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Keywords:

  • walking;
  • semicircular canals;
  • angular vestibulo-collic reflex (aVCR);
  • vestibular;
  • cynomolgus;
  • swing-phase dynamics

The vestibular system plays an important role in controling gait, but where in the labyrinths relevant activity arises is largely unknown. After the semicircular canals are plugged, low frequency (0.01–2 Hz) components of the angular vestibulo-ocular reflex (aVOR) and angular vestibulo-collic reflex (aVCR) are lost, but high frequency (3–20 Hz) components remain. We determined how loss of low frequency canal afference affects limb and head movements during quadrupedal locomotion. Head, body, and limb movements were recorded in three dimensions (3-D) in a cynomolgus monkey with a motion detection system, while the animal walked on a treadmill. All six canals were plugged, reducing the canal time constants from ≈4.0 sec to ≈0.07 sec. Major changes in the control of the limbs occurred after surgery. Fore and hind limbs were held farther from the body, producing a broad-based gait. Swing-phase trajectories were inaccurate, and control of medial-lateral limb movement was erratic. These changes in gait were present immediately after surgery, as well as 15 months later, when the animal had essentially recovered. Thus, control of the limbs in the horizontal plane was defective after loss of the low-frequency semicircular canal input and never recovered. Cycle-averaged pitch and roll head rotations, and 3-D head translations were also significantly larger and more erratic after than before surgery. Head rotations in yaw could not be quantified due to intrusion of voluntary head turns. These findings indicate that the semicircular canals provide critical low frequency information to maximize the accuracy of stepping and stabilize the head during normal quadrupedal locomotion.