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J Neurophysiol (June 7, 2006). doi:10.1152/jn.00281.2006
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00281.2006v1
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Submitted on March 15, 2006
Accepted on May 31, 2006

Transformation of vestibular signals into motor commands in the vestibulo-ocular reflex pathways of monkeys

Ramnarayan Ramachandran1* and Stephen G Lisberger2

1 Dept. of Physiology, UCSF, San Francisco, California, United States
2 Physiology, UCSF, San Francisco, California, United States

* To whom correspondence should be addressed. E-mail: rramacha{at}phy.ucsf.edu.

Parallel pathways mediate the rotatory vestibulo-ocular reflex (VOR). If the VOR undergoes adaptive modification with spectacles that change the magnification of the visual scene, signals in one neural pathway are modified while those in another are not. By recording the responses of vestibular afferents and Abducens neurons for vestibular oscillations at frequencies from 0.5 to 50 Hz, we have elucidated how vestibular signals are processed in the modified versus unmodified VOR pathways. For small stimuli (±15°/s), the afferents with the most regular spontaneous discharge fired throughout the cycle of oscillation even at 50 Hz, while afferents with more irregular discharge showed phase locking. For all afferents, firing rate was in phase with stimulus head velocity at low frequencies and showed progressive phase lead as frequency increased. Sensitivity to head velocity increased steadily as a function of frequency. Abducens neurons showed highly regular spontaneous discharge and little evidence of phase locking. Their sensitivity to head velocity during the VOR was relatively flat across frequencies; firing rate lagged head velocity at low frequencies and shifted to large phase leads as stimulus frequency increased. When afferent responses were provided as inputs to a two pathway model of the VOR, the output of the model reproduced the responses of Abducens neurons if the unmodified and modified VOR pathways had frequency-dependent internal gains and included fixed time delays of 1.5 and 9 ms. The phase shifts predicted by the model provide fingerprints for identifying brainstem neurons that participate in the modified versus unmodified VOR pathways.




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