to estimate their body pointing direction. Menière's disease patients were tested before unilateral vestibular neurotomy and during the recovery period (one week and one month after the operation), and healthy participants were tested at similar times. Unilateral vestibular loss impaired the representation of both the external space and the body pointing direction: in the dark, the configuration of perceived targets was shifted toward the lesioned side and compressed toward the contralesioned hemifield, with higher pointing error in the near space. Performance varied according to the time elapsed after neurotomy: deficits were stronger during the early stages, while gradual compensation occurred subsequently. These findings provide the first demonstration of the critical role of vestibular signals in the representation of external space and of body pointing direction in the early stages after unilateral vestibular loss.

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Related in: MedlinePlus

Effect of unilateral vestibular loss on pointing error in darkness.Average left-right (top) and fore-aft (bottom) pointing error for each group of participants in the near (black) and far (gray) spaces. Three sessions were plotted for the patients, while only the average values were plotted for the controls because the performances of these individuals remained consistent throughout the three sessions. Mean (±95% CI).
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pone-0088576-g002: Effect of unilateral vestibular loss on pointing error in darkness.Average left-right (top) and fore-aft (bottom) pointing error for each group of participants in the near (black) and far (gray) spaces. Three sessions were plotted for the patients, while only the average values were plotted for the controls because the performances of these individuals remained consistent throughout the three sessions. Mean (±95% CI).

Mentions: Significant effects of Group (F1,24 = 12.28; p<0.01) and Session (F2,48 = 20.15; p<0.001) were found for the pointing error in the left-right direction. The pointing error was significantly higher for patients than for healthy participants. A significant interaction between Group and Session (F2,48 = 18.08; p<0.001) showed that the pointing error differed over time more in patients than in healthy participants. Planned comparisons revealed that the effect of Session was obvious only for the patients (F1,12 = 12.26; p<0.01), indicating a drastic impairment in target location after unilateral vestibular loss. An overall effect of Space was also found (F1,24 = 11.17; p<0.01), with a higher pointing error observed in the near space than in the far space. A major effect of Condition (F1,24 = 14.83; p<0.001) and significant effects of the Group x Condition interaction (F1,24 = 14.88; p<0.001) and the Group x Space x Condition interaction (F1,24 = 4.68; p<0.05) were observed, indicating that the pointing error was differentially affected in patients and healthy participants as a function of space and condition (Table 2). To specify these data, planned comparisons were conducted separately on near and far spaces. Figure 2 (top) illustrates the pointing error in the left-right direction for the two groups of participants as a function of space in the dark. The pointing error significantly differed between patients and healthy participants for near (F1,24 = 13.12; p<0.01) and far (F1,24 = 9.62; p<0.01) spaces. The difference between the groups was obvious during the early stages following unilateral vestibular loss at D+7 for the near (p<0.001) and far (p<0.001) spaces; mean lateral deviations toward the operated side of 3.4±0.8° (Mean±CI) and 2.6±0.5° relative to the target location in the near and far spaces, respectively, were observed for patients, and deviations of 0.1±0.1° and 0.1±0.1° were observed in the healthy group. For patients, the pointing error regained preoperative values at D+30. Under light conditions, the mean pointing error was less than that observed in darkness. At D+7, only a slight difference was reported between patients (0.4±0.5°) and healthy participants (0.1±0.1°) for the near space (p<0.01).


Unilateral vestibular loss impairs external space representation.

Borel L, Redon-Zouiteni C, Cauvin P, Dumitrescu M, Devèze A, Magnan J, Péruch P - PLoS ONE (2014)

Effect of unilateral vestibular loss on pointing error in darkness.Average left-right (top) and fore-aft (bottom) pointing error for each group of participants in the near (black) and far (gray) spaces. Three sessions were plotted for the patients, while only the average values were plotted for the controls because the performances of these individuals remained consistent throughout the three sessions. Mean (±95% CI).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3921214&req=5

pone-0088576-g002: Effect of unilateral vestibular loss on pointing error in darkness.Average left-right (top) and fore-aft (bottom) pointing error for each group of participants in the near (black) and far (gray) spaces. Three sessions were plotted for the patients, while only the average values were plotted for the controls because the performances of these individuals remained consistent throughout the three sessions. Mean (±95% CI).
Mentions: Significant effects of Group (F1,24 = 12.28; p<0.01) and Session (F2,48 = 20.15; p<0.001) were found for the pointing error in the left-right direction. The pointing error was significantly higher for patients than for healthy participants. A significant interaction between Group and Session (F2,48 = 18.08; p<0.001) showed that the pointing error differed over time more in patients than in healthy participants. Planned comparisons revealed that the effect of Session was obvious only for the patients (F1,12 = 12.26; p<0.01), indicating a drastic impairment in target location after unilateral vestibular loss. An overall effect of Space was also found (F1,24 = 11.17; p<0.01), with a higher pointing error observed in the near space than in the far space. A major effect of Condition (F1,24 = 14.83; p<0.001) and significant effects of the Group x Condition interaction (F1,24 = 14.88; p<0.001) and the Group x Space x Condition interaction (F1,24 = 4.68; p<0.05) were observed, indicating that the pointing error was differentially affected in patients and healthy participants as a function of space and condition (Table 2). To specify these data, planned comparisons were conducted separately on near and far spaces. Figure 2 (top) illustrates the pointing error in the left-right direction for the two groups of participants as a function of space in the dark. The pointing error significantly differed between patients and healthy participants for near (F1,24 = 13.12; p<0.01) and far (F1,24 = 9.62; p<0.01) spaces. The difference between the groups was obvious during the early stages following unilateral vestibular loss at D+7 for the near (p<0.001) and far (p<0.001) spaces; mean lateral deviations toward the operated side of 3.4±0.8° (Mean±CI) and 2.6±0.5° relative to the target location in the near and far spaces, respectively, were observed for patients, and deviations of 0.1±0.1° and 0.1±0.1° were observed in the healthy group. For patients, the pointing error regained preoperative values at D+30. Under light conditions, the mean pointing error was less than that observed in darkness. At D+7, only a slight difference was reported between patients (0.4±0.5°) and healthy participants (0.1±0.1°) for the near space (p<0.01).

Bottom Line: These individuals were also required to estimate their body pointing direction.Performance varied according to the time elapsed after neurotomy: deficits were stronger during the early stages, while gradual compensation occurred subsequently.These findings provide the first demonstration of the critical role of vestibular signals in the representation of external space and of body pointing direction in the early stages after unilateral vestibular loss.

View Article: PubMed Central - PubMed

Affiliation: Aix-Marseille Université, Marseille, France ; CNRS, UMR 7260 Laboratoire de Neurosciences Intégratives et Adaptatives, Marseille, France.

ABSTRACT
The vestibular system is responsible for a wide range of postural and oculomotor functions and maintains an internal, updated representation of the position and movement of the head in space. In this study, we assessed whether unilateral vestibular loss affects external space representation. Patients with Menière's disease and healthy participants were instructed to point to memorized targets in near (peripersonal) and far (extrapersonal) spaces in the absence or presence of a visual background. These individuals were also required to estimate their body pointing direction. Menière's disease patients were tested before unilateral vestibular neurotomy and during the recovery period (one week and one month after the operation), and healthy participants were tested at similar times. Unilateral vestibular loss impaired the representation of both the external space and the body pointing direction: in the dark, the configuration of perceived targets was shifted toward the lesioned side and compressed toward the contralesioned hemifield, with higher pointing error in the near space. Performance varied according to the time elapsed after neurotomy: deficits were stronger during the early stages, while gradual compensation occurred subsequently. These findings provide the first demonstration of the critical role of vestibular signals in the representation of external space and of body pointing direction in the early stages after unilateral vestibular loss.

Show MeSH
Related in: MedlinePlus