Electrical Stimulation of the Frontal Eye Field in a Monkey Produces Combined Eye and Head Movements

Abstract

The frontal eye field (FEF), an area in the primate frontal lobe, has long been considered important for the production of eye movements. Past studies have evoked saccade-like movements from the FEF using electrical stimulation in animals that were not allowed to move their heads. Using electrical stimulation in two monkeys that were free to move their heads, we have found that the FEF produces gaze shifts that are composed of both eye and head movements. Repeated stimulation at a site evoked gaze shifts of roughly constant amplitude. However, that gaze shift could be accomplished with varied amounts of head and eye movements, depending on their (head and eye) respective starting positions. This evidence suggests that the FEF controls visually orienting movements using both eye and head rotations rather than just shifting the eyes as previously thought.

Dissociation of Eye and Head Components of Gaze Shifts by Stimulation of the Omnipause Neuron Region

“…Evidence supporting the notion of a head-movement command, not necessarily associated with a gaze shift, comes from neural recordings in the superior colliculus , central mesencephalic reticular formation (Pathmanathan et al 2006a,b), microstimulation of the frontal and supplementary eye fields (Chen 2006;Chen and Walton 2005), and adaptation of eye-head coordination in the context of a limited visual field (Constantin et al 2004). Neural signals encoding a desired gaze-displacement command have been proposed to exist at the level of the superior colliculus (Freedman and Sparks 1997a;Freedman et al 1996;Klier et al 2001;Munoz et al 1991), frontal eye field (Guitton and Mandl 1978;Knight and Fuchs 2007;Tu and Keating 2000;but see Chen 2006 for an alternative hypothesis), and supplementary eye field (Chen and Walton 2005;Martinez-Trujillo et al 2003). The ⌬G d command, perhaps after some processing that incorporates the effect of the eye position in the orbits and the location of the stimulus (Freedman 2001), adds to the neck muscle drive at the level of the pontine burst generator (BG).…”

Differential Influence of Attention on Gaze and Head Movements

“…These include the frontal eye fields (Chen 2006;Elsley et al 2007;Knight and Fuchs 2007;Monteon et al 2005;Tu and Keating 2000;van der Steen et al 1986), the supplementary eye fields (Chen and Walton 2005;MartinezTrujillo et al 2003MartinezTrujillo et al , 2004, and the superior colliculus (Freedman and Sparks 1997a;Freedman et al 1996;Klier et al 2001;Martinez-Trujillo et al 2003;Walton et al 2007Walton et al , 2008. Previous studies have provided evidence in support of a single gaze controller that programs both the eye and head components (Galiana and Guitton 1992;Guitton 1992;Guitton et al 2003;Lefèvre and Galiana 1992;Sparks et al 2001).…”

“…Since the head movement system is not gated by omnipause neurons (OPNs) (Gandhi and Sparks 2007), as is the case for saccades (Keller 1974(Keller , 1977Luschei and Fuchs 1972), this neck muscle response is believed to reflect the attentional cueing effect of the exogenous cue. The lack of inhibition by OPNs might also cause the observation that movement decisions are generally reflected first in neck muscle activity, followed later by eye movements, as has been observed in a saccade countermanding paradigm (Corneil and Elsley 2005) or with frontal eye field (FEF) or superior colliculus (SC) microstimulation (Chen 2006;Elsley et al 2007;Tu and Keating 2000). Despite these recent electrophysiological insights into the role of attention on head movements in gaze saccades, it remains largely unexplored how attention influences the timing of the head drive during combined eye-head gaze shifts.…”

Eye, Head, and Body Coordination During Large Gaze Shifts in Rhesus Monkeys: Movement Kinematics and the Influence of Posture

“…Electrical stimulation of the superior colliculus (SC) (reviewed in Sparks 1999) evokes coordinated eye-head gaze shifts that are kinematically indistinguishable from natural gaze shifts; they are characterized by the same velocity relationships and the relative amplitudes of the eye and head contributions depend on eye position at stimulation onset. Similarly, stimulation of the supplementary eye fields (SEFs) (Martinez-Trujillo et al 2003, 2005 and frontal eye fields (FEFs) (Monteon et al 2005;Tu and Keating 2000) can evoke combined movements of the eye and the head that are similar to natural gaze shifts. These findings have been taken as evidence that each of these structures play an important role in planning and/or controlling the head as well as the saccadic components of gaze shifts.…”