The influence of future gaze orientation upon eye-head coupling during saccades

Abstract

Mammals with foveas (or analogous retinal specializations) frequently shift gaze without moving the head, and their behavior contrasts sharply with "afoveate" mammals, in which eye and head movements are strongly coupled. The ability to move the eyes without moving the head could reflect a gating mechanism that blocks a default eye-head synergy when an attempted head movement would be energetically wasteful. Based upon such considerations of efficiency, we predicted that for saccades to targets lying within the ocular motor range, the tendency to generate a head movement would depend upon a subject's expectations regarding future directions of gaze. We tested this hypothesis in two experiments with normal human subjects instructed to fixate sequences of lighted targets on a semicircular array. In the target direction experiment, we determined whether subjects were more likely to move the head during a small gaze shift if they expected that they would be momentarily required to make a second, larger shift in the same direction. Adding the onward-directed target increased significantly the distribution of final head positions (customary head orientation range, CHOR) observed during fixation of the primary target from 16.6+/-4.9 degrees to 25.2+/-7.8 degrees. The difference reflected an increase in the probability, and possibly the amplitude, of head movements. In the target duration experiment, we determined whether head movements were potentiated when subjects expected that gaze would be held in the vicinity of the target for a longer period of time. Prolonging fixation increased CHOR significantly from 53.7+/-18.8 degrees to 63.2+/-15.9 degrees. Larger head movements were evoked for any given target eccentricity, due to a narrowing in the gap between the x-intercepts of the head amplitude:target eccentricity relationship. The results are consistent with the idea that foveate mammals use knowledge of future gaze direction to influence the coupling of saccadic commands to premotor circuitry of the head. While the circuits ultimately mediating the coupling may lie within the brainstem, our results suggest that the cerebrum plays a supervisory role, since it is a likely seat of expectation regarding target behavior. Eye-head coupling may reflect separate gating and scaling mechanisms, and changes in head movement tendencies may reflect parametric modulation of either mechanism.

Countermanding Eye-Head Gaze Shifts in Humans: Marching Orders Are Delivered to the Head First

“…It is possible that this mechanism has evolved given the paramount importance of retinal stability for foveal vision or because of the sluggish biomechanics of the head. Alternatively, our results may testify to a brain stem mechanism that specifies the head movement trajectory before the gaze shifts begins to optimize the final position of the eyes within the head in different behavioral contexts (Crawford and Guitton 1997;Oommen et al 2004;Tweed et al 1998). It remains to be seen whether these results are specific for the oculomotor system or generalize to other movement systems such as reaching or eye-hand coordination.…”

Steering by Hearing: A Bat’s Acoustic Gaze Is Linked to Its Flight Motor Output by a Delayed, Adaptive Linear Law

“…It requires less energy to maneuver a small part of the body, such as the head or eye, than to change the orientation or direction of motion of the whole animal. By controlling sensory gaze through a part of the body that is light and independently movable, animals are able to conserve energy when redirecting gaze (Oommen et al, 2004). When an animal is not executing target-directed locomotion, therefore, one may expect the gaze direction to be uncoupled from locomotion direction, because the animal may be scanning the environment.…”

Variables Contributing to the Coordination of Rapid Eye/Head Gaze Shifts

“…Likewise, determination of target in space (T ) requires the availability of static head (H ) and eye (E) position signals. Note that this is a logic diagram that is not intended to signify operation by linear systems It is clear from experimental evidence that quite different relationships between the stimulus and response can occur for different subjects or even for the same subject in different contexts (Oommen et al (2004); Stahl (1999); Herst et al (2001); Goldring et al (1987); Fuller (1992a,b)). What we are looking for are fundamental characteristics of the control structure that do not vary between subjects or contexts.…”

“…Fuller (1992a,b) and Stahl (1999Stahl ( , 2001 have addressed this issue explicitly, showing that different subjects can exhibit radically different head movement tendencies, both in terms of the amplitude of the head movement and the likelihood of incorporating any head movement at all. Moreover, even the same subject can alter this basic strategy in order to better address the demands of a specific task (Oommen et al 2004). Nevertheless, this function has been thoroughly investigated experimentally (Guitton and Volle 1987;Fuller 1992a;Stahl 1999;Goldring et al 1987), and many characteristics of the response can be agreed upon (Fig.…”

“…There are certainly other contextual factors influencing the gaze shift response, such as the surroundings, the mental and physical states of the subject, the nature of the task (Epelboim et al 1997), or the expected locations of future targets (Oommen et al 2004). We will assume, however, that within a particular experimental situation the context either remains constant or changes in ways that do not affect the measured responses.…”