Transformation of Vestibular Signals Into Motor Commands in the Vestibuloocular Reflex Pathways of Monkeys

Abstract

(VOR). If the VOR undergoes adaptive modification with spectacles that change the magnification of the visual scene, signals in one neural pathway are modified, whereas 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 the small stimuli we used (Ϯ15°/s), the afferents with the most regular spontaneous discharge fired throughout the cycle of oscillation even at 50 Hz, whereas afferents with more irregular discharge showed phase locking. For all afferents, the 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 very 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 brain stem neurons that participate in the modified versus unmodified VOR pathways. I N T R O D U C T I O NThe rotatory vestibuloocular reflex (VOR) is an excellent system for understanding how neural circuits generate simple behaviors. VOR performance has been studied thoroughly and the neural circuit is localized in the brain stem and cerebellum, where it can be studied in awake animals. The inputs to the horizontal rotatory VOR arise from vestibular primary afferents of the horizontal semicircular canal, which discharge in relationship to head velocity and acceleration. At the outputs, motoneurons in the abducens nucleus discharge in relation to eye velocity and position. Afferents and motoneurons are connected by a series of parallel pathways, the shortest of which include only one interneuron.Most of what we know about the operation of the neural circuits for the VOR comes from recordings made during the VOR induced by either low-frequency sinusoidal head oscillation or brief pulses of head velocity. In general, these stimuli have statistics that fall within the range found in head turns ( (1973) showed that signal transformations for the VOR can be modeled as two parallel pathways: 1) a velocity pathway that transmits afferent signals with little modification to provide the eye velocity component of motoneuron firing and 2) a position pathway that integrates the vestibular inputs to provide the eye position component of motoneuron firing. Second, Lisberger (1984, 1994 provi...

Rotational Responses of Vestibular–Nerve Afferents Innervating the Semicircular Canals in the C57BL/6 Mouse

“…The mean resting discharge rate was higher for regular than irregular afferents. The resting rate of afferents in mice was comparable to that previously reported in chinchillas, cats, and gerbils for both groups of afferents (Baird et al 1988;Hullar et al 2005;Tomko et al 1981; Murofushi and Curthoys 1997) but lower than that reported in monkeys Ramachandran and Lisberger 2006;Sadeghi et al 2007). The dependence of sensitivity and phase on rotational frequency is similar in the mouse to that reported in cats, chinchillas, and other mammals.…”

“…The striking difference between findings in mice and those in other mammalian species was the two-to fourfold lower rotational sensitivities of afferents in mice when compared to the sensitivities measured in monkeys Ramachandran and Lisberger 2006;Sadeghi et al 2007), chinchillas (Baird et al 1988;Hullar and Minor 1999;Hullar et al 2005), and cats (Tomko et al 1981). Lower phase leads with respect to head velocity were also noted in responses to highfrequency rotations (94 Hz) in mice when compared to these other species.…”

Neural Variability, Detection Thresholds, and Information Transmission in the Vestibular System

“…Our results with sinusoidal stimuli confirmed those of previous studies showing that, although irregular and regular afferents have comparable gains at frequencies of 0.5 Hz, irregular afferents consistently displayed higher gains with increasing frequency (Goldberg and Fernandez, 1971b;Baird et al, 1988;Hullar and Minor, 1999;Goldberg, 2000;Haque et al, 2004;Hullar et al, 2005;Ramachandran and Lisberger, 2006;Sadeghi et al, 2006). Moreover, random stimuli gave rise to qualitatively similar gains, which is consistent with the traditional linear system's approach applied to the vestibular system.…”

“…This suggests that irregular afferents play a greater role in vestibular processing of highfrequency head rotations, as suggested by previous studies (Goldberg and Fernandez, 1971a,b;Hullar et al, 2005;Ramachandran and Lisberger, 2006;Sadeghi et al, 2006). Another proposed function for irregular afferents is to mediate behaviorally appropriate changes in the VOR such as those necessitated by changes in viewing distance (Chen-Huang et al, 1997).…”

“…We note that linear decoding algorithms perform poorly when significant nonlinearities are present (Roddey et al, 2000). The low coding fractions and information rates observed for irregular afferents are most likely not attributable to static nonlinearities because our stimuli were within the linear encoding range (Hullar and Minor, 1999;Hullar et al, 2005;Sadeghi et al, 2006) where no phase-locking occurs (Ramachandran and Lisberger, 2006). Rather, our modeling results suggest that they are caused by high levels of intrinsic noise, which will also limit the performance of linear decoders (Roddey et al, 2000).…”