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 memoryguided 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 m 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 m), 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.

Absence of Spatial Updating when the Visuomotor System Is Unsure about Stimulus Motion

“…For example, neck-muscle vibration causes illusory motion of foveated targets (Biguer et al, 1988), and vibration of monkey dorsal neck-muscles shifts memory-guided saccade endpoints upwards (Corneil and Andersen, 2004).…”

Representation of Horizontal Head-on-Body Position in the Primate Superior Colliculus

“…A likely source signaling head-on-body position is the plentiful spindle organs found within the deeper neck muscles adjacent to the spinal column (Bakker and Richmond 1982;Cooper and Daniel 1963;Richmond and Abrahams 1975;Richmond et al 1999). Mechanical vibration of the muscles of the eyes or neck also influences the metrics of many movements, including saccades (e.g., Corneil and Andersen 2004;Roll et al 1991;Taylor and McCloskey 1991), and head-restraint and changes in head-on-body orientation influence the localization of auditory stimuli (Goossens and Van Opstal 1999;Populin 2006;Tollin et al 2005). Finally, profound deficits in balance, posture, and guided actions follow disruption of proprioceptive inputs from neck muscles (Biemond and de Jong 1969;Cohen 1961;de Jong et al 1977).…”

Muscular proprioception contributes to the control of interceptive actions.

“…Such responses of Ia muscle spindle afferents are well known to evoke illusory sensation of movement (Goodwin, McCloskey, & Matthews, 1972). The influence of vibration applied to neck and/or ocular muscles when pointing toward stationary targets has also been extensively investigated in the past (Biguer, Donaldson, Hein, & Jeannerod, 1988; Roll, Velay, & Roll, 1991; Taylor & McCloskey, 1991; Corneil & Andersen, 2004). Generally, the head of the participant is immobilized and the task is performed (visual) open loop toward a previously seen target.…”