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From Vision to Action: Sensory-Motor Processing for Eye Movements
Summary: Stephen Lisberger studies the brain mechanisms that transform the motion of objects in the world, or our own motion, into accurate eye movements.
We move our eyes to facilitate excellent vision. The propensity of things to move poses a major threat to excellent vision, because it tends to cause images to move across the retina, degrading visual acuity. One source of image motion comes from the motion of objects through the world. Smooth pursuit eye movements allow us to track the visual stimuli that are created when objects move. A second source of image motion is created by our own head turns, which could drag our eyes along and thus cause images to smear across the retina. The vestibulo-ocular reflex keeps the position of gaze stable in space by generating eye movements that compensate for head motion. Our laboratory studies how these two kinds of eye movement are generated by the intact brain in behaving primates.
Smooth Pursuit Eye Movements
The basic anatomical circuits for pursuit eye movements are known. Visual inputs arise in the primary visual cortex. They are transmitted through the middle temporal visual area (MT) to the parietal and frontal cortex and, in parallel, from these three cortical areas to the brain stem and cerebellum for the assembly of motor commands. We are asking how the sensory signals created by moving visual stimuli are processed and transformed to create neural signals suitable to guide accurate smooth pursuit eye movements.
To analyze how moving images are processed in the visual parts of the brain, we have asked how signals related to target speed are transformed as they are transmitted from the extrastriate motion area MT to the pursuit system. As others have reported, the firing rate of MT neurons is tuned for the speed of moving stimuli: they give the strongest response for a given speed and weaker responses for either faster or slower speeds.
We have been analyzing the variation in neural responses and behavior as a way to understand how visual signals in MT are converted into commands for smooth pursuit eye movements. Our research has revealed a surprising and reliable structure in the movement-by-movement variation in the pursuit evoked by repetition of the same target motion. We have formed the hypothesis (based on the properties of the variation) that correlated noise in the sensory system leads to errors in estimating target speed and direction, and the motor system tracks those erroneous estimates loyally and reliably.
We tested our hypothesis through recordings from the floccular complex of the cerebellum, which is strategically located three synapses downstream from the sensory input in area MT and two synapses upstream from extraocular motor neurons. We found remarkably strong movement-by-movement covariation in the firing of the cerebellar Purkinje cells and the evoked pursuit behavior: variation in eye movement accounts for more than 35 percent of the variation in neural firing. The correlations would be expected if all Purkinje cells are receiving the same input from the sensory system and therefore are highly correlated with each other and the behavior they drive. The same situation pertains for a part of the motor cortex that is important for pursuit eye movements, the smooth eye movement region of the frontal eye fields. We conclude that variation in pursuit arises upstream from the cerebellum and the motor cortex.
Because the neural circuit for smooth pursuit includes many areas of the cerebral cortex as well as the cerebellum, pursuit provides an excellent system for understanding how we learn motor skills. Two recent experiments have revealed key links in the neural process of learning. First, we have found the microstimulation in visual area MT, but not in the smooth eye movement region of the frontal eye fields or the cerebellum, can substitute for changes in the direction of target motion and cause precisely timed learning that mimics the learning induced by real visual stimuli. Second, analysis of the learned responses of cerebellar Purkinje cells has provided strong evidence that plasticity in the cerebellar cortex plays a causal role in pursuit learning. Purkinje cells receive two kinds of inputs that are very different in their anatomy and physiology. We found that the occurrence during one movement of the rare "climbing fiber inputs" is linked to a depression during the next movement of the firing rate of the conventional and frequent "simple spikes." Our observation provides strong support for the popular theory that climbing fiber inputs instruct learning in Purkinje cells, but with new evidence that this mechanism operates during learning in awake animals, and on a very fast timescale.
Vestibulo-ocular Reflex
In primates, the performance of the vestibulo-ocular reflex (VOR) is normally nearly ideal. During rotatory head turns in darkness, the compensatory eye movements of the VOR are opposite in direction and nearly equal in amplitude to head turns. The VOR attains and maintains this excellent performance with a learning mechanism that is intact throughout life. In the laboratory, we study learning by fitting monkeys with goggles that either double or quarter the size of their visual inputs. When, for example, a monkey is wearing the doubling spectacles, visual scenes will be stabilized only if head turns in one direction are accompanied by eye rotations in the opposite direction at twice the usual speed. Initially, the VOR retains its normal response amplitude. Over several days, however, the persistent association of image motion and head turns causes the size of the VOR to increase gradually. At the end of the learning, head turns in darkness evoke an eye movement of twice the normal size.
We are exploring a number of hypotheses suggested by our earlier finding that learning occurs at specific sites in the cerebellar cortex and the vestibular nucleus. In an attempt to analyze system function by finding its limits, we have found that learning induced during a monkey's free head turns has an effect on the responses of the VOR in the dark for sinusoidal head motions at frequencies up to 25 Hz, but not for higher frequencies. Recordings from vestibular afferents and extraocular motor neurons have provided precise predictions about the transformations done in the neural pathways for the VOR. We can model the eye movements across the full frequency range if we assume that the VOR is mediated by separate modifiable and unmodified pathways that interpose time delays of 9 and 2 ms, respectively. Recordings from interneurons in the brain stem reveal two groups that conform well to the model's predictions for the responses within the modified and unmodified pathways. Our attention, therefore, is focused on mechanisms of plasticity that could operate on the interneurons in the modified brain stem pathway, as well as at the site in the cerebellar cortex that plays a causal role in pursuit learning.
Our work on learning in pursuit and the VOR has led to an understanding that motor learning is a system property. Behavioral learning appears, at least superficially, to be monolithic, but it is mediated by neural changes that occur at several sites in the brain and by multiple mechanisms of cellular modification that operate over a range of times—from seconds to days. In both movement systems, the cerebellum plays an important role, and sites of learning seem to exist both in the cerebellar cortex and the deep cerebellar nuclei.
This work was supported in part by the National Eye Institute and the National Institute of Mental Health.
Last updated May 08, 2009
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