Vestibular control of the head: possible functions of the vestibulocollic reflex

Abstract

Here, we review the angular vestibulocollic reflex (VCR) focusing on its function during unexpected and voluntary head movements. Theoretically, the VCR could (1) stabilize the head in space during body movements and/or (2) dampen head oscillations that could occur as a result of the head’s underdamped mechanics. The reflex appears unaffected when the simplest, trisynaptic VCR pathways are severed. The VCR’s efficacy varies across species; in humans and monkeys, head stabilization is ineffective during low-frequency body movements in the yaw plan. While the appearance of head oscillations after the attenuation of semicircular canal function suggests a role in damping, this interpretation is complicated by defects in the vestibular input to other descending motor pathways such as gaze premotor circuits. Since the VCR should oppose head movements, it has been proposed that the reflex is suppressed during voluntary head motion. Consistent with this idea, vestibular-only (VO) neurons, which are possible vestibulocollic neurons, respond vigorously to passive, but not active, head rotations. Although VO neurons project to the spinal cord, their contribution to the VCR remains to be established. VCR cancelation during active head movements could be accomplished by an efference copy signal negating afferent activity related to active motion. Oscillations occurring during active motion could be eliminated by some combination of reflex actions and voluntary motor commands that take into account the head’s biomechanics. A direct demonstration of the status of the VCR during active head movements is required to clarify the function of the reflex.

Appendix

The model depicted in Fig. 6 includes the following transfer functions, expressed in terms of the Laplace operator, s (Peng et al. 1996).

$$ {\text{Vestibulocollic}}:\quad {\text{VCR}} = {\frac{{K_{\text{VCR}} \left( {\tau_{1A} s + 1} \right)\left( {\tau_{{{\text{CNS}}1}} s + 1} \right)}}{{\left( {\tau_{C} s + 1} \right)\left( {\tau_{{{\text{CNS}}2}} s + 1} \right)}}} $$

(3)

$$ {\text{Cervicocollic}}:\quad {\text{CCR}} = {\frac{{K_{\text{CCR}} \left( {\tau_{{{\text{MS}}1}} s + 1} \right)\left( {\tau_{{{\text{MS}}2}} s + 1} \right)}}{{s^{2} }}} $$

(4)

$$ {\text{Plant}}:\quad P = {\frac{{s^{2} }}{{Is^{2} + Bs + K}}} $$

(5)

$$ {\text{Torque}}\;{\text{converter}}:\quad T = {\frac{{K_{TC} }}{{\tau_{TC} + 1}}} $$

(6)

The s ² operator in Eq. 5, which is equivalent in the time domain to taking a second derivative, converts the position variables (Ψ, Θ and VOL) to acceleration variables.

Parameters: I = 0.0148 kg m², B = 0.1 N m s/rad, K = 2.077 N m/rad, K _VCR = 30, K _tc  = 1, τ _tc  = 0.1 s, τ _1A  = 0.1 s, τ _C  = 7 s, τ _CNS1 = 0.4 s, τ _CNS2 = 20 s, K _CCR = 0.1, τ _MS1 = 0.1 s, τ _MS2 = 0.1 s. Mechanical properties of the head: I, moment of inertia; B, viscosity; K, elasticity. K _VCR, K _CCR, and K _TC , gains of VCR, CCR, and T.

Calculations in Figs. 8 and 9 were based on the following transfer function:

$$ {\frac{\theta (s)}{\psi (s)}} = {\frac{{ - I - {\text{VCR}}(s) \cdot T(s)}}{{{\frac{1}{P(s)}} + T(s)\left[ {{\text{VCR}}(s) + {\text{CCR}}(s)} \right]}}} $$

(7)