Abstract
The vestibuloocular reflex and other oculomotor functions are subserved by populations of neurons operating in parallel. This distributed aspect of the system's organization has been largely ignored in previous block diagram models. Neurons that transmit oculomotor signals, such as those in the vestibular nucleus (VN), actually combine the different types of signals in a diverse, seemingly random way that could not be predicted from a block diagram. We used the backpropagation learning algorithm to program distributed neural-network models of the vestibulo-oculomotor system. Networks were trained to combine vestibular, pursuit and saccadic eye velocity command signals. The model neurons in these neural networks have diverse combinations of vestibulo-oculomotor signals that are qualitatively similar to those reported for actual VN neurons in the monkey. This similarity implicates a learning mechanism as an organizing influence on the vestibulo-oculomotor system and demonstrates how VN neurons can encode vestibulo-oculomotor signals in a diverse, distributed manner.
Similar content being viewed by others
References
Chubb MC, Fuchs AF, Scudder CA (1984) Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements. J Neurophysiol 52:724–742
Collewijn H (1977) Optokinetic and vestibulo-ocular reflexes in dark-reared rabbits. Exp Brain Res 27:287–300
Fuchs AF, Kimm J (1975) Unit activity in the vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J Neurophysiol 38:1140–1161
Gisbergen JAM van, Robinson DA, Gielen S (1981) A quantitative analysis of generation of saccadic eye movements by burst neurons. J Neurophysiol 45:417–442
Ito M (1982) Cerebellar control of the vestibulo-ocular reflex — around the flocculus hypothesis. Ann Rev Neurosci 5:275–296
Lisberger SG, Miles FA (1980) Role of primate medial vestibular nucleus in long-term adaptive plasticity of vestibuloocular reflex. J Neurophysiol 43:1725–1745
Miles FA, Braitman DJ (1980) Long-term adaptive changes in primate vestibuloocular reflex. II. Electrophysiological observations on semicircular canal primary afferents. J Neurophysiol 43:1426–1436
Miles FA, Fuller JH, Braitman DJ, Dow BM (1980) Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. J Neurophysiol 43:1437–1476
Pola J, Robinson DA (1978) Oculomotor signals in the medial longitudinal fasciculus of the monkey. J Neurophysiol 41:245–259
Robinson DA (1970) Oculomotor unit behavior in the monkey. J Neurophysiol 33:393–404
Rumelhart DE, Hinton GE, Williams RJ (1986) Learning internal representations by error propagation. In: Rumelhart DE, McClelland JL, PDP Research Group (eds) Parallel distributed processing: explorations in the microstructure of cognition, vol 1: Foundations. MIT Press, Cambridge, pp 318–362
Sejnowski TJ, Rosenberg CR (1987) Parallel networks that learn to pronounce english text. Compl Syst 1:145–168
Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29:467–492
Tomlinson RD, Robinson DA (1984) Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol 51:1121–1136
Zipser D, Anderson RA (1988) A back propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 33:679–684
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Anastasio, T.J., Robinson, D.A. The distributed representation of vestibulo-oculomotor signals by brain-stem neurons. Biol. Cybern. 61, 79–88 (1989). https://doi.org/10.1007/BF00204592
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00204592