Introduction
Our nervous system labors to represent the rich arrays of percepts and actions in support of meaningful goal-driven behavior. The superior colliculus (SC), a key node in a distributed oculomotor network, mediates orienting behaviors (e.g., gaze shifts) designed to streamline this perception-action cycle. The SC is a laminar structure containing two tightly registered eye-centered topographic maps: a visual map in the superficial layer, and a motor map in the intermediate and deep layers representing the angle and amplitude of saccades (\citealt*{Wurtz_1980}; \citealt*{Sparks1986}; \citealt*{Sparks1999}; \citealt*{Gandhi_2011}). Classically, the motor map is subdivided into a rostral zone containing neurons that actively maintain fixation and a caudal zone whose neurons mediate the generation of saccadic eye-movements. These zones form a push-pull mechanism for mediating orienting behaviors (\citealt*{Munoz1992}; \citealt*{Munoz1993}; \citealt*{8410158}). However, two recent lines of evidence challenge this motor-centric model of SC function. (1) Pharmacological inactivation of the macaque SC motor map induces a form of visual neglect akin to extinction, but does not cause paresis or anopsia (\citealt*{McPeek2004}; \citealt*{Lovejoy2010}; \citealt*{Nummela_2011};\citealt*{Z_non_2012}). (2) Neural activity in the cat and macaque SC motor map represents a more abstract location of a behavioral goal, independent of the sequence of eye movements required for acquiring the target (\citealt*{Bergeron_2003}; \citealt*{Keller1996}; \citealt*{Freedman1997}). Therefore, the functional role of the SC cannot be explained simply in terms of visual input or motor output. Instead, the SC may integrate sensory salience and behavioral relevance signals computed throughout the brain into a common topographical organization, acting as a staging area for organizing flexible and goal-oriented behavior into a prioritized map of space (\citealt*{16843702}). Here we sought to explore the extent to which persistent delay-period activity measured in the human SC using functional imaging techniques reflects spatially specific representations of priority apart from visual input and motor output. First, we show that we can derive the detailed retinotopic organization of the human SC using the population receptive field (pRF) model (\citealt*{Dumoulin_2008}).
Methods
Subjects. 4 subjects participated in the study (ages 27-49; 4 male). One subject was left-handed. The subjects were in good health with no history of psychiatric or neurological disorders, had normal or corrected-to-normal visual acuity, and gave informed written consent. The study was approved by the New York University Committee on Activities Involving Human Subjects and the New York University Abu Dhabi Internal Review Board. All subjects participated in three scanning sessions encompassing three different functional experiments.
Display and response hardware. The stimuli were generated on a STIM_PC computer using MATLAB software (The MathWorks) and Psychophysics Toolbox 3 functions (\citealt*{Brainard_1997}; \citealt*{Pelli_1997}). Stimuli were presented using a PROPixx DLP LED projector (VPixx, Saint-Bruno, QC, Canada) located outside the scanner room and projected through a waveguide and onto a translucent screen located at the end of the scanner bore. Subjects viewed the screen at a total viewing distance of 64 cm through a mirror attached to the head coil. The display subtended approximately 32˚ of visual angle horizontally vertically. A trigger pulse from the scanner synchronized the onsets of stimulus presentation and image acquisition. EYETRACKING
Visual stimuli and procedure. The pRF mapping stimuli consisted of a checkerboard-patterned bar whose elements reversed contrast with a full-cycle frequency of 8 Hz (Figure 1A). The bar subtended 8˚ of visual angle across its width and extended beyond the boundaries of the screen along its length. During a single run, the bar appeared at two orientations (0˚ and 90˚) and transited across the screen perpendicular to the bar orientation and passed through central fixation. Thus, each bar consisted of four 30 s bar sweeps with 12 s mean-luminance blank periods at the beginning and end of each run. Subjects performed a demanding fixation task where they responded via buttonbox as to which of four colors (red, green, blue, yellow) the fixation was set every 1.5 s. To measure the spatial representation for remember locations in the visual field, we used a delayed oculomotor response task with participants responding with eye movements, either towards or away from a visual sample. Each trial commenced with the brief (300 ms) presentation of a visual sample, followed by a 10.5 s delay-period while subjects maintained the sample location and hold central fixation (Figure 1B). After the delay, we presented a randomly located visual stimulus, cueing the subject to execute a visually-guided saccade (VGS) to this location and then to immediately executed a memory-guided saccade (MGS) to the remembered sampled location. Feedback of the true MGS location is given for 500 ms, whereafter the subject returns to central fixation during a 9.8 s inter-trial interval (ITI). The entire trial duration was 22.5 s (15 volume acquisitions), and each run was comprised of 16 trials with two repetitions at each of the eight target locations. The locations of the samples and memory locations were evenly space from 22.5 to 337.5˚ in 45˚ intervals of polar angle and presented at 10˚ eccentricity. Sample locations were were jittered by ±10˚ tangentially and ±1˚ eccentrically from trial to trial. The location of the memory guided saccade (MGS) was always the same as the sample location during pro-saccade trials but was rotated by 180˚ of polar angle for anti-saccade trials. The location of the visually guided saccade for each trial was drawn from a uniform random distribution spanning 360˚, ensuring that the VGS was independent of the sample and MGS locations (Figure 1C).