Frames of reference for eye-head gaze shifts evoked during stimulation of the primate frontal eye fields

Abstract

Electrical microstimulation of gaze control structures as the superio\r colliculus (SC) produces gaze shifts defined in an eye-centered reference frame (Klier et al. 2001). In contrast, the supplementary eye fields (SEF) appear to encode gaze commands in multiple reference frames (Martinez-Trujillo et al. 2004; Park et al. 2006). Previous single-unit recording experiments in head-restrained monkeys (Russo and Bruce 1996) suggest that the frontal eye field (FEF) encodes the location of visual targets in an eye-centered reference frame. However, there is reason to suspect that the input code (revealed by unit recording) and the output code (probably revealed by stimulation) should not always employ the same reference frame (Smith and Crawford 2005). Currently it is not known if electrical stimulation of the FEF in head-free animals produces gaze shifts toward an eye, head, or space-fixed goal. We implanted two macaques with recording chambers over the FEF and search coils to measure eye and head rotations. Stimulation trains were delivered at 80 µA, 300 Hz, 200 ms, with gaze oriented at a variety of positions. Gaze shifts were evoked from 114 FEF sites in two monkeys (M1 n= 70, M2 n=44). Evoked gaze trajectories were mathematically rotated trajectories into three coordinate systems (eye/ head/space). Then we examined gaze convergence in each of these frames. The distribution of gaze end-points had the lowest amount of convergence to a common point when plotted in gaze coordinates (M1 = 4639.82°2, M2 = 2485.60°2). In contrast, gaze end-points had greater convergence when plotted in head (M1 =1277.95°2, M2 = 423.23°2) or eye (M1 = 423.2°2, M2 = 170.21°2) coordinates. This suggest that the FEF stimulation output is characterized by an intermediate trend between an eye-centered reference frame as observed in the SC (Klier et al. 2001) and a multiple reference frame code used in the SEF (Martinez-Trujillo et al. 2004).