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The disturbance of gaze in progressive supranuclear palsy: implications for pathogenesis.

Chen AL, Riley DE, King SA, Joshi AC, Serra A, Liao K, Cohen ML, Otero-Millan J, Martinez-Conde S, Strupp M, Leigh RJ - Front Neurol (2010)

Bottom Line: These vertical and vergence eye movements habitually work in concert to enable visuomotor skills that are important during locomotion with the hands free.Taken with the prominent early feature of falls, these findings suggest that PSP tauopathy impairs a recently evolved neural system concerned with bipedal locomotion in an erect posture and frequent gaze shifts between the distant environment and proximate hands.This approach provides a conceptual framework that can be used to address the nosological challenge posed by overlapping clinical and neuropathological features of neurodegenerative tauopathies.

View Article: PubMed Central - PubMed

Affiliation: Veterans Affairs Medical Center, University Hospitals Case Medical Center Cleveland, OH, USA.

ABSTRACT
Progressive supranuclear palsy (PSP) is a disease of later life that is currently regarded as a form of neurodegenerative tauopathy. Disturbance of gaze is a cardinal clinical feature of PSP that often helps clinicians to establish the diagnosis. Since the neurobiology of gaze control is now well understood, it is possible to use eye movements as investigational tools to understand aspects of the pathogenesis of PSP. In this review, we summarize each disorder of gaze control that occurs in PSP, drawing on our studies of 50 patients, and on reports from other laboratories that have measured the disturbances of eye movements. When these gaze disorders are approached by considering each functional class of eye movements and its neurobiological basis, a distinct pattern of eye movement deficits emerges that provides insight into the pathogenesis of PSP. Although some aspects of all forms of eye movements are affected in PSP, the predominant defects concern vertical saccades (slow and hypometric, both up and down), impaired vergence, and inability to modulate the linear vestibulo-ocular reflex appropriately for viewing distance. These vertical and vergence eye movements habitually work in concert to enable visuomotor skills that are important during locomotion with the hands free. Taken with the prominent early feature of falls, these findings suggest that PSP tauopathy impairs a recently evolved neural system concerned with bipedal locomotion in an erect posture and frequent gaze shifts between the distant environment and proximate hands. This approach provides a conceptual framework that can be used to address the nosological challenge posed by overlapping clinical and neuropathological features of neurodegenerative tauopathies.

No MeSH data available.


Related in: MedlinePlus

Comparison of the vertical linear or translational (bob) vestibulo-ocular reflex (tVOR) in the top panels and the horizontal angular (yaw) vestibulo-ocular reflex (aVOR) in the lower panels from a normal elderly subject (A,B,E,F) and a patient with PSP (C,D,G,H). When the normal subject viewed the far target (A), vertical eye movements (red line) due to tVOR were appropriately small; during near viewing (B), when the subject converged (blue line), they increase, although not as much as would be required to hold the foveal line of sight on the visual target (black dotted line). When the PSP patient subject viewed the far target (C), vertical eye movements due to tVOR were small; during near viewing (D), the patient neither converged nor increased the tVOR response. The normal subject shows near-perfect aVOR during far viewing (E); during near viewing (F), the magnitude of the response increases by about 24%, although not as much as needed for ideal viewing. The PSP patient also shows a near-perfect aVOR during far viewing (G); however, during near viewing (H) there is no measurable increase of the response, as is required by geometric factors (see text). Note that positive values indicate downward, leftward or divergence movements in this figure; different records have been offset to aid clarity except for vergence. The angle of vergence achieved in each of the lower panels corresponds to that in the panel above. The inset in the lower right corner of the upper panel summarizes the geometric relationship between viewing distance (D), amplitude of head translation (A), and the angle of eye rotation (θ) required to hold the foveal line of sight on the target.
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Figure 6: Comparison of the vertical linear or translational (bob) vestibulo-ocular reflex (tVOR) in the top panels and the horizontal angular (yaw) vestibulo-ocular reflex (aVOR) in the lower panels from a normal elderly subject (A,B,E,F) and a patient with PSP (C,D,G,H). When the normal subject viewed the far target (A), vertical eye movements (red line) due to tVOR were appropriately small; during near viewing (B), when the subject converged (blue line), they increase, although not as much as would be required to hold the foveal line of sight on the visual target (black dotted line). When the PSP patient subject viewed the far target (C), vertical eye movements due to tVOR were small; during near viewing (D), the patient neither converged nor increased the tVOR response. The normal subject shows near-perfect aVOR during far viewing (E); during near viewing (F), the magnitude of the response increases by about 24%, although not as much as needed for ideal viewing. The PSP patient also shows a near-perfect aVOR during far viewing (G); however, during near viewing (H) there is no measurable increase of the response, as is required by geometric factors (see text). Note that positive values indicate downward, leftward or divergence movements in this figure; different records have been offset to aid clarity except for vergence. The angle of vergence achieved in each of the lower panels corresponds to that in the panel above. The inset in the lower right corner of the upper panel summarizes the geometric relationship between viewing distance (D), amplitude of head translation (A), and the angle of eye rotation (θ) required to hold the foveal line of sight on the target.

Mentions: The angular and linear vestibulo-ocular reflexes (VORs) are important for clear vision during locomotion. The angular VOR generates eye movements at short-latency (<15 ms) to compensate for rotational head perturbations (Maas et al., 1989). The angular VOR depends on the semicircular canals of the vestibular labyrinth, which act as angular accelerometers (Leigh and Zee, 2006). During near viewing, since the eyes lie anterior to the axis of head rotation, larger eye rotations are required to hold the eye on target – by as much as 30% if the target is very near (Viirre et al., 1986). The translational or linear VOR compensates for linear head movements by generating eye movements that are highly dependent on the subject's viewing distance (Liao et al., 2008b). The linear VOR depends on the otolithic organs of the vestibular labyrinth, which sense linear accelerations including gravity (Leigh and Zee, 2006). During far viewing, geometry dictates that no eye movements at all are necessary to hold images steady on the retina during head translations. However, during viewing of a near target, large eye movements may be necessary to keep the subject's foveal line of sight pointed at a target (see inset on upper panel of Figure 6). Thus, the modulation of the linear VOR by viewing distance is much greater than for the angular VOR. Another important behavioral difference is that whereas the angular VOR usually generates eye movements that hold the line of sight on the target (i.e., the eye movements compensate for head rotations – even when viewing optical infinity), the linear VOR does not (Liao et al., 2008b). These important differences are demonstrated in Figure 6. Studies suggest that the eye movements generated by the linear VOR during viewing of a near target are more suitable for minimizing relative motion between the near target and the distant background (Liao et al., 2008b). This strategy may have evolved to optimize motion parallax, which is used to determine the relative distances of objects as the subject walks through the environment.


The disturbance of gaze in progressive supranuclear palsy: implications for pathogenesis.

Chen AL, Riley DE, King SA, Joshi AC, Serra A, Liao K, Cohen ML, Otero-Millan J, Martinez-Conde S, Strupp M, Leigh RJ - Front Neurol (2010)

Comparison of the vertical linear or translational (bob) vestibulo-ocular reflex (tVOR) in the top panels and the horizontal angular (yaw) vestibulo-ocular reflex (aVOR) in the lower panels from a normal elderly subject (A,B,E,F) and a patient with PSP (C,D,G,H). When the normal subject viewed the far target (A), vertical eye movements (red line) due to tVOR were appropriately small; during near viewing (B), when the subject converged (blue line), they increase, although not as much as would be required to hold the foveal line of sight on the visual target (black dotted line). When the PSP patient subject viewed the far target (C), vertical eye movements due to tVOR were small; during near viewing (D), the patient neither converged nor increased the tVOR response. The normal subject shows near-perfect aVOR during far viewing (E); during near viewing (F), the magnitude of the response increases by about 24%, although not as much as needed for ideal viewing. The PSP patient also shows a near-perfect aVOR during far viewing (G); however, during near viewing (H) there is no measurable increase of the response, as is required by geometric factors (see text). Note that positive values indicate downward, leftward or divergence movements in this figure; different records have been offset to aid clarity except for vergence. The angle of vergence achieved in each of the lower panels corresponds to that in the panel above. The inset in the lower right corner of the upper panel summarizes the geometric relationship between viewing distance (D), amplitude of head translation (A), and the angle of eye rotation (θ) required to hold the foveal line of sight on the target.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3008928&req=5

Figure 6: Comparison of the vertical linear or translational (bob) vestibulo-ocular reflex (tVOR) in the top panels and the horizontal angular (yaw) vestibulo-ocular reflex (aVOR) in the lower panels from a normal elderly subject (A,B,E,F) and a patient with PSP (C,D,G,H). When the normal subject viewed the far target (A), vertical eye movements (red line) due to tVOR were appropriately small; during near viewing (B), when the subject converged (blue line), they increase, although not as much as would be required to hold the foveal line of sight on the visual target (black dotted line). When the PSP patient subject viewed the far target (C), vertical eye movements due to tVOR were small; during near viewing (D), the patient neither converged nor increased the tVOR response. The normal subject shows near-perfect aVOR during far viewing (E); during near viewing (F), the magnitude of the response increases by about 24%, although not as much as needed for ideal viewing. The PSP patient also shows a near-perfect aVOR during far viewing (G); however, during near viewing (H) there is no measurable increase of the response, as is required by geometric factors (see text). Note that positive values indicate downward, leftward or divergence movements in this figure; different records have been offset to aid clarity except for vergence. The angle of vergence achieved in each of the lower panels corresponds to that in the panel above. The inset in the lower right corner of the upper panel summarizes the geometric relationship between viewing distance (D), amplitude of head translation (A), and the angle of eye rotation (θ) required to hold the foveal line of sight on the target.
Mentions: The angular and linear vestibulo-ocular reflexes (VORs) are important for clear vision during locomotion. The angular VOR generates eye movements at short-latency (<15 ms) to compensate for rotational head perturbations (Maas et al., 1989). The angular VOR depends on the semicircular canals of the vestibular labyrinth, which act as angular accelerometers (Leigh and Zee, 2006). During near viewing, since the eyes lie anterior to the axis of head rotation, larger eye rotations are required to hold the eye on target – by as much as 30% if the target is very near (Viirre et al., 1986). The translational or linear VOR compensates for linear head movements by generating eye movements that are highly dependent on the subject's viewing distance (Liao et al., 2008b). The linear VOR depends on the otolithic organs of the vestibular labyrinth, which sense linear accelerations including gravity (Leigh and Zee, 2006). During far viewing, geometry dictates that no eye movements at all are necessary to hold images steady on the retina during head translations. However, during viewing of a near target, large eye movements may be necessary to keep the subject's foveal line of sight pointed at a target (see inset on upper panel of Figure 6). Thus, the modulation of the linear VOR by viewing distance is much greater than for the angular VOR. Another important behavioral difference is that whereas the angular VOR usually generates eye movements that hold the line of sight on the target (i.e., the eye movements compensate for head rotations – even when viewing optical infinity), the linear VOR does not (Liao et al., 2008b). These important differences are demonstrated in Figure 6. Studies suggest that the eye movements generated by the linear VOR during viewing of a near target are more suitable for minimizing relative motion between the near target and the distant background (Liao et al., 2008b). This strategy may have evolved to optimize motion parallax, which is used to determine the relative distances of objects as the subject walks through the environment.

Bottom Line: These vertical and vergence eye movements habitually work in concert to enable visuomotor skills that are important during locomotion with the hands free.Taken with the prominent early feature of falls, these findings suggest that PSP tauopathy impairs a recently evolved neural system concerned with bipedal locomotion in an erect posture and frequent gaze shifts between the distant environment and proximate hands.This approach provides a conceptual framework that can be used to address the nosological challenge posed by overlapping clinical and neuropathological features of neurodegenerative tauopathies.

View Article: PubMed Central - PubMed

Affiliation: Veterans Affairs Medical Center, University Hospitals Case Medical Center Cleveland, OH, USA.

ABSTRACT
Progressive supranuclear palsy (PSP) is a disease of later life that is currently regarded as a form of neurodegenerative tauopathy. Disturbance of gaze is a cardinal clinical feature of PSP that often helps clinicians to establish the diagnosis. Since the neurobiology of gaze control is now well understood, it is possible to use eye movements as investigational tools to understand aspects of the pathogenesis of PSP. In this review, we summarize each disorder of gaze control that occurs in PSP, drawing on our studies of 50 patients, and on reports from other laboratories that have measured the disturbances of eye movements. When these gaze disorders are approached by considering each functional class of eye movements and its neurobiological basis, a distinct pattern of eye movement deficits emerges that provides insight into the pathogenesis of PSP. Although some aspects of all forms of eye movements are affected in PSP, the predominant defects concern vertical saccades (slow and hypometric, both up and down), impaired vergence, and inability to modulate the linear vestibulo-ocular reflex appropriately for viewing distance. These vertical and vergence eye movements habitually work in concert to enable visuomotor skills that are important during locomotion with the hands free. Taken with the prominent early feature of falls, these findings suggest that PSP tauopathy impairs a recently evolved neural system concerned with bipedal locomotion in an erect posture and frequent gaze shifts between the distant environment and proximate hands. This approach provides a conceptual framework that can be used to address the nosological challenge posed by overlapping clinical and neuropathological features of neurodegenerative tauopathies.

No MeSH data available.


Related in: MedlinePlus