Jhj. Allum et F. Honegger, INTERACTIONS BETWEEN VESTIBULAR AND PROPRIOCEPTIVE INPUTS TRIGGERING AND MODULATING HUMAN BALANCE-CORRECTING RESPONSES DIFFER ACROSS MUSCLES, Experimental Brain Research, 121(4), 1998, pp. 478-494
Interactions between proprioceptive and vestibular inputs contributing
to the generation of balance corrections may vary across muscles depe
nding on the availability of sensory information at centres initiating
and modulating muscle synergies, and the efficacy with which the musc
le action can prevent a fall. Information which is not available from
one sensory system may be obtained by switching to another. Alternativ
ely, interactions between sensory systems and the muscle to which this
interaction is targeted may be fixed during neural development and no
t switchable. To investigate these different concepts, balance correct
ions with three different sets of proprioceptive trigger signals were
examined under eyes-open and eyes-closed conditions in the muscles of
normal subjects and compared with those of subjects with bilateral per
ipheral vestibular loss. The different sets of early proprioceptive in
puts were obtained by employing three combinations of support surface
rotation and translation, for which ankle inputs were nulled, normal o
r enhanced, the knees were either locked or in flexion, and the trunk
was either in flexion or extension. Three types of proprioceptive and
vestibulospinal interactions were identified in muscles responses. The
se interactions were typified by the responses of triceps surae, quadr
iceps, and paraspinal muscles. The amplitudes of stretch responses at
50 ms after the onset of ankle flexion in triceps surae muscles were r
elated to the velocity of ankle stretch. The amplitude of balance-corr
ecting responses at 100 ms corresponded more with stretch of the biart
icular gastrocnemius when the knee was re-extended at 60 ms. Absent st
retch reflexes at 50 ms in triceps surae with nulled ankle inputs caus
ed a minor, 12-ms delay in the onset of balance-correcting responses i
n triceps surae muscles. Vestibular loss caused no change in the ampli
tude of balance-correcting responses, but a negligible decrease in ons
et latency in triceps surae even with nulled ankle inputs. Stretch res
ponses in quadriceps at 80 ms increased with the velocity of knee flex
ion but were overall lower in amplitude in vestibular loss subjects. B
alance-correcting responses in quadriceps had amplitudes which were re
lated to the directions of initial trunk movements, were still present
when knee inputs were negligible and were also altered after vestibul
ar loss. Stretch and unloading responses in paraspinals at 80 ms were
consistent with the direction of initial trunk flexion and extension.
Subsequent balance-correcting responses in paraspinals were delayed 20
ms in onset and altered in amplitude by vestibular loss. The changes
in the amplitudes of ankle (tibialis anterior), knee (quadriceps) and
trunk (paraspinal) muscle responses with vestibular loss affected the
amplitudes and timing of trunk angular velocities, requiring increased
stabilizing tibialis anterior, paraspinal and trapezius responses pos
t 240 ms as these subjects attempted to remain upright. The results su
ggest that trunk inputs provide an ideal candidate for triggering bala
nce corrections as these would still be present when vestibular, ankle
and knee inputs are absent. The disparity between the amplitudes of s
tretch reflex and automatic balance-correcting responses in triceps su
rae and the insignificant alteration in the timing of balance-correcti
ng responses in these muscles with nulled ankle inputs indicates that
ankle inputs do not trigger balance corrections. Furthermore, modulati
on of balance corrections normally performed by vestibular inputs in s
ome but not all muscles is not achieved by switching to another sensor
y system on vestibular loss. We postulate that a confluence of trunk a
nd upper-leg proprioceptive input establishes the basic timing of auto
matic, triggered balance corrections which is then preferentially weig
hted by vestibular modulation in muscles that prevent falling. The org
anisation of balance corrections around trunk inputs portrayed here wo
uld have considerable advantage for the infant learning balance contro
l, but forces balance control centres to rely on limited sensory infor
mation related to this most unstable body segment, the trunk, when tri
ggering balance corrections.