Multiple spatial representations interact to increase reach accuracy when coordinating a saccade with a reach

Abstract

Reaching is an essential behavior that allows primates to interact with the environment. Precise reaching to visual targets depends on our ability to localize and foveate the target. Despite this, how the saccade system contributes to improvements in reach accuracy remains poorly understood. To assess spatial contributions of eye movements to reach accuracy, we performed a series of behavioral psychophysics experiments in nonhuman primates (). We found that a coordinated saccade with a reach to a remembered target location increases reach accuracy without target foveation. The improvement in reach accuracy was similar to that obtained when the subject had visual information about the location of the current target in the visual periphery and executed the reach while maintaining central fixation. Moreover, we found that the increase in reach accuracy elicited by a coordinated movement involved a spatial coupling mechanism between the saccade and reach movements. We observed significant correlations between the saccade and reach errors for coordinated movements. In contrast, when the eye and arm movements were made to targets in different spatial locations, the magnitude of the error and the degree of correlation between the saccade and reach direction were determined by the spatial location of the eye and the hand targets. Hence, we propose that coordinated movements improve reach accuracy without target foveation due to spatial coupling between the reach and saccade systems. Spatial coupling could arise from a neural mechanism for coordinated visual behavior that involves interacting spatial representations. How visual spatial representations guiding reach movements involve coordinated saccadic eye movements is unknown. Temporal coupling between the reach and saccade system during coordinated movements improves reach performance. However, the role of spatial coupling is unclear. Using behavioral psychophysics, we found that spatial coupling increases reach accuracy in addition to temporal coupling and visual acuity. These results suggest that a spatial mechanism to couple the reach and saccade systems increases the accuracy of coordinated movements.

Eye-head-hand coordination during visually guided reaches in head-unrestrained macaques

“…Reaches tend to decrease saccade latency and increase saccade velocity in both macaques and humans (Sailer et al 2016;Snyder et al 2002). Although macaques can be trained to decouple gaze fixation from reach direction (Hawkins et al 2013), accuracy and temporal coupling are higher when animals are allowed to coordinate the eye and hand toward a common goal (Vazquez et al 2017). In general, the kinematic rules for eye-hand coordination in macaques are similar to those observed in the more frequently studied human eye-hand coordination system (Van Donkelaar and Staub 2000;Henriques et al 1998;Prablanc et al 1979).…”

“…Studies of eye-hand coordination in macaques are somewhat less common than either studies of eye-head coordination in macaques or eye-hand coordination in the human. These can be grouped into studies where gaze fixation and hand motion were confined to a common twodimensional plane (Dean et al 2011;Pesaran et al 2006;Snyder et al 2002;Song and McPeek 2009;Vazquez et al 2017), versus those where animals performed a three-dimensional reach in depth (Battaglia-Mayer A Genovesio A, et al 2001;Ferraina et al 1997;Hawkins et al 2013;Marconi B Battaglia-Mayer A, et al 2001;Marzocchi et al 2008). Macaques will generally saccade in advance to capture the reach target (Pelz and Canosa 2001;Song and McPeek 2009).…”

Eye movement training is most effective when it involves a task-relevant sensorimotor decision

“…Eye movements are usually made spontaneously when observers engage in visually-guided manual tasks such as reaching, grasping, pointing, or hitting. Eye and hand movements are spatially and temporally coordinated: gaze leads the hand by up to 1 s (Ballard, Hayhoe, Li, & Whitehead, 1992;Smeets et al, 1996;Sailer, Flanagan, & Johansson, 2005;Land, 2006), and gaze locations are anchored to future contact points on the target, indicating strong spatial coupling (van Donkelaar, Lee, & Gellman, 1994;Neggers & Bekkering, 2000;Gribble, Everling, Ford, & Mattar, 2002;Brenner & Smeets, 2011;Cesqui, Mezzetti, Lacquaniti, & d'Avella, 2015;Vazquez, Federici, & Pesaran, 2017). Many of these studies have focused on the saccade-toreach relationship.…”

Contrasting effects of exogenous cueing on saccades and reaches

“…Numerous studies have demonstrated that simultaneous eye and arm movements are coordinated both spatially and temporally, suggesting a shared representation for planning movements of the eyes and the arms (Carey, 2000;Crawford, Medendorp, & Marotta, 2004;Dean, Marti, Tsui, Rinzel, & Pesaran, 2011;Fischer & Rogal, 1986;Fisk & Goodale, 1985;Frens & Erkelens, 1991;Gribble, Everling, Ford, & Mattar, 2002;Herman, Herman, & Maulucci, 1981;Jeannerod, 1988;Land & Hayhoe, 2001;Neggers & Bekkering, 2002;Prablanc, Echallier, Komilis, & Jeannerod, 1979;Sailer, Eggert, Ditterich, & Straube, 2000;Song & McPeek, 2009). The shared representation implies that motor commands for the eyes can also influence the arm, and vice versa (Lee, Poizner, Corcos, & Henriques, 2014;Sailer, Eggert, Ditterich, & Straube, 2002;Soechting, Engel, & Flanders, 2001;Vazquez, Federici, & Pesaran, 2017). There are other studies that show little or no correlations between the timings (onsets) of eye and arm movements, suggesting independent representations for the different effectors (Guitton & Volle, 1987;Tweed, Glenn, & Vilis, 1995;Vercher, Magenes, Prablanc, & Gauthier, 1994).…”