Over the past
30 years, equilibrium-point theories (Feldman, 1966, 1986;
Bizzi, Polit & Morasso, 1976; Bizzi, Accornero, Chapple
& Hogan, 1984) have become the predominant explanations
for how descending neural commands regulate movement and
posture, and the "perturbation paradigm" has
emerged as a key method for testing them. Recently, we
(Lackner & DiZio, 1994; DiZio & Lackner, 1995)
introduced a novel technique for perturbing movements
that employs a rotating "artificial gravity"
environment and obtained results that violate basic predictions
of current theories.
Equilibrium-point
theories state that commands issued to spinal neurons
and interneurons directly regulate muscle length-tension
relationships. According to this theory, movement is a
mechanical consequence of attraction to an equilibrium
posture at which muscles exert spring-like forces that
balance opposing limb loads. If sufficient settling time
is allowed, neither transient external loads imposed during
a movement nor transient internal errors in the motor
program will affect movement endpoint, which is a balance
between only the final external forces and the final programmed
length-tension relationships. Bizzi, Accornero, Chapple
and Hogan (1984) showed experimentally that the ability
to move a manipulandum to targets is not altered by brief
assistive or resistive perturbations applied through the
manipulandum.
We explored
the effects of a novel sort of transient perturbation
produced in a rotating room and found that movement endpoints
and paths were deviated. Rotation provides one means of
generating "artificial gravity" (centrifugal
force) for long duration space missions and also produces
Coriolis forces. We avoided the former by keeping experimental
subjects at the axis of rotation and took advantage of
the latter for perturbing movements. During rotation,
transient Coriolis forces perpendicular to movement direction
and proportional to velocity are generated, as illustrated
in Figure 1A. Coriolis forces act without contacting the
limb because they are inertial forces. By contrast, deviations
produced with a manipulandum are always associated with
spatially significant contact forces on the hand.
One experiment
demonstrated that when subjects rotating at 10 rpm reach
out to touch targets, they show substantial movement curvature
and miss the desired target position by a large amount,
both deviations being in the direction of the Coriolis
force generated. Within about 10 movements, subjects adapt
completely and move in straight paths to the target, without
ever seeing their arm or feeling the targets (which are
embedded in a smooth surface). When rotation ceases, subjects
again make reaching errors with the adapted arm; endpoints
and movement paths are initially deviated in the direction
opposite the Coriolis force that had been present during
rotation. Figures 1B and 1C illustrate the results.
Deviation of
movement endpoints by Coriolis forces violates the fundamental
prediction of equilibrium-point theories and excludes
muscle length-tension characteristics from consideration
as a neural control variable for motor programming. Rapid,
complete adptation to Coriolis force perturbations without
vision means movement trajectories are closely monitored
and controlled, on the basis of afferent signals from
muscle spindles, joint receptors and Golgi tendon organs
in relation to efferent commands. The differences between
results from these experiments with non-contacting Coriolis
force perturations and results from previous experiments
with mechanical perturbations applied through local contact
indicate that cutaneous sensory signals also have a critical
regulatory role in real-time trajectory control. Adaptation
to Coriolis forces requires new motor commands to achieve
the original trajectory, and the presence of mirror-image
aftereffects reveals that these new commands produce forces
that exactly cancel the Coriolis forces at every point
in the movement trajectory, suggesting force as the controlled
variable and a neural representation of limb dynamics
as a mediator.
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