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Event-Related Brain Potentials for Goal-Related Power Grips

  • Jan Westerholz ,

    jan.westerholz@uni-bielefeld.de

    Affiliations Center of Excellence Cognitive Interaction Technology (CITEC), Bielefeld, Germany, Neurocognition and Action Research Group, Faculty of Psychology and Sports Sciences, University of Bielefeld, Bielefeld, Germany

  • Thomas Schack,

    Affiliations Center of Excellence Cognitive Interaction Technology (CITEC), Bielefeld, Germany, Neurocognition and Action Research Group, Faculty of Psychology and Sports Sciences, University of Bielefeld, Bielefeld, Germany, Research Institute for Cognition and Robotics (CoR-Lab), Bielefeld, Germany

  • Dirk Koester

    Affiliations Center of Excellence Cognitive Interaction Technology (CITEC), Bielefeld, Germany, Neurocognition and Action Research Group, Faculty of Psychology and Sports Sciences, University of Bielefeld, Bielefeld, Germany

Event-Related Brain Potentials for Goal-Related Power Grips

  • Jan Westerholz, 
  • Thomas Schack, 
  • Dirk Koester
PLOS
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Abstract

Recent research has shown that neurophysiological activation during action planning depends on the orientation to initial or final action goals for precision grips. However, the neural signature for a distinct class of grasping, power grips, is still unknown. The aim of the present study was to differentiate between cerebral activity, by means of event-related potentials (ERPs), and its temporal organization during power grips executed with an emphasis on either the initial or final parts of movement sequences. In a grasp and transportation task, visual cues emphasized either the grip (the immediate goal) or the target location (the final goal). ERPs differed between immediate and final goal-cued conditions, suggesting different means of operation dependent on goal-relatedness. Differences in mean amplitude occurred earlier for power grips than for recently reported precision grips time-locked to grasping over parieto-occipital areas. Time-locked to final object placement, differences occurred within a similar time window for power and precision grips over frontal areas. These results suggest that a parieto-frontal network of activation is of crucial importance for grasp planning and execution. Our results indicate that power grip preparation and execution for goal-related actions are controlled by similar neural mechanisms as have been observed during precision grips, but with a distinct temporal pattern.

Introduction

The ability to control the movements of our hands is of utmost importance to our daily life. Controlling the hands enables us to perform a wide range of actions, like grasping objects of various shapes, manipulating items, or using tools, all of which involve action transformations. In the middle of the last century, Napier [1] emphasized that the anatomical and biomechanical features of the human hand make it ideal for tool use; grasping can be performed with high precision, but also with strong force. Furthermore, our hands even give us the ability to communicate using gestures, sign language, or writing messages. Because of their clear importance for human action and interaction, manual movements and manual intelligence have become an important topic in cognitive robotics in recent years. Such complex manual movements require anticipatory control, which seems to be based on cognitive networks in long-term memory [2]. Only very few electroencephalographic (EEG) studies have investigated overt complex movements. Up to now, most event-related potential (ERP) studies have either focused on simple movements like button presses or on the preparation phase of a movement. Therefore, we decided to use a grasping task to study the neural mechanisms underlying overt complex human movement control using EEG.

Grasping is a complex and cognitively organized activity. Therefore, it is used in motor control research to investigate the cognitive architecture of goal-oriented action [2]. More than a century ago, Woodworth [3] suggested that goal-directed actions consist of two phases. The first movement phase depends mostly on planning processes that take place before the action. The second movement phase involves discrete feedback-based action control [3], [4]. The anticipatory character of motor planning processes have been demonstrated in a study by Rosenbaum et al. [5], which showed that people chose different initial grips when reaching for the same rod depending on which end they planned to place on a disc on the table. Through this change in initial posture, participants in the study of Rosenbaum and colleagues avoided finishing their movements with awkward end postures (i.e., holding the rod with their thumb pointing down), even if this meant initially grasping the rod with an uncomfortable grip (i.e., an underhand grip). The authors concluded that participants anticipated their future hand postures, as the participants showed a preference for final comfort over initial comfort. This tendency to avoid awkward postures at the final position of a movement was termed the end-state comfort effect [5].

Interestingly, such planning processes during a reach and grasp task can be observed on a finer scale than the decision between overhand and underhand grasp. Schütz et al. [6] tested participants in a sequential (predictable) and a randomized (unpredictable) perceptual-motor task, which offered a continuous range of posture solutions for each movement trial. Participants were asked to open a column of drawers in a sequential or randomized order, grasping each drawer on a protruding cylindrical knob. The end-state comfort effect was reproduced under both predictable and unpredictable conditions.

Looking in more detail into the modular organization of grasping, we will find further indicators for anticipation. Before we grasp an object, we reach for it. During this reach phase the fingers preshape in anticipation of the forthcoming grasp. The preshaping of the fingers is not only matched to the object that is grasped, but also to the task that has to be performed with the object [7]. These kinematic effects suggest that anticipation is not only a sensorimotor function, but also a cognitive function reflecting the action goal [7]. In a bar transport task, for example, that replicated the end-state comfort effect, Hughes et al. [8] observed that the formation of the grasp posture started at the beginning of the action. This finding implies that participants had selected a grasp prior to the movement which would satisfy end-state comfort. Moreover, when the action goal was changed shortly after movement onset, participants modified their reach-to-grasp movements to ensure a comfortable posture at the end of the movement, demonstrating the influence of action goals for movement planning and execution.

Different planning processes can, additionally, be observed in the kinematic parameters of power and precision grips [9]. Participants in the study of Castiello et al. [9] had to grasp a small or large dowel and use either a precision grip or a whole hand power grip to do so. On 20% of the trials the object size was unexpectedly changed during the reach phase. The results show shorter movement time and shorter deceleration time for the power grip compared to the precision grip. Maximum grip aperture occurred earlier for the precision grip than for the power grip and, according to Castiello et al. [9], indicates the temporal coordination of grasp and transport components. They suggest that this temporal difference indicates an earlier anticipation of an object’s characteristics in the case of higher precision demands. For trials in which the grip had to be altered during the action, they found changes during the deceleration phase of the reaching movement and, of course, during grasping. Faster movement and deceleration times for power grips indicate that planning processes for these movements must be faster or happen earlier in comparison to the planning processes for precision grips.

There is also neurophysiological evidence for a cognitive function of planning processes toward the action goal, in the form of activation of the motor system during action anticipation [10]. Further neurophysiological studies are likely to discover different variables that influence the spatial and, using EEG, particularly the temporal organization of movement planning and execution.

Following the results of behavioral studies, Majdandzic et al. [11] used fMRI to examine the spatial neuroanatomical organization of movement preparation and the neural correlates of action planning. Their participants inserted an object into one of two slots. The object consisted of a large and a small cube. The two slots matched the objects in size. Participants were given a cue which determined the final goal (which slots to fill) or the immediate goal (which part of the object to grasp). Thus, participants always executed the same movement, but with an emphasis on either of two different parts of the movement sequence. The researchers observed differential preparatory activity along the superior frontal gyrus and in left inferior parietal cortex during the final goal trials, and differential activity in parieto-occipital and occipito-temporal cortex during the immediate goal trials. Their results also show different parieto-frontal circuits responsible for planning of the same action depending on which factors are emphasized. In addition to the previously mentioned study, Castiello and Begliomini [12] report fMRI results that indicate a specific area to be tuned to the type of grasp, namely the anterior intra parietal sulcus. Castiello and Begliomini [12] further suggest that a larger number of precision grip configurations, rather than whole hand grip configurations, might be represented here. Taken together, the aforementioned studies demonstrate the importance of goals for motor control. They suggest that the goals of an action are more crucial for motor planning than the trajectory of the movement itself.

In accordance with the above-mentioned fMRI studies, Filimon [13] found the intra parietal sulcus (IPS) to play an important role for the control of grasping within the distributed parieto-frontal network. Within this network premotor activity seems to precede posterior parietal activity in some instances, depending on the task, parieto-frontal circuit, and effector used. However, the individual contributions of premotor and parietal areas remain unclear. In 2012, Bozzacchi et al. [14] used EEG to investigate temporal aspects of action planning, and they reported some controversial findings. They based their study on the assumption of a parieto-frontal network and recorded pre-movement event-related potentials, more specifically the Bereitschaftspotential (BP). The BP can be observed prior to voluntary movement and is considered to be a manifestation of the preparation for action [15]. One main interest of Bozzacchi et al.’s study was the temporal organization of motor preparation for grasping. Participants performed three different actions: reaching for a teacup, grasping a teacup, and attempting to grasp a teacup while their fingers were constrained by a band, making grasping impossible. Bozzacchi et al. [14] observed activity over parietal areas well before action onset for the goal-oriented action of grasping an object, but not for reaching or impossible grasping. They found that activity for grasping preparation started earlier and was more widespread and complex than was previously described in the literature, as reviewed by Shibasaki and Hallett [16]. Regarding the temporal relation of parietal and frontal activity, Bozzacchi et al. [14] reported that the earliest parietal activity was followed by frontal activity. They conclude that action preparation is affected in an early phase by the meaning of an action as well as by the type of action to be performed.

In a different EEG experiment, Bozzacchi et al. [17] observed similar motor preparation processes for real and virtual grasps (the virtual grasp being a key press, which started a video showing a grasping action) over posterior parietal areas. From this study they conclude that the final action effect, and not the movement kinematics, influenced the early preparation phase. The results provide further support for the suggestion that parietal areas are of crucial importance for grasp planning and that they provide information for grasp preparation. The temporal organization of the neurophysiological correlates underlying grasping and its preparation remains controversial [13]. As far as we know, only few ERP studies have focused on the temporal organization of overt dynamic grasping movements.

Gratton et al. [18] examined the mechanisms of pre- and poststimulus response activation in a choice reaction time paradigm that required an overt movement, namely squeezing a zero-displacement dynamometer. Motor potentials following stimulus presentation suggested that partial analyses of stimulus information could activate responses. Gratton et al. [18] further observed that, at the time of the EMG response, the level of response activation was constant for trials with different response latencies. This study exemplifies that it is possible to investigate the temporal organization of response selection using overt grasping movements.

Van Schie and Bekkering [19] tried to “clarify the individual contributions of the different parts of the motor system that have been implied to underlie goal representations in action control” (p. 184). They instructed a grasp and transport task which dictated either the grasp participants had to use (immediate goal) or the end position of the transport (final goal). Although participants executed the same overt movement in both conditions, Van Schie and Bekkering observed different ERPs for immediate and final action goals. The immediate goal was accompanied by a parieto-occipital slow wave, while the final goal was accompanied by a slow wave over left frontal regions. The authors suggested that the enhanced activation found in posterior parts for the immediate goal indicates this area’s involvement in the prehension of the object. This interpretation is supported by findings of Van Elk et al. [20], who observed enhanced parietal activation for the observation of grip errors and suggested that it reflects a representation of hand-object interaction. The enhanced activation Van Schie and Bekkering found in anterior parts for the final goal might indicate frontal involvement in the planning and control of sequential behavior [19].

In sum, a parieto-frontal network underlying grasping has been shown in several studies. While premotor activity seems to precede posterior parietal activity in some instances [13], Bozzacchi et al. [14] report in their experiment that the earliest parietal activity was followed by frontal activity. Thus, the temporal organization of the neural mechanisms underlying grasping and its preparation remains