Neural network simulations of the primate oculomotor system. II. Frames of reference

doi:10.1016/0361-9230(96)00124-4

Brain Research Bulletin

Volume 40, Issues 5–6, 1996, Pages 337-343

https://doi.org/10.1016/0361-9230(96)00124-4 Get rights and content

Abstract

Theories of motor control often assume that the location of visual stimuli is expressed in non retinotopic frames of reference. The saccadic system is known in enough detail for us to examine the evidential basis of this assumption. The organization of the neural circuit that controls saccades is first summarized. It is shown to consist of at least two interconnected modules. The first one is the burst generator, which resides in the reticular formation, and is entrusted with the tasks of impedance matching, synergist coactivation and reciprocal inhibition between antagonists. The second is a metric computer, which resides in the superior colliculus and the cerebral cortex, and computes the size and direction of the desired movement. Alternative models of the burst generator are presented and their “verisimilitude” is assessed in the light of evidence concerning saccadic trajectories, neuronal discharge patterns, interneuronal connections, as well as the results of lesion and stimulation experiments. Several models of the “metric computer” in the superior colliculus are then examined; their performance is again evaluated in the light of psychophysical, anatomical, physiological, and clinical evidence. It is demonstrated that the location of visual stimuli need not be expressed in nonretinotopic frames of reference for either the burst generator or the metric computer to issue appropriate commands to move the eyes. Instead, using information concerning intervening movements of the eyes to update the location of visual stimuli in a retinotopic frame of reference suffices for the planning and execution of correct saccades. More generally, it is proposed that the location of sensory stimuli need not be expressed in higher order frames of reference (e.g., centered in the body or even in extrapersonal space) provided that their location in a sensorium specific map is updated on the basis of effector movements.

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Implications of interrupted eye-head gaze shifts for resettable integrator reset
2006, Brain Research Bulletin
Citation Excerpt :
Although not tested in circumstances identical to the herein simulated ones (i.e., when the line of sight shifts towards a distractor before its redirection to the “target”), this is true even when the line of sight shifts in the interval between presentation of a target and execution of a saccade towards it (e.g., “double-step” stimulation experiments [12]). The neural processes needed to account for the accuracy of saccades in double-step stimulation experiments are thought to be complete by the time commands exit the SC (reviewed in [43,26]) and are therefore beyond the scope of the present model. Suffices to say that a model that is consistent with subject performance and relies on signals indicative of eye displacement rather than eye position has been proposed for the SC in the form of the “vector subtraction hypothesis” [28,26].
The neural circuit responsible for saccadic eye movements is generally thought to resemble a closed loop controller. Several models of the saccadic system assume that the feedback signal of such a controller is an efference copy of “eye displacement”, a neural estimate of the distance already travelled by the eyes, provided by the so-called “resettable integrator” (RI). The speed, with which the RI is reset, is thought to be fast or instantaneous by some authors and gradual by others. To examine this issue, psychophysicists have taken advantage of the target-distractor paradigm. Subjects engaged in it, are asked to look to only one of two stimuli (the “target”) and not to a distractor presented in the diametrically opposite location and they often generate movement sequences in which a gaze shift towards the “distractor” is followed by a second gaze shift to the “target”. The fact that the second movement is not systematically erroneous even when very short time intervals (about 5 ms) separate it from the first movement has been used to question the verisimilitude of gradual RI reset. To explore this matter we used a saccade-generating network that relies on a RI coupled to a head controller and a model of the rotational vestibulo-ocular reflex. An analysis of the activation functions of model units provides disproof by counterexample: “targets” can be accurately acquired even when the RI of the saccadic burst generator is not reset at all after the end of the first, interrupted eye-head gaze shift to the distractor and prior to the second, complete eye-head gaze shift to the “target”.
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This paper describes a neural network model that directs saccades back to targets after they disappear and other saccades intervene. This is a simple example of knowing where something is after it is no longer visible and the observer has moved. These tasks require a short-term memory that can store continuous values of spatial location. The model was generated by training a neural network with a recurrently connected hidden layer to specify memory-guided saccades. The trained network maintains stored locations accurately for a few seconds. It uses a leaky integrator mechanism in which there is a slow decay of the stored value to a small number of fixed point attractors. Similar mechanisms have been used to model oculomotor integration (Cannon, S., Robinson, D., & Shamma, S. (1983). A proposed neural network for the integrator of the oculomotor system. Biological Cybernetics, 49, 127–136; Seung, H. (1998). Continuous attractors and oculomotor control. Neural Networks, 11, 1253–1258). The mechanism is robust to parameters such as the input and output format and the constraints in training. However, the receptive field properties of the hidden units do depend on these parameters. It was possible to find biologically plausible parameters that produced hidden unit behavior similar to that of real neurons involved in saccade memory. In particular, training the model to simultaneously represent the target location in both eye- and head-based reference frames produces units similar to neurons in parietal saccade areas.
The superior colliculus and eye movement control
1996, Current Opinion in Neurobiology
Saccade metrics are largely determined by command signals generated in the superior colliculus. Recent work has improved our knowledge of the highly complex axonal trees the disseminate these signals. It has also demonstrated that electrical stimulation of the superior colliculus evokes slow (drifts) as well as fast (saccades) eye movements and has provided detailed quantitative descriptions of their metrical properties. New biologically influenced models of the superior colliculus provide a detailed and realistic account of the discharge of tectal pre-saccadic neurons, the properties of evoked saccades and the ability of subjects to execute correct saccades in a variety of circumstances.
Web alert Neural control
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Modeling saccadic action selection: Cortical and basal ganglia signals coalesce in the superior colliculus
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Neural network simulations of the primate oculomotor system. II. Frames of reference

Abstract

Brain Res.

Brain Res.

Vision Res.

Vision Res.

Heavy metal intensification of DAB-based HRP reaction product

J. Histochem. Cytochem.

Visual and eye movement functions of the posterior parietal cortex

Annu. Rev. Neurosci.

Encoding of spatial location by posterior parietal neurons

Science

Eye movements in patients with absent voluntary horizontal gaze

Ann. Neurol.

Fine structure of primary afferent axon terminals of slowly adapting cutaneous receptors in the cat

Q. J. Exp. Physiol.

The coordination of eye, head and arm movements during reaching at a single visual target

Exp. Brain Res.

Oculomotor localization relies on a damped representation of saccadic eye displacement in human and nonhuman primates

Vis. Neurosci.

A neural network model of sensoritopic maps with predictive short-term memory properties

Early stages in a sensorinotor transformation

Behav. Brain Sci.

Parietal neurons encoding spatial locations in craniotopic coordinates

Exp. Brain Res.

In reaching, the task is to move the hand to a target

Behav. Brain Sci.

Tests of two models of the neural saccade generator: Saccadic eye movement deficits following ibotenic acid lesions of the nuclei raphe interpositus and prepositus hypoglossi in monkey

Saccadic eye movement deficits following ibotenic acid lesions of the nuclei raphe interpositus and prepositus hypoglossi in monkey

Acta Otolaryngol. (Stockh.)

Reticular control of vertical saccadic eye movements by mesencephalic burst neurons

J. Neurophysiol.

The efferent projections of the intestitial nucleus of Cajal in the squirrel monkey

Eur. J. Neurosci.

Neural model of adaptive hand-eye coordination for simple postures

Science

Gating of retinal transmission by afferent eye position and movement signals

Science

Ultrastructure of hair follicle afferent terminations in the spinal cord of the cat

J. Neurocytol.

Fine structure of primary axon terminals projecting from rapidly adapting mechanoreceptors of the toe and foot pads of the cat

Q. J. Exp. Physiol.

Properties of signals that determine the amplitude and direction of saccadic eye movements in monkeys

J. Neurophysiol.

Spatial control of arm movements

Exp. Brain Res.