Learning and Maintaining Saccadic Accuracy: A Model of Brainstem–Cerebellar Interactions

Abstract

Saccadic accuracy requires that the control signal sent to the motor neurons must be the right size to bring the fovea to the target, whatever the initial position of the eyes (and corresponding state of the eye muscles). Clinical and experimental evidence indicates that the basic machinery for generating saccadic eye movements, located in the brainstem, is not accurate: learning to make accurate saccades requires cerebellar circuitry located in the posterior vermis and fastigial nucleus. How do these two circuits interact to achieve adaptive control of saccades? A model of this interaction is described, based on Kawato's principle of feedback-error-learning. Its three components were (1) a simple controller with no knowledge of initial eye position, corresponding to the superior colliculus; (2) Robinson's internal feedback model of the saccadic burst generator, corresponding to preoculomotor areas in the brain-stem; and (3) Albus's Cerebellar Model Arithmetic Computer (CMK), a neural net model of the cerebellum. The connections between these components were (I) the simple feedback controller passed a (usually inaccurate) command to the pulse generator, and (2) a copy of this command to the CMAC; (3) the CMAC combined the copy with information about initial eye position to (4) alter the gain on the pulse generator's internal feedback loop, thereby adjusting the size of burst sent to the motor neurons. (5) If the saccade were inaccurate, an error signal from the feedback controller adjusted the weights in the CMAC. It was proposed that connection (2) corresponds to the mossy fiber projection from superior colliculus to oculomotor vermis via the nucleus reticularis tegmenti pontis, and connection (5) to the climbing fiber projection from superior colliculus to the oculomotor vermis via the inferior olive. Plausible initialization values were chosen so that the system produced hypometric saccades (as do human infants) at the start of learning, and position-dependent hypermetric saccades when the cerebellum was removed. Simulations for horizontal eye movements showed that accurate saccades from any starting position could be learned rapidly, even if the error signal conveyed only whether the initial saccade were too large or too small. In subsequent tests the model adapted realistically both to simulated weakening of the eye muscles, and to intrasaccadic displacement of the target, thereby mimicking saccadic plasticity in adults. The architecture of the model may therefore offer a functional explanation of hitherto mysterious tectocerebellar projections, and a framework for investigating in greater detail how the cerebellum adaptively controls saccadic accuracy.

Learning Signals from the Superior Colliculus for Adaptation of Saccadic Eye Movements in the Monkey

“…The SC deeper layers also have a direct projection to subnucleus b of the medial accessory nucleus of the inferior olive, which houses neurons that send axons to the oculomotor vermis (Frankfurter et al, 1976;Yamada and Noda, 1987). This tecto-olivo-cerebellar pathway has been postulated to transmit a learning signal in modeling studies (Dean et al, 1994;Fujita, 2005) but its function remains to be defined. Recent recording studies have provided strong support for the olivary relay of learning signals (Soetedjo and Fuchs, 2006;Soetedjo et al, 2008).…”

Discharge of Monkey Nucleus Reticularis Tegmenti Pontis Neurons Changes During Saccade Adaptation

“…For example, in some models, a pontine nucleus, either the NRTP (Dean et al 1994) or the dorsolateral pontine nucleus (Schweighofer et al 1996), simply serves as a passive relay for a saccadic command to the OMV. In another popular model (Quaia et al 1999), there is no pontine relay nucleus at all.…”

A simple system for monitoring the timing of infant gaze to stimuli at specific locations

“…Human newborns make eye movements that are spatially coordinated with the locus of a sound (Butterworth & Castillo, 1976;Wertheimer, 1961) and that track a slowly moving target (Kremenitzer, Vaughan, Kurtzberg, & Dowling, 1979).1 Detailed analyses of infant eye movements during the 1st year provide data that are relevant for theoretical accounts of the organization of visual activity (see, e.g., Bronson, 1990bBronson, , 1991Bronson, , 1994Bronson, , 1997Hainline, Harris, & Krinsky, 1990;Haith, 1980;Shea & Aslin, 1990), the development ofthe object concept (see, e.g., Bremner, 1985;Moore, Borton, & Darby, 1978), the formation of expectations (see, e.g., Haith, Wentworth, & Canfield, 1993;Johnson, Posner, & Rothbart, 1991, and the organization ofneural development (see, e.g., Dean, Mayhew, & Langdon, 1994;Johnson, 1990).…”