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Journal of Neuroscience, Vol 3, 1234-1244, Copyright © 1983 by Society for Neuroscience
Frequency-selective adaptation: evidence for channels in the vestibulo- ocular reflex?
SG Lisberger, FA Miles and LM Optican
The vestibulo-ocular reflex (VOR) is under long-term adaptive regulation to
minimize retinal image slip during head movement; normally this process
keeps VOR gain (eye velocity divided by head velocity) near 1.0. It has
been common to think of the adaptive mechanism as a single pure gain
element, although some properties of the system (e.g., frequency-selective
changes in the gain of the VOR) argue that it must be more complex. We now
report new observations on the frequency selectivity of the adaptive
mechanism. Our data suggest a new model in which the VOR operates as a
series of parallel, temporal frequency channels, each of which has an
independently adjustable gain element. Adaptive changes were produced by
oscillating monkeys sinusoidally at a single temporal frequency (0.2 or 2.0
Hz) in visual conditions that cause either increases (toward two) or
decreases (toward zero) in VOR gain. When tested in darkness at the
adapting frequency, the VOR showed large changes in gain and little or no
change in phase. When tested at frequencies other than the adapting
frequency, the VOR showed less pronounced changes in gain and unexpected
changes in phase. The phase changes were orderly but depended in a complex
way on adapting frequency, testing frequency, and VOR gain. We have tested
the channels concept by calculating the response properties of a
mathematical model that processed its inputs in parallel pathways. The
model reproduced our data when we assumed that the vestibular primary
afferents were distributed in an orderly way to parallel brain channels
that had differing dynamics: vestibular inputs with more phase lead
projected to higher frequency channels, which themselves had faster
dynamics than their low frequency counterparts. Such an organization, when
regulated by an adaptive controller that can selectively alter the gain of
one channel, could play a key role in establishing and maintaining the
frequency-independent performance seen in the adult VOR.
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