457 
DISTRIBUTED NEURAL INFORMATION PROCESSING 
IN THE VESTIBULO-OCULAR SYSTEM 
Clifford Lau 
Office of Naval Research Detachment 
Pasadena, CA 91106 
Vicente Honrubia* 
UCLA Division of Head and Neck Surgery 
Los Angeles, CA 90024 
ABSTRACT 
A new distributed neural information-processing 
model is proposed to explain the response characteristics 
of the vestibulo-ocular system and to reflect more 
accurately the latest anatomical and neurophysiological 
data on the vestibular afferent fibers and vestibular nuclei. 
In this model, head motion is sensed topographically by hair 
cells in the semicircular canals. Hair cell signals are then 
processed by multiple synapses in the primary afferent 
neurons which exhibit a continuum of varying dynamics. The 
model is an application of the concept of "multilayered" 
neural networks to the description of findings in the 
bullfrog vestibular nerve, and allows us to formulate 
mathematically the behavior of an assembly of neurons 
whose physiological characteristics vary according to their 
anatomical properties. 
INTRODUCTION 
Traditionally the physiological properties of 
individual vestibular afferent neurons have been modeled as 
a linear time-invariant system based on Steinhausen's 
description of cupular motion. 1 The vestibular nerve input 
to different parts of the central nervous system is usually 
represented by vestibular primary afferents that have 
*Work supported by grants NS09823 and NS08335 from the National 
Institutes of Health (NINCDS) and grants from the Pauley Foundation and the 
Hope for Hearing Research Foundation. 
American Institute of Physics 1988 
458 
response properties defined by population averages from 
individual neurons. 2 
A new model of vestibular nerve organization is 
proposed to account for the observed variabilities in the 
primary vestibular afferent's anatomical and physiological 
characteristics. The model is an application of the concept 
of "multilayered" neural networks, 3,4 and it attempts to 
describe the behavior of the entire assembly of vestibular 
neurons based on new physiological and anatomical findings 
in the frog vestibular nerve. It was found that primary 
vestibular afferents show systematic differences in 
sensitivity and dynamics and that there is a correspondence 
between the individual neuron's physiological properties and 
the location of innervation in the area of the crista and also 
the sizes of the neuron's fibers and somas. This new view 
of topological organization of the receptor and vestibular 
nerve afferents is not included in previous models of 
vestibular nerve function. Detailed findings from this 
laboratory on the anatomical and physiological properties of 
the vestibular afferents in the bullfrog have been 
published. 5,6 
REVIEW OF THE ANATOMY AND PHYSIOLOGY 
OF THE VESTIBULAR NERVE 
The most pertinent anatomical and physiological data 
on the bullfrog vestibular afferents are summarized here. 
In the vestibular nerve from the anterior canal four major 
branches (bundles) innervate different parts of the crista 
(Figure 1). From serial histological sections it has been 
shown that fibers in the central bundle innervate hair cells 
at the center of the crista, and the lateral bundles project 
to the periphery of the crista. In each nerve there is an 
average of 1170 _+ 171 (n -- 5) fibers, of which the thick 
fibers (diameter > 7.0 microns, large dots) constitute 8% 
and the thin fibers (< 4.0 microns, small dots) 76%. The 
remaining fibers (16%) fall into the range between 4.0 and 
7.0 microns. We found that the thick fibers innervate only 
the center of the crista, and the thinner ones predominantly 
innervate the periphery. 
459 
400 
00 2 4 6 8 10 12 14 16 18 20 
DIAMETER (m i cron) 
Fig. 1. Number of fibers and their diameters in the anterior 
semicircular canal nerve in the bullfrog. 
There appears to be a physiological and anatomical 
correlation between fiber size and degree of regularity of 
spontaneous activity. By recording from individual neurons 
and subsequently labeling them with horseradish peroxidase 
intracellularly placed in the axon, it is possible to visualize 
and measure individual ganglion cells and axons and to 
determine the origin of the fiber in the crista as well as the 
projections in different parts of the vestibular nuclei. 
Figure 2 shows an example of three neurons of different 
sizes and degrees of regularity of spontaneous activity. In 
general, fibers with large diameters tend to be more 
irregular with large coefficients of variation (CV) of the 
interspike intervals, whereas thin fibers tend to be more 
regular. There is also a relationship for each neuron 
between CV and the magnitude of the response to 
physiological rotatory stimuli, that is, the response gain. 
(Gain is defined as the ratio of the response in spikes per 
second to the stimulus in degrees per second.) Figure 3 
shows a plot of gain as a function of CV as well as of fiber 
diameter. For the more regular fibers (CV < 0.5), the gain 
tends to increase as the diameter of the fiber increases. 
460 
,500um 
THIN MEDIUM THICK 
C.V. = 0.25 C V = 0 39 C V = 0 61 
,t . 
0 200 0 200 0 200 
MILLISECONDS 
Fig. 2. Examples of thin, medium and thick fibers and their 
spontaneous activity. CV - coefficient of variation. 
For the more irregular fibers (CV > 0.5), the gain tends to 
remain the same with increasing fiber diameter (4.9 _+ 1.9 
spik es/seco n d/d eg rees/seco nd). 
Figure 4 shows the location of projection of the 
afferent fibers at the vestibular nuclei from the anterior, 
posterior, and horizontal canals and saccule. There is an 
overall organization in the pattern of innervation from the 
afferents of each vestibular organ to the vestibular nuclei, 
with fibers from different receptors overlapping in various 
461 
0.1 
3.8 6.1 8.4 10.7 13.0 15.3 
FIBER DIAMETER 
I , ! . I I . I . 
0 0.2 0.4 0.6 0.8 1 1.2 
Coefficient of Variation 
Fig. 3. Gain versus fiber diameters and CV. Stimulus was a 
sinusoidal rotation of 0.05 Hz at 22 degrees/second peak 
velocity. 
parts of the vestibular nuclei. Fibers from the anterior 
semicircular canal tend to travel ventrally, from the 
horizontal canal dorsally, and from the posterior canal the 
most dorsally. 
For each canal nerve the thick fibers (indicated by 
large dots) tend to group together to travel lateral to the 
thin fibers (indicated by diffused shading); thus, the 
topographical segregation between thick and thin fibers at 
the periphery is preserved at the vestibular nuclei. 
In following the trajectories of individual neurons in 
the central nervous system, however, we found that each 
fiber innervates all parts of the vestibular nuclei, caudally 
to rostrally as well as transversely, and because of the 
spread of the large number of branches, as many as 200 
from each neuron, there is a great deal of overlap among the 
projections. 
DISTRIBUTED NEURAL INFORMATION-PROCESSING MODEL 
Figure 5 represents a conceptual organization, based 
on the above anatomical and physiological data, of Scarpa's 
462 
ANT. 
HORIZ. 
Fig. 4. 
POST. 
SAC. 
Three-dimensional reconstruction of the primary 
afferent fibers' location in the vestibular nuclei. 
ganglion cells of the vestibular nerve and their innervation 
of the hair cells and of the vestibular nuclei. The diagram 
depicts large Scarpa's ganglion cells with thick fibers 
innervating restricted areas of hair cells near the center of 
the crista (top) and smaller Scarpa's ganglion cells with 
thin fibers on the periphery of the crista innervating 
multiple hair cells with a great deal of overlap among 
fibers. At the vestibular nuclei, both thick and thin fibers 
innervate large areas with a certain gradient of overlapping 
among fibers of different diameters. 
The new distributed neural information-processing 
model for the vestibular system is based on this anatomical 
organization, as shown in Figure 6. The response 
463 
S, G, 
H.C. 
Fig. 5. Anatomical 
organization of the 
vestibular nerve. 
H.C. - hair ceils. 
S.G.- Scarpa's 
ganglion ceils. 
V.N. - vestibular 
nuclei. 
Fig. 6. Distributed neural 
the vestibular nerve. 
information-processing model of 
464 
characteristic of the primary afferent fiber is represented 
by the transfer function SGj(s). This transfer function 
serves as a description of the gain and phase response of 
individual neurons to angular rotation. The simplest model 
would be a first-order system with d.c. gain Kj (spikes/ 
second over head acceleration) and a time constant Tj 
(seconds) for the jth fiber as shown in equation (1): 
Kj 
SGj(s) = 1 + sT'j'"' (1) 
For the bullfrog, Kj can range from about 3 to 25 
spikes/second/degree/second 2, and Tj from about 10 to 0.5 
second. The large and high-gain neurons are more phasic 
than the small neurons and tend to have shorter time 
constants. As described above, Kj and Tj for the jth neuron 
are functions of location and fiber diameter. Bode plots 
(gain and phase versus frequency) of experimental data 
seem to indicate, however, that a better transfer function 
would consist of a higher-order system that includes 
fractional power. This is not surprising since the afferent 
fiber response characteristic must be the weighted sum of 
several electromechanical steps of transduction in the hair 
cells. A plausible description of these processes is given in 
equation (2): 
K k 
SGj(s) = '. Wjk 1 + sT k ' 
k 
(2) 
where gain K k and time constant T k are the electro- 
mechanical properties of the hair cell-cupula complex and 
are functions of location on the crista, and Wjk is the 
synaptic efficacy (strength) between the jth neuron and the 
kth hair cell. In this context, the transfer function given 
in equation (1) provides a measure of the "weighted 
average" response of the multiple synapses given in 
equation (2). 
465 
We also postulate that the responses of the vestibular 
nuclei neurons reflect the weighted sums of the responses 
of the primary vestibular afferents, as follows: 
VN i=f(y., Tij SGj), (3) 
J 
where f(.) is a sigmoid function describing the change in 
firing rates of individual neurons due to physiological 
stimulation. It is assumed to saturate between 100 to 300 
spikes/second, depending on the neuron. Tij is the synaptic 
efficacy (strength) between the ith vestibular neuron and 
the jth afferent fiber. 
CONCLUSIONS 
Based on anatomical and physiological data from the 
bullfrog we presented a description of the organization of 
the primary afferent vestibular fibers. The responses of 
the afferent fibers represent the result of summated 
excitatory processes. The information on head movement in 
the assemblage of neurons is codified as a continuum of 
varying physiological responses that reflect a sensoritopic 
organization of inputs from the receptor to the central 
nervous system. We postulated a new view of the 
organization in the peripheral vestibular organs and in the 
vestibular nuclei. This view does not require unnecessary 
simplification of the varying properties of the individual 
neurons. The model is capable of extracting the weighted 
average response from assemblies of large groups of 
neurons while the unitary contribution of individual neurons 
is preserved. The model offers the opportunity to 
incorporate further developments in the evaluation of the 
different roles of primary afferents in vestibular function. 
Large neurons with high sensitivity and high velocity of 
propagation are more effective in activating reflexes that 
require quick responses such as vestibulo-spinal and 
vestibulo-ocular reflexes. Small neurons with high 
thresholds for the generation of action potentials and lower 
sensitivity are more tuned to the maintenance of posture 
466 
and muscle tonus. We believe the physiological differences 
reflect the different physiological roles. 
In this emerging scheme of vestibular nerve 
organization it appears that information about head 
movement, topographically filtered in the crista, is 
distributed through multiple synapses in the vestibular 
centers. Consequently, there is also reason to believe that 
different neurons in the vestibular nuclei preserve the 
variability in response characteristics and the topological 
discrimination observed in the vestibular nerve. Whether 
this idea of the organization and function of the vestibular 
system is valid remains to be proven experimentally. 
1. W. Steinhausen, Arch. Ges. Physiol. 217, 747 (1927). 
2. J. M. Goldberg and C. Fernandez, in: Handbook of 
Physiology, Sect. 1, Vol. III, Part 2 (I. Darian-Smith, 
ed., Amer. Physiol. Soc., Bethesda, MD, 1984), p. 977. 
3. D. E. Rumelhart, G. E. Hinton and J. L. McClelland, in: 
Parallel Distributed Processing: Explorations in the 
Microstructure of Cognition, Vol. 1: Foundations 
(D. E. Rumelhart, J. L. McClelland and the PDP Research 
Group, eds., MIT Press, Cambridge, MA, 1986), p. 45. 
4. J. Hopfield, Proc. Natl. Acad. Sci. 7), 2554 (1982). 
5. V. Honrubia, S. Sitko, J. Kimm, W. Betts and I. Schwartz, 
Intern. J. Neurosci. 1,, 197 (1981). 
6. V. Honrubia, S. Sitko, R. Lee, A. Kuruvilla and I. Schwartz, 
Laryngoscope 94, 464 (1984). 
