The frontal eye field (FEF) is a region of the primate prefrontal cortex that is central to eye-movement generation and target selection. It has been shown that neurons in this area encode commands for saccadic eye movements. Furthermore, it has been suggested that the FEF may be involved in the generation of gaze commands for the eye and the head. To test this suggestion, we systematically stimulated (with pulses of 300 Hz frequency, 200 ms duration, 30-100 μA intensity) the FEF of two macaques, with the head unrestrained, while recording three-dimensional (3D) eye and head rotations. In a total of 95 sites, the stimulation consistently elicited gaze-orienting movements ranging in amplitude from 2 to 172°, directed contralateral to the stimulation site, and with variable vertical components. These movements were typically a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between the stimulation-evoked movements and gaze shifts voluntarily made by the animal. The kinematics of the stimulation-evoked movements (i.e., their spatiotemporal properties, their velocity-amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were very similar to those of natural gaze shifts. Moreover, they obeyed the same 3D constraints as the natural gaze shifts (i.e., modified Listing's law for eye-in-head movements). As in natural gaze shifts, saccade and vestibuloocular reflex torsion during stimulation-evoked movements were coordinated so that at the end of the head movement the eye-in-head ended up in Listing's plane. In summary, movements evoked by stimulation of the FEF closely resembled those of naturally occurring eye-head gaze shifts. Thus we conclude that the FEF explicitly encodes gaze commands and that the kinematic aspects of eye-head coordination are likely specified by downstream mechanisms.
asymmetry in memory-guided pointing during single-pulse transcranial magnetic stimulation of human parietal cortex. J Neurophysiol 96: 3016 -3027, 2006. First published September 27, 2006 doi:10.1152/jn.00411.2006. Dorsal posterior parietal cortex (PPC) has been implicated through single-unit recordings, neuroimaging data, and studies of brain-damaged humans in the spatial guidance of reaching and pointing movements. The present study examines the causal effect of single-pulse transcranial magnetic stimulation (TMS) over the left and right dorsal posterior parietal cortex during a memory-guided "reach-to-touch" movement task in six human subjects. Stimulation of the left parietal hemisphere significantly increased endpoint variability, independent of visual field, with no horizontal bias. In contrast, right parietal stimulation did not increase variability, but instead produced a significantly systematic leftward directional shift in pointing (contralateral to stimulation site) in both visual fields. Furthermore, the same lateralized pattern persisted with left-hand movement, suggesting that these aspects of parietal control of pointing movements are spatially fixed. To test whether the right parietal TMS shift occurs in visual or motor coordinates, we trained subjects to point correctly to optically reversed peripheral targets, viewed through a left-right Dove reversing prism. After prism adaptation, the horizontal pointing direction for a given visual target reversed, but the direction of shift during right parietal TMS did not reverse. Taken together, these data suggest that induction of a focal current reveals a hemispheric asymmetry in the early stages of the putative spatial processing in PPC. These results also suggest that a brief TMS pulse modifies the output of the right PPC in motor coordinates downstream from the adapted visuomotor reversal, rather than modifying the upstream visual coordinates of the memory representation.
Humans adopt very different head movement strategies for different gaze behaviors, for example, when playing sports versus watching sports on television. Such strategy switching appears to depend on both context and expectation of future gaze positions. Here, we explored the neural mechanisms for such behaviors by training three monkeys to make head-unrestrained gaze shifts toward eccentric radial targets. A randomized color cue provided predictive information about whether that target would be followed by either a return gaze shift to center or another, more eccentric gaze shift, but otherwise animals were allowed to develop their own eye-head coordination strategy. In the first two animals we then stimulated the frontal eye fields (FEF) in conjunction with the color cue, and in the third animal we recorded from neurons in the superior colliculus (SC). Our results show that 1) monkeys can optimize eye-head coordination strategies from trial to trial, based on learned associations between color cues and future gaze sequences, 2) these cue-dependent coordination strategies were preserved in gaze saccades evoked during electrical stimulation of the FEF, and 3) two types of SC responses (the saccade burst and a more prolonged response related to head movement) modulated with these cue-dependent strategies, although only one (the saccade burst) varied in a predictive fashion. These data show that from one moment to the next, the brain can use contextual sensory cues to set up internal "coordination states" that convert fixed cortical gaze commands into the brain stem signals required for predictive head motion.
The frontal eye field (FEF), in the prefrontal cortex, participates in the transformation of visual signals into saccade motor commands and in eye-head gaze control. The FEF is thought to show eye-fixed visual codes in head-restrained monkeys, but it is not known how it transforms these inputs into spatial codes for head-unrestrained gaze commands. Here, we tested if the FEF influences desired gaze commands within a simple eye-fixed frame, like the superior colliculus (SC), or in more complex egocentric frames like the supplementary eye fields (SEFs). We electrically stimulated 95 FEF sites in two head-unrestrained monkeys to evoke 3D eye-head gaze shifts and then mathematically rotated these trajectories into various reference frames. In theory, each stimulation site should specify a specific spatial goal when the evoked gaze shifts are plotted in the appropriate frame. We found that these motor output frames varied site by site, mainly within the eye-to-head frame continuum. Thus, consistent with the intermediate placement of the FEF within the high-level circuits for gaze control, its stimulation-evoked output showed an intermediate trend between the multiple reference frame codes observed in SEF-evoked gaze shifts and the simpler eye-fixed reference frame observed in SC-evoked movements. These results suggest that, although the SC, FEF and SEF carry eye-fixed information at the level of their unit response fields, this information is transformed differently in their output projections to the eye and head controllers.
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