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Testing animal models of human oculomotor control with neuroimaging

We know more about the primate oculomotor system than any other motor system. From numerous studies that have measured electrical activity in single neurons, applied electrical microstimulation, characterized the behavioral sequelae of lesions, and mapped the afferent and efferent connections in oculomotor areas, exquisite animal models of human oculomotor control have evolved. In this chapter, I review studies that have begun to test these animal models in humans using neuroimaging techniques. I hope to highlight the importance of this form of translational research by describing several successes involving our understanding of the roles of the frontal and parietal cortex in saccade control. Moreover, I will discuss several problematic methodological issues that have proven challenging to our efforts of translation. The primate oculomotor network-The superior colliculus (SC) is a phylogenetically ancient midbrain structure whose neural activity is synonymous with the conversion of sensory signals to commands used to control gaze (D.(see also chapter by White and Munoz in the current volume). Indeed, there are both visual and motor topographic maps within the SC's laminated intermediate and superficial layers, respectively. The SC is thought to reflect a convergence point where a variety of afferent cortical and subcortical signals are weighed, averaged, and compared to produce saccade commands The SC is particularly well positioned anatomically in the primate brain to integrate such signals (May, 2006). Importantly, in addition to visual signals from striate cortex that target the SC, a number of other cortical areas are known to influence neural activity in the SC. The frontal cortex contains over four distinct areas whose monosynaptic connections with the SC are thought to influence gaze programming. David Ferrier first reported that electrical stimulation of the monkey dorsal frontal cortex evoked contraversive eye movements (Ferrier, 1886). A dorsolateral portion of the large region he described has become known as the frontal eye field (FEF). With microstimulation, the FEF has been more precisely localized to the anterior bank of the arcuate sulcus in Brodmann's area 8 saccades can be elicited with very low current thresholds (< 50 µA). However, the boundaries of the functionally defined monkey FEF remain unclear and may extend into Brodmann's area 6 and Walker's area 45 The FEF contains an organized map of mostly contralateral visual space defined in eye-centered coordinates (Bruce, et al., 1985; Sommer & Wurtz, 2000). A rough progression of cells that code for large to short amplitude saccades can be …