I. Toni

Complementary systems for understanding action intentions.

How humans understand the intention of others actions remains controversial. Some authors have suggested that intentions are recognized by means of a motor simulation of the observed action with the mirror-neuron system [1-3]. Others emphasize that intention recognition is an inferential process, often called mentalizing or employing a theory of mind, which activates areas well outside the motor system [4-6]. Here, we assessed the contribution of brain regions involved in motor simulation and mentalizing for understanding action intentions via functional brain imaging. Results show that the inferior frontal gyrus (part of the mirror-neuron system) processes the intentionality of an observed action on the basis of the visual properties of the action, irrespective of whether the subject paid attention to the intention or not. Conversely, brain areas that are part of a mentalizing network become active when subjects reflect about the intentionality of an observed action, but they are largely insensitive to the visual properties of the observed action. This supports the hypothesis that motor simulation and mentalizing have distinct but complementary functions for the recognition of others intentions.

Parieto-Frontal Connectivity during Visually Guided Grasping

Grasping an object requires processing visuospatial information about the extrinsic features (spatial location) and intrinsic features (size, shape, orientation) of the object. Accordingly, manual prehension has been subdivided into a reach component, guiding the hand toward the object on the basis of its extrinsic features, and a grasp component, preshaping the fingers around the center of mass of the object on the basis of its intrinsic features. In neural terms, this distinction has been linked to a dedicated dorsomedial “reaching” circuit and a dorsolateral “grasping” circuit that process extrinsic and intrinsic features, linking occipital areas via parietal regions with the dorsal and ventral premotor cortex, respectively. We have tested an alternative possibility, namely that the relative contribution of the two circuits is related to the degree of on-line control required by the prehension movement. We used dynamic causal modeling of functional magnetic resonance imaging time series to assess how parieto-frontal connectivity is modulated by planning and executing prehension movements toward objects of different size and width. This experimental manipulation evoked different movements, with different planning and execution phases for the different objects. Crucially, grasping large objects increased inter-regional couplings within the dorsomedial circuit, whereas grasping small objects increased the effective connectivity of a mainly dorsolateral circuit, with a degree of overlap between these circuits. These results argue against the presence of dedicated cerebral circuits for reaching and grasping, suggesting that the contributions of the dorsolateral and the dorsomedial circuits are a function of the degree of on-line control required by the movement.

Spatial and Effector Processing in the Human Parietofrontal Network for Reaches and Saccades

It is generally accepted that interactions between parietal and frontal cortices subserve the visuomotor processing for eye and hand movements. Here, we used a sequential-instruction paradigm in 3-T functional MRI to test the processing of effector and spatial signals, as well as their interaction, as a movement is composed and executed in different stages. Subjects prepared either a saccade or a reach following two successive visual instruction cues, presented in either order. One cue instructed which effector to use (eyes, right hand); the other signaled the spatial goal (leftward vs. rightward target location) of the movement. During the first phase of the prepared movement, after cueing of either goal or effector information, we found significant spatial goal selectivity but no effector specificity along the parietofrontal network. During the second phase of the prepared movement, when both goal and effector information were available, we found a large overlap in the neural circuitry involved in the planning of eye and hand movements. Gradually distributed along this network, we observed clear spatial goal selectivity and limited, but significant, effector specificity. Regions in the intraparietal sulcus and the dorsal premotor cortex were selective to both goal location and motor effector. Taken together, our results suggest that the relative weight of spatial goal and effector selectivity changes along the parietofrontal network, depending on the status of the movement plan.

Cerebral Changes during Performance of Overlearned Arbitrary Visuomotor Associations

The posterior parietal cortex (PPC) is known to be involved in the control of automatic movements that are spatially guided, such as grasping an apple. We considered whether the PPC might also contribute to the performance of visuomotor associations in which stimuli and responses are linked arbitrarily, such as producing a certain sound for a typographical character when reading aloud or pressing pedals according to the color of a traffic light when driving a motor vehicle. The PPC does not appear to be necessary for learning new arbitrary visuomotor associations, but with extensive training, the PPC can encode nonspatial sensory features of task-relevant cues. Accordingly, we have tested whether the contributions of the PPC might become apparent once arbitrary sensorimotor mappings are overlearned. We have used functional magnetic resonance imaging to measure cerebral activity while subjects were learning novel arbitrary visuomotor associations, overlearning known mappings, or attempting to learn frequently changing novel mappings. To capture the dynamic features of cerebral activity related to the learning process, we have compared time-varying modulations of activity between conditions rather than average (steady-state) responses. Frontal, striatal, and intraparietal regions showed decreasing or stable activity when subjects learned or attempted to learn novel associations, respectively. Importantly, the same frontal, striatal, and intraparietal regions showed time-dependent increases in activity over time as the mappings become overlearned, i.e., despite time-invariant behavioral responses. The automaticity of these mappings predicted the degree of intraparietal changes, indicating that the contribution of the PPC might be related to a particular stage of the overlearning process. We suggest that, as the visuomotor mappings become robust to interference, the PPC may convey relevant sensory information toward the motor cortex. More generally, our findings illustrate how rich cerebral dynamics can underlie stable behavior.

Functional Rather than Effector-Specific Organization of Human Posterior Parietal Cortex

Neurophysiological and neuroimaging studies have shown that the posterior parietal cortex (PPC) distinguishes between the planning of eye and hand movements. This distinction has usually been interpreted as evidence for a modular, effector-specific organization of this cerebral region. However, the eyes differ markedly from other body parts both in terms of their functional purpose and with regard to the spatial transformations required to plan goal-directed movements. PPC may therefore provide specialized subregions for eye movements, but distinguish less for other effectors. Using functional magnetic resonance imaging, we compared activity during memory-guided eye, hand, and foot movements in human participants. The results did not reveal any significant activation differences during the planning of hand and foot movements, except in the most anterior part of PPC [Brodmanns area (BA) 5], marginally extending into anterior BA 7/40. This region showed a lateral-to-medial gradient for hand versus foot movement planning. The limb-unspecific PPC regions were functionally connected with hand and foot motor regions. In contrast, a gradient-like organization was found for all of PPC for the planning of eye versus hand and foot movements. Although planning-related activity across the three effectors considerably overlapped, saccade planning activated occipitoparietal regions more than limb movements, whereas limb movements activated anterior regions of the superior parietal lobule more than saccades. We infer that PPC does not follow a strict effector-specific organization. Rather, the large-scale organization of this region might reflect the different computational constraints that need to be satisfied when planning eye and limb movements.

Reference Frames for Reach Planning in Human Parietofrontal Cortex

To plan a reaching movement, the brain must integrate information about the spatial goal of the reach with positional information about the selected hand. Recent monkey neurophysiological evidence suggests that a mixture of reference frames is involved in this process. Here, using 3T functional magnetic resonance imaging (fMRI), we tested the role of gaze-centered and body-centered reference frames in reach planning in the human brain. Fourteen human subjects planned and executed arm movements to memorized visual targets, while hand starting position and gaze direction were monitored and varied on a trial-by-trial basis. We further introduced a variable delay between target presentation and movement onset to dissociate cerebral preparatory activity from stimulus- and movement-related responses. By varying the position of the target and hand relative to the gaze line, we distinguished cerebral responses that increased for those movements requiring the integration of peripheral target and hand positions in a gaze-centered frame. Posterior parietal and dorsal premotor areas showed such gaze-centered integration effects. In regions closer to the primary motor cortex, body-centered hand position effects were found. These results suggest that, in humans, spatially contiguous neuronal populations operate in different frames of reference, supporting sensorimotor transformations according to gaze-centered or body-centered coordinates. The former appears suited for calculating a difference vector between target and hand location, whereas the latter may be related to the implementation of a joint-based motor command.

Increased dependence of action selection on recent motor history in Parkinson's disease.

It is well known that the basal ganglia are involved in switching between movement sequences. Here we test the hypothesis that this contribution is an instance of a more general role of the basal ganglia in selecting actions that deviate from the context defined by the recent motor history, even when there is no sequential structure to learn or implement. We investigated the effect of striatal dopamine depletion [in Parkinsons disease (PD)] on the ability to switch between independent action plans. PD patients with markedly lateralized signs performed a hand laterality judgment task that involved action selection of their most and least affected hand. Trials where patients selected the same (repeat) or the alternative (switch) hand as in a previous trial were compared, and this was done separately for the most and least affected hand. Behaviorally, PD patients showed switch-costs that were specific to the most affected hand and that increased with disease severity. Functional magnetic resonance imaging (fMRI) showed that this behavioral effect was related to the state of the frontostriatal system: as disease severity increased, contributions of the basal ganglia to the selection process and their effective connectivity with the medial frontal cortex (MFC) decreased, whereas involvement of the MFC increased. We conclude that the basal ganglia are important for rapidly switching toward novel motor plans even when there is no sequential structure to learn or implement. The enhanced MFC activity may result either from reduced focusing abilities of the basal ganglia or from compensatory processes.

Cortical dynamics of sensorimotor integration during grasp planning

Our sensorimotor interactions with objects are guided by their current spatial and perceptual features, as well as by learned object knowledge. A fresh red tomato is grasped differently than a soft overripe tomato, even when those objects possess the same spatial metrics of size and shape. Objects spatial and perceptual features need to be integrated during grasping, but those features are analyzed in two anatomically distinct neural pathways. The anterior intraparietal sulcus (aIPS) might support the integration of those features. We combine transcranial magnetic stimulation (TMS) interference, EEG recordings, and psychophysical methods to test aIPS causal contributions to sensorimotor integration, characterizing the dynamics of those contributions during motor planning. Human subjects performing grasping movements were provided with visual information about a target object, namely spatial and pictorial cues, whose availability and information value were independently modulated on each trial. Maximally informative visual cues, irrespective of their spatial or perceptual nature, led to enhanced motor preparatory activity early during movement planning, and to stronger spatial congruency between finger trajectories and target object. Disturbing aIPS activity with single-pulse TMS within 200 ms after object presentation reduced those electrophysiological and behavioral indices of enhanced motor planning. TMS interference with aIPS also disturbed subjects ability to use learned object knowledge during motor planning. These results indicate that aIPS is necessary for the fast generation of a new motor plan on the basis of both spatial and pictorial cues. Furthermore, as learned object knowledge becomes available, aIPS comes to strongly depend on this prior information for structuring the motor plan.

Comparable mechanisms for action and language: Neural systems behind intentions, goals and means

In this position paper we explore correspondence between neural systems for language and action starting from recent electrophysiological findings on the roles of posterior and frontal areas in goal-directed grasping actions. The paper compares the perceptual and motor organization for action and language, and discusses similarities between the impairments of apraxic and aphasic patients. Furthermore, based on the anatomical connectivity of Brodmann areas (BA) 44 and 45 separate functional roles are proposed for the two constituent parts of Brocas area. The final part of the paper includes a discussion on the role of BA 44 and neighboring areas in sequential processing for action and language.

Selection, preparation, and monitoring: Current approaches to studying the neural control of action

F.C. Donders Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, The NetherlandsImagine an athlete throwing a disc, as shown on the cover ofthis issue. We see him tensing his muscles but how can weknow which brain structures control this powerful action?The ancient Greeks could only observe and measure limited,externalaspectsofthismovement,suchasthetimingofmus-cle flexions and the distance the discus is thrown. Just as theancient Greeks, until recently we had little way to observe thebrainmechanismsthatgiverisetothisfeat.Sincemovementswere considered to be difficult to transfer to the laboratory toprovide quantitative data, the study of movement has foralongtimebeenoneof theless studiedfieldsofcognitivepsy-chology. The rise of various techniques to study the humanbrain during task performance initially seemed to aggravatethese problems, as they all require the participant to remainmotionless for an extended period and are highly sensitiveto movement artifacts. As such, the study of movement haslong been a neglectedchild in the realm of cognitive neurosci-ence. Over the last 15 years, however, this situation haschanged.Thisisdueinparttotheriseofvariousimagingtech-niques and accompanying statistical tools that are less sensi-tive to these problems, but also to the increasing interest inthe cognitive processes associated with any movement.Indeed, rather than focusing on the movement directly, thisresearch is focusing on the processes leading up to the move-ment and the evaluation of the consequences of the move-ment following its execution. All these processes thatprecede and directly follow observable movements are nowa-days collectively referred to as actions. These developments,in turn, have led to a large rise in popularity of action-relatedresearch. Thegoal of this specialissueof Cortexis to illustratethe diverse experimental approaches currently employed instudying the neural control of actions and the consequencesthis is having on other domains of cognitive neuroscience.Thecontributions inthisissueconstituteamixtureof reviewsandnovelexperimentaldata.Thepaperspartlyoriginatefroma symposium on this topic held at the Radboud UniversityNijmegen, November 9–10, 2006.The techniques most often used to probe neural activityduring selection, preparation, and monitoring of actions in-clude various signals derived from EEG and MEG, such as theevent-related potential (ERP), motor-evoked potentials in theelectromyogramelicitedusingtranscranial magneticstimula-tion(TMS),andimagingtechniques suchaspositronemissiontomography (PET) and functional magnetic resonance imag-ing (fMRI). By necessity, the overt movements that can be per-formed by participants in these experiments are limited. EEGsignals are highly sensitive to movement artifacts, as are im-ages obtained with fMRI. Although recently solutions havebeenfoundtostudymorecomplexmovementsinthefMRIen-vironment (Diedrichsen et al., 2005; Majdandzic´ et al., 2007;Re´my et al., 2008, this issue), the movement studied is oftennothing more than a simple button press. However, a numberof paradigms have been proposed that allow imaging of therepresentations underlying actions uncontaminated by theexecution of complex movements (Jeannerod, 2006). Forinstance, a window on the neural processesunderlying actionspecification can be provided by studying imagery of theseactions (De Lange et al., 2008, this issue) or the preparationof actions. These paradigms allow the researcher a windowon processes far more complex than the simple execution of