A pathway in the brainstem for roll-tilt of the subjective visual vertical: evidence from a lesion-behavior mapping study

Abstract

The perceived subjective visual vertical (SVV) is an important sign of a vestibular otolith tone imbalance in the roll plane. Previous studies suggested that unilateral pontomedullary brainstem lesions cause ipsiversive roll-tilt of SVV, whereas pontomesencephalic lesions cause contraversive roll-tilts of SVV. However, previous data were of limited quality and lacked a statistical approach. We therefore tested roll-tilt of the SVV in 79 human patients with acute unilateral brainstem lesions due to stroke by applying modern statistical lesion-behavior mapping analysis. Roll-tilt of the SVV was verified to be a brainstem sign, and for the first time it was confirmed statistically that lesions of the medial longitudinal fasciculus (MLF) and the medial vestibular nucleus are associated with ipsiversive tilt of the SVV, whereas contraversive tilts are associated with lesions affecting the rostral interstitial nucleus of the MLF, the superior cerebellar peduncle, the oculomotor nucleus, and the interstitial nucleus of Cajal. Thus, these structures constitute the anatomical pathway in the brainstem for verticality perception. Present data indicate that graviceptive otolith signals present a predominant role in the multisensory system of verticality perception.

Figure 1.

A, Simple overlay of all patients (n = 79); images of left-side lesions were flipped to the right side. The number of overlapping lesions is illustrated by different colors that code increasing frequencies from violet (n = 1) to red (n = 79). B, C, VLBM analysis comparing the patients with contraversive tilt of SVV (n = 39) (B) and the patients with ipsiversive tilt (n = 40) with respect to absolute SVV tilt (t test statistics) (C). All voxels that survived a correction for multiple comparisons using a 5% FDR cutoff threshold are shown. D, Subtraction analysis of patients with lesions that affect the anteromedial pontomesencephalic region with tilt (tilt, >2.5°) versus patients without tilt of the SVV. The percentage of overlapping lesions in the patients with tilt after subtraction of the controls is illustrated by different colors coding increasing frequencies, from violet (0%) to dark red (100%). This reflects the relative frequency of damage, i.e., the corresponding percentage of patients with tilt who are more frequently affected than in the control group.

Figure 2.

A, Subtraction analysis of patients with contraversive roll-tilts of SVV and pathological OT versus no OT. B, Subtraction analysis of patients with ipsiversive roll-tilts of SVV and pathological OT versus no OT. C, D, Uncorrected data including the standard deviation within subjects as continuous variable for the patients with contralesional (C) and ipsilesional (D) tilt of SVV.