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J Neurophysiol 101: 2847-2858, 2009. First published April 1, 2009; doi:10.1152/jn.90895.2008
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Tonic Central and Sensory Stimuli Facilitate Involuntary Air-Stepping in Humans

V. A. Selionov1, Y. P. Ivanenko2, I. A. Solopova1 and V. S. Gurfinkel3

1Laboratory of Neurobiology of Motor Control, Institute for Information Transmission Problems, Russian Academy of Science, Moscow, Russia; 2Laboratory of Neuromotor Physiology, Istituti di Ricovero e Cura a Carattere Scientifico Fondazione Santa Lucia Roma, Rome, Italy; and 3Neurological Sciences Institute, Oregon Health and Science University, Beaverton, Oregon

Submitted 7 August 2008; accepted in final form 25 March 2009

Air-stepping can be used as a model for investigating rhythmogenesis and its interaction with sensory input. Here we show that it is possible to entrain involuntary rhythmic movement patterns in healthy humans by using different kinds of stimulation techniques. The subjects lay on their sides with one or both legs suspended, allowing low-friction horizontal rotation of the limb joints. To evoke involuntary stepping of the suspended leg, either we used continuous muscle vibration, electrical stimulation of the superficial peroneal or sural nerves, the Jendrassik maneuver, or we exploited the postcontraction state of neuronal networks (Kohnstamm phenomenon). The common feature across all stimulations was that they were tonic. Air-stepping could be elicited by most techniques in about 50% of subjects and involved prominent movements at the hip and the knee joint (~40–70°). Typically, however, the ankle joint was not involved. Minimal loading forces (4–25 N) applied constantly to the sole (using a long elastic cord) induced noticeable (~5–20°) ankle-joint-angle movements. The aftereffect of a voluntary long-lasting (30-s) contraction in the leg muscles featured alternating rhythmic leg movements that lasted for about 20–40 s, corresponding roughly to a typical duration of the postcontraction activity in static conditions. The Jendrassik maneuver per se did not evoke air-stepping. Nevertheless, it significantly prolonged rhythmic leg movements initiated manually by an experimenter or by a short (5-s) period of muscle vibration. Air-stepping of one leg could be evoked in both forward and backward directions with frequent spontaneous transitions, whereas involuntary alternating two-legged movements were more stable (no transitions). The hypothetical role of tonic influences, contact forces, and bilateral coordination in rhythmogenesis is discussed. The results overall demonstrated that nonspecific tonic drive may cause air-stepping and the characteristics and stability of the evoked pattern depended on the sensory input.


Address for reprint requests and other correspondence: Y. P. Ivanenko, Laboratory of Neuromotor Physiology, IRCCS Fondazione Santa Lucia, 306 via Ardeatina, 00179 Rome, Italy (E-mail: y.ivanenko{at}hsantalucia.it)







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