Perturbing gaze shifts reveals new visuo-motor encoding mechanisms

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Humans are skilled at making rapid, accurate movements that involve functionally coupled body segments that move simultaneously. How the brain orchestrates such complex movements has been a major focus of my lab and, as an experimental model, we have studied coordinated eye + head movements that routinely generate rapid orienting movements of the visual axis called gaze saccades. ***The midbrain's superior colliculus (SC) is a critical structure in gaze control. The classic hypothesis is that the SC contains a motor map which drives rapid (saccadic) gaze shifts according to a coding scheme wherein one-site on the map encodes one gaze shift vector. We call this the “one-site, one- saccade” hypothesis. We have preliminary evidence that this hypothesis fails when one looks about the environment using a sequence of rapid gaze saccades separated by periods of fixation. In this context the SC encodes the overall displacement not individual saccades. This critical break with the dominant hypothesis of SC function needs to be verified which we propose to do here. If we confirm failure then this will call for a critical re-evaluation of current models of how the brain controls how we look about the environment. ***The objective of looking about the environment is obviously to see'. This simple day to day term hides an extraordinarily complex ensemble of brain functions that underlie perception. For one thing we need to link vision with movements of the eyes. Such a link is necessary because: 1) our visual world appears stable across saccadic gaze shifts despite a perceived object changing position on the retina as we make saccades 3-5 times/sec; and 2) a spatially-fixed locus of attention occupies a different position on the retina after each saccade but must internally be perceived as spatially immobile. *** ***Interestingly, the brain's visual system is organized in visual maps in a manner analogous to the SC's motor map. Thus, one site on a visual map encodes one small location in visual space. This is called the “one-site, one-receptive-field” hypothesis. Similar to the gaze motor system there is evidence that this hypothesis can fail. Indeed, a neuron in a visual map can respond to a visual stimulus presented anywhere in the visual world depending on the direction and amplitude of the upcoming saccade. Thus one site on a visual map can encode an infinite number of spatial positions! This radical break with classic thinking needs to be understood to understand vision. We plan to do this here by studying how visual neurons respond to visual stimuli when the intended gaze saccade is perturbed. ***Together, the key principles of brain organization in the motor and visual system can be referred to as the “one-site, one-function” hypotheses. We have models of how these systems work but when they don't work, it is critical to understand why if we are to understand brain function and how we see when we scan our environment.**