It's in the eyes: Planning precise manual actions before execution

Abstract

It is well-known that our eyes typically fixate those objects in a scene, with which interactions are about to unfold. During manual interactions, our eyes usually anticipate the next subgoal and thus serve top-down, goal-driven information extraction requirements, probably driven by a schema-based task representation. On the other hand, motor control research concerning object manipulations has extensively demonstrated how grasping choices are often influenced by deeper considerations about the final goal of manual interactions. Here we show that also these deeper considerations are reflected in early eye fixation behavior, significantly before the hand makes contact with the object. In this study, subjects were asked to either pretend to drink out of the presented object or to hand it over to the experimenter. The objects were presented upright or upside down, thus affording a thumb-up (prone) or a thumb-down (supine) grasp. Eye fixation data show a clear anticipatory preference for the region where the index finger is going to be placed. Indeed, fixations highly correlate with the final index finger position, thus subserving the planning of the actual manual action. Moreover, eye fixations reveal several orders of manual planning: Fixation distributions do not only depend on the object orientation but also on the interaction task. These results suggest a fully embodied, bidirectional sensorimotor coupling of eye-hand coordination: The eyes help in planning and determining the actual manual object interaction, considering where to grasp the presented object in the light of the orientation and type of the presented object and the actual manual task to be accomplished with the object.

The Intersection between Ocular and Manual Motor Control: Eye–Hand Coordination in Acquired Brain Injury

“…The primary motor cortex begins on the anterior wall of the central sulcus and continues rostrally to comprise what is the anterior paracentral lobule. It is the cortical region responsible for the collective generation of action potentials that relay neural information to the descending corticospinal tract to produce hand movements (71). The premotor cortex (PMC) is located anterior to the primary motor cortex (M1) and in a lateral position from midline; this region is in close spatial proximity to the inferior precentral sulcus (70).…”

“…The line of sight is often directed at items of interest in an environment, upon which manual interactions may subsequently be focused. Based on the final goal of an intended manual interaction, grasping choices will be affected; this not only has relevance for motor control and planning requisite to finger position but also for eye fixation position, as gaze is paramount to precise manual action before execution (71). Eye fixations suggest a multitiered manual motor planning hierarchy.…”

“…If needed, at the third level the movement plan incorporates a joint action component reflecting, e.g., the final resting place for the tool, handing it to a second person or placing it in a convenient location. Changes in the second and third levels of motor planning alter eye movement patterns and suggest a bidirectional sensorimotor coupling of eye to hand in coordinated activities (71). …”

Eye Control Deficits Coupled to Hand Control Deficits: Eye–Hand Incoordination in Chronic Cerebral Injury

“…The neuroanatomy of human eye-movement control depends on a large interconnected system of cortical and subcortical structures, and includes the frontal eye field, the parietal eye field, the dorsolateral prefrontal cortex, the supplementary eye field, the cingulate eye field, and the basal ganglia (30, 44–58). The neuroanatomy of human reach control depends on the primary motor cortex and the premotor and supplementary cortices, relaying neural information corticofugally through the descending corticospinal tracts to orchestrate hand movements (59, 60). The somatosensory cortex, posterior parietal cortex, cerebellum, and basal ganglia further supplement reach control.…”

Neurophysiology of Grasping Actions: Evidence from ERPs

“…dual-channel hypothesis; Jeannerod, 1981; Castiello, 2005; Goodale, 2011). In contrast, internal factors are properties of the person or the task; that is, largely cognitive variables, such as action planning, the goal of the action, habits or familiarity with the object or action (Rosenbaum et al, 1992; Meulenbroek et al, 1993; Kunde et al, 2007; van der Wel et al, 2007; Logan, 2009; Herbort and Butz, 2010, 2011; Knudsen et al, 2012; Belardinelli et al, 2016). For example, when grasping a bottle, the hand movement including the shaping of the fingers differs depending on whether the bottle will be thrown or precisely placed (Ansuini et al, 2008).…”