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Which Way is Up?
Abstract & Commentary
By Marc Dinkin, MD, Assistant Professor of Ophthalmology, Weill Cornell Medical College. Dr. Dinkin reports no financial interest in this field of study.
Synopsis: A novel technique used to study deviations in the subjective visual vertical may assist in the localization of brainstem lesions.
Source: Frisén L. Deviations of the visual upright in three dimensions in disorders of the brainstem: A clinical exploration. Brain 2010;133:3541-3551.
Deficits in the ability to determine one's position relative to the field of gravity are not uncommon in patients with neurological disease, and yet they often go undetected and may be underestimated in terms of their effect on patients' daily quality of life. In fact, it has been shown that 94% of patients with brainstem damage suffer from a deviation in their perception of what is straight up ("the subjective visual vertical" or SVV) in either the roll plane (rotating around an axis through one's stomach) or pitch plane (rotating around an axis extending from one hip to another). It follows that measuring a patient's sense of the SVV might help diagnose brainstem disease and even aid in localization. The bulk of prior studies have focused on deviations in roll, since they are parallel to ocular torsional movements, and since an association between imbalanced utricular-vestibular tone and the pathological ocular tilt reaction (OTR) has been well described. Deviations in perception of pitch were examined by Wikkels several years ago using a self-illuminated rod that was fixed in the sagittal plane and could be pushed forward and backward, in patients with hydrocephalus, with inconclusive results.
In a recent article in Brain, Lars Frisén studied 176 patients with neurological disease, using a similar self-illuminated rod that could be tilted along both the roll and pitch axes, in complete darkness, in an attempt to examine deviations in the SVV in three dimensions and their correlation with neuro-anatomical localization.
a.though control subjects showed almost no deviation in pitch, many patients with diffuse neurodegenerative disease (Parkinson disease and progressive supranuclear palsy [PSP]) showed an abnormal sense of pitch (defined as > ± 4°), but the direction of deviation could not be predicted based on disease. Interestingly, those patients in the obstructive hydrocephalus and pineal pathology groups tended to show negative deviations in pitch, with a shared downstream effect of dorsal midbrain compression proposed as an explanation for this common finding. Patients with cerebellar or craniocervical junction lesions also tended to show negative deviations in pitch, while medullary lesions typically produced positive deviations. Midbrain and pontine lesions varied, although analysis of a subset in the midbrain group suggested that ventral lesions were associated with positive deviations and dorsal lesions with negative deviations. Surprisingly, the degree of deviation in pitch did not correlate with limitations of vertical gaze in patients with the dorsal midbrain syndrome or PSP, implying that there is a separate substrate for static positioning and dynamic eye movements along the pitch axis.
In looking at deviations in roll, the only anatomical correlation was that laterally placed focal brainstem lesions tended to produce ipsiversive deviations in roll, in line with our current understanding of the neural substrate of the ocular tilt reaction. In general, the absolute value of deviation in pitch did not correlate well with that of roll, but in patients with the ocular tilt reaction, there was actually a tight correlation. How can this be explained? The author proposed a geometrical model to explain this phenomenon: Assuming a degree of convergence, the vertical planes of the two eyes overlaps in a vertical line at some point in the distance. Since, in patients with OTR, the degree of torsion typically is not symmetric between the two eyes, some extorsion or intorsion ensues. In the case of extorsion, the line of intersection of the two eyes' vertical planes tilts forward, and with intorsion, it tilts backwards, thus explaining how a greater deviation in roll (assumed to correlate with a larger difference in roll between the two eyes) would in turn cause a greater deviation in pitch.
The author supports this model by pointing out that an observer with a Maddox rod in front of each eye looking at a point source of light will perceive a forward pitch of the line produced when both rods are extorted and vice versa. It is then suggested that double Maddox rod testing could be used as a bedside clinical assay for deviations in roll and pitch simultaneously.
This appears to be one of the first studies to look at combined deviations in multiple planes at once in a large group of patients with neurological disease, and is strengthened by its unique multidirectional version of the self-illuminated rod. Among a plethora of papers examining roll, it provides novel analysis of some neuro-anatomical correlations with deviations in subjective pitch, and offers a satisfying geometrical model explaining its finding of an association between deviations in pitch and roll in patients with OTR. It is therefore enlightening from a neurophysiological perspective, but perhaps more importantly, suggests that the examination of deviations in subjective pitch could be used not only as a means to detect brainstem disease in patients with vertigo or ataxia, but perhaps to hone in on a more specific localization.
Its weakness lies in the relatively small numbers of patients in each clinical group, so that directional correlations, when present, need to be confirmed. Furthermore, the neuro-anatomical categories were fairly gross (midbrain, pons, etc.) while, in reality, finer subdivisions likely would yield stronger conclusions. Further research with larger numbers of patients and with higher resolution imaging techniques, might help confirm and expand proposed associations. Finally, the technique does not analyze deviations in yaw (around the axis of the body), which previously have been associated with peripheral vestibular lesions. Combining the present method with a simple pointing test aimed at detecting such deviations in yaw would yield a more truly 3D picture of pathological perception of position in space in patients suffering from brainstem disease.