Dorsal neck muscle vibration induces upward shifts in the endpoints of memory-guided saccades in monkeys.

Abstract

Producing a movement in response to a sensory stimulus requires knowledge of the body's current configuration, and spindle organs embedded within muscles are a primary source of such kinesthetic information. Here, we sought to develop an animal model of kinesthetic illusions induced by mechanically vibrating muscles as a first step toward a mechanistic understanding of how kinesthesia is integrated into neural plans for action. We elected to examine the effects of mechanical vibration of dorsal neck muscles in head-restrained monkeys performing memory-guided saccades requiring them to look to the remembered location of a flashed target only after an imposed delay. During the delay on one-half of all trials, mechanical vibration (usually 1,500 ms in duration, 200 microm in amplitude, 100 Hz in frequency) was applied to the dorsal aspect on one side of the monkey's neck. We compared the metrics of such vibration saccades to control saccades without vibration during the delay interval. Relative to control saccades, the endpoints of vibration saccades were shifted consistently upward, even though the variability in saccadic endpoints was unaltered. Although the stability of the eye was compromised during the delay interval of vibration trials, as evidenced by an increased incidence of upward drifts and downward microsaccades, vibration saccades displayed different metrics than control saccades, including an upwardly deviated radial direction and increased vertical amplitude. The influence of variations in the duration (500-2,500 ms), amplitude (100-300 microm), or frequency (75-125 Hz) of vibration scaled well with the presumed change in spindle activity entrained by vibration. Comparisons of the profile of these results are made to the human literature. We conclude that neck muscle vibration induces alterations in oculomotor performance in monkeys consistent with a central interpretation of illusory neck flexion and downward gaze deviation due to increased activation in the spindles of neck extensor muscles.