Abnormal vestibular control of gaze and posture in a strain of a waltzing rat.

Abstract

The waltzing behavior is usually attributed to vestibular dysfunction. However, the vestibular control of gaze and posture has not yet been measured quantitatively in any waltzing mutant. Therefore, this study was aimed at investigating the relationship between inner-ear morphology, the circling behavior, and the vestibular control of gaze and posture in a new strain of waltzing rats. Light- and electron-microscopy studies of these mutants did not reveal any structural abnormalities of the vestibular neural epithelia. In addition, the expression of Calretinin and 200-kD phosphorylated and non-phosphorylated neurofilaments was also found to be normal in the vestibular neural epithelia and ganglion cells. In contrast, the mutants showed severe dysfunctions of the vestibular control of gaze and posture. The skeletal geometry of the alert unrestrained animals was studied using cineradiography. At rest, waltzing rats held their heads tilted down: the horizontal semicircular-canal's plane was near the earth-horizontal's plane, instead of being tilted up as in Long Evans control rats. In addition, their cervical column was pitched more forward (33.6 degrees) than in the control group (6.9 degrees). The circling behavior was observed frequently, and the rats had episodes of circling in both directions. The episodes of circling amounted to an average of 17 turns, and the average angular velocity of the circling was 645 degrees/s. Unilateral labyrinthectomy induced the same postural and oculomotor syndromes in the waltzing and control groups. This indicates that the mutant vestibular nerve had a significant resting discharge before the lesion. Eye movements were recorded using acutely implanted search coils. Although waltzing rats were able to perform normal spontaneous eye movements, they showed a complete deficit of the horizontal vestibulo-ocular reflex (HVOR) and an impairment of the maculo-ocular reflex (MOR) during constant velocity, off-vertical axis rotation (OVAR). These results show, for the first time, that deficient transduction and/or processing of the horizontal-canal- and macular-related information can be causally related to the circling behavior and abnormal posture, respectively.