How your hand drives my eyes

When viewing object-related hand actions people make proactive eye movements of the same kind as those made when performing such actions. Why is this so? It has been suggested that proactive gaze when viewing a given hand action depends on the recruitment of motor areas such as the ventral premotor (PMv) cortex that would be involved in the execution of that action. However, direct evidence for a distinctive role of the PMv cortex in driving gaze behavior is still lacking. We recorded eye moments while viewing hand actions before and immediately after delivering repetitive transcranial magnetic stimulation (rTMS) over the left PMv and the posterior part of the left superior temporal sulcus, which is known to be involved in high-order visual action processing. Our results showed that rTMS-induced effects were selective with respect to the viewed actions following the virtual lesion of the left PMv only. This, for the first time, provides direct evidence that the PMv cortex might selectively contribute to driving the viewer’s gaze to the action’s target. When people view another’s action, their eyes may be driven by motor processes similar to those they would need to perform the action themselves.     

When emulation becomes reciprocity

It is well known that perceiving another''s body movements activates corresponding motor representations in an observer''s brain. It is nevertheless true that in many situations simply imitating another''s actions would not be an effective or appropriate response, as successful interaction often requires complementary rather than emulative movements. At what point does the automatic tendency to mirror another''s actions become the inclination to carry out appropriate, complementary movements? In the present study, single-pulse transcranial magnetic stimulation (TMS) was used to explore corticospinal excitability in participants observing action sequences evoking imitative or complementary movements. TMS was delivered at five time points corresponding to different moments in time when key kinematic landmarks characterizing an observed action occurred. A variation in motor evoked potentials (MEPs) confirmed that the motor system flexibly shifts from imitative to complementary action tendencies. That shift appears to take place very precociously in time. Observers are attuned to advance movement information and can use it to anticipate a future course of action and to prepare for an appropriate, complementary action. Altogether, these findings represent a step forward in research concerning social action-perception coupling mechanisms providing important data to better understand the role of predictive simulation in social contexts.     

Neural underpinnings of the ‘agent brain’: new evidence from transcranial direct current stimulation

Intentional binding (IB) refers to the temporal compression between a voluntary action and its sensory effect, and it is considered an implicit measure of sense of agency (SoA), that is, the capacity to control one's own actions. IB has been thoroughly studied from a behavioural point of view but only few studies have investigated its neural underpinnings, always using the same two paradigms. Although providing evidence that the supplementary motor complex is involved, findings are still too scarce to draw definitive conclusions. The aim of the present study was to establish a causal relationship between the pre‐supplementary motor area (pre‐SMA), known for its key role in action planning and initiation, and IB by means of transcranial direct current stimulation (tDCS). Participants underwent anodal, cathodal and sham control stimulations during three separate sessions (Experiment I). Subsequently, they underwent the same stimulation protocol (Experiment II) using as control a region potentially involved in the processing of the sensory effects of voluntary action (i.e., the right primary auditory cortex for the auditory effects of action). A significant reduction in IB was found only after stimulation of the pre‐SMA, which supports the causal contribution of this prefrontal area in the perceived linkage between action and its effects. As SoA could be disrupted in many psychiatric and neurological diseases, these results have direct clinical relevance as tDCS could be successfully used in this domain in virtue of the promising advantages it offers for rehabilitation.     

Transcranial direct current stimulation for the treatment of focal hand dystonia

The treatment of writer's cramp, a task‐specific focal hand dystonia, needs new approaches. A deficiency of inhibition in the motor cortex might cause writer's cramp. Transcranial direct current stimulation modulates cortical excitability and may provide a therapeutic alternative. In this randomized, double‐blind, sham‐controlled study, we investigated the efficacy of cathodal stimulation of the contralateral motor cortex in 3 sessions in 1 week. Assessment over a 2‐week period included clinical scales, subjective ratings, kinematic handwriting analysis, and neurophysiological evaluation. Twelve patients with unilateral dystonic writer's cramp were investigated; 6 received transcranial direct current and 6 sham stimulation. Cathodal transcranial direct current stimulation had no favorable effects on clinical scales and failed to restore normal handwriting kinematics and cortical inhibition. Subjective worsening remained unexplained, leading to premature study termination. Repeated sessions of cathodal transcranial direct current stimulation of the motor cortex yielded no favorable results supporting a therapeutic potential in writer's cramp. © 2011 Movement Disorder Society     

Does it make a difference if I have an eye contact with you or with your picture? An ERP study

Several recent studies have begun to examine the neurocognitive mechanisms involved in perceiving and responding to eye contact, a salient social signal of interest and readiness for interaction. Laboratory experiments measuring observers'' responses to pictorial instead of live eye gaze cues may, however, only vaguely approximate the real-life affective significance of gaze direction cues. To take this into account, we measured event-related brain potentials and subjective affective responses in healthy adults while viewing live faces with a neutral expression through an electronic shutter and faces as pictures on a computer screen. Direct gaze elicited greater face-sensitive N170 amplitudes and early posterior negativity potentials than averted gaze or closed eyes, but only in the live condition. The results show that early-stage processing of facial information is enhanced by another person''s direct gaze when the person is faced live. We propose that seeing a live face with a direct gaze is processed more intensely than a face with averted gaze or closed eyes, as the direct gaze is capable of intensifying the feeling of being the target of the other''s interest and intentions. These results may have implications for the use of pictorial stimuli in the social cognition studies.     

Infants’ Goal Prediction for Simple Action Events: The Role of Experience and Agency Cues

Looking times and gaze behavior indicate that infants can predict the goal state of an observed simple action event (e.g., object‐directed grasping) already in the first year of life. The present paper mainly focuses on infants’ predictive gaze‐shifts toward the goal of an ongoing action. For this, infants need to generate a forward model of the to‐be‐obtained goal state and to disengage their gaze from the moving agent at a time when information about the action event is still incomplete. By about 6 months of age, infants show goal‐predictive gaze‐shifts, but mainly for familiar actions that they can perform themselves (e.g., grasping) and for familiar agents (e.g., a human hand). Therefore, some theoretical models have highlighted close relations between infants’ ability for action‐goal prediction and their motor development and/or emerging action experience. Recent research indicates that infants can also predict action goals of familiar simple actions performed by non‐human agents (e.g., object‐directed grasping by a mechanical claw) when these agents display agency cues, such as self‐propelled movement, equifinality of goal approach, or production of a salient action effect. This paper provides a review on relevant findings and theoretical models, and proposes that the impacts of action experience and of agency cues can be explained from an action‐event perspective. In particular, infants’ goal‐predictive gaze‐shifts are seen as resulting from an interplay between bottom‐up processing of perceptual information and top‐down influences exerted by event schemata that store information about previously executed or observed actions.     

Kick with the finger: symbolic actions shape motor cortex excitability

A large body of research indicates that observing actions made by others is associated with corresponding motor facilitation of the observer's corticospinal system. However, it is still controversial whether this matching mechanism strictly reflects the kinematics of the observed action or its meaning. To test this issue, motor evoked potentials induced by single‐pulse transcranial magnetic stimulation were recorded from hand and leg muscles while participants observed a symbolic action carried out with the index finger, but classically performed with the leg (i.e., a soccer penalty kick). A control condition in which participants observed a similar (but not symbolic) hand movement was also included. Results showed that motor facilitation occurs both in the observer's hand (first dorsal interosseous) and leg (quadriceps femoris) muscles. The present study provides evidence that both the kinematics and the symbolic value of an observed action are able to modulate motor cortex excitability. The human motor system is thus not only involved in mirroring observed actions but is also finely tuned to their symbolic value.     

Predictive gaze shifts elicited during observed and performed actions in 10-month-old infants and adults

We asked whether people's actions are understood by projecting them onto one's own action programs, according to the direct matching hypothesis, and whether this mode of control functions in infants. Adults’ and infants’ gaze and hand movements were measured in two live situations. The task was either to move an object between two places in the visual field, or to observe the corresponding action performed by another person. When performing the action, infants and adults behaved strikingly similar. Hand and gaze movements were simultaneously initiated and gaze arrived at the goal ahead of the hand. When observing the actions, the initiation of the gaze shift was delayed relative to the observed hand movement in both infants and adults, but it still arrived at the goal ahead of the hand. For both the performance and observation of actions the proactiveness of gaze shifts was associated with saccades ahead of the velocity peak of the hand. The close similarity between adults’ and infants’ actions when performing the movements and the great advantage of the adults when observing them support the conclusion that one's own motor actions develop ahead of the ability to predict other people's actions.     

When gaze turns into grasp

Previous research has provided evidence for a neural system underlying the observation of another person's hand actions. Is the neural system involved in this capacity also important in inferring another person's motor intentions toward an object from their eye gaze? In real-life situations, humans use eye movements to catch and direct the attention of others, often without any accompanying hand movements or speech. In an event-related functional magnetic resonance imaging study, subjects observed videos showing a human model either grasping a target object (grasping condition) or simply gazing (gaze condition) at the same object. These two conditions were contrasted with each other and against a control condition in which the human model was standing behind the object without performing any gazing or grasping action. The results revealed activations within the dorsal premotor cortex, the inferior frontal gyrus, the inferior parietal lobule, and the superior temporal sulcus in both "grasping" and "gaze" conditions. These findings suggest that signaling the presence of an object through gaze elicits in an observer a similar neural response to that elicited by the observation of a reach-to-grasp action performed on the same object.     

Roles of the orexin system in central motor control

The neuropeptides orexin-A and orexin-B are produced by one group of neurons located in the lateral hypothalamic/perifornical area. However, the orexins are widely released in entire brain including various central motor control structures. Especially, the loss of orexins has been demonstrated to associate with several motor deficits. Here, we first summarize the present knowledge that describes the anatomical and morphological connections between the orexin system and various central motor control structures. In the next section, the direct influence of orexins on related central motor control structures is reviewed at molecular, cellular, circuitry, and motor activity levels. After the summarization, the characteristic and functional relevance of the orexin system's direct influence on central motor control function are demonstrated and discussed. We also propose a hypothesis as to how the orexin system orchestrates central motor control in a homeostatic regulation manner. Besides, the importance of the orexin system's phasic modulation on related central motor control structures is highlighted in this regulation manner. Finally, a scheme combining the homeostatic regulation of orexin system on central motor control and its effects on other brain functions is presented to discuss the role of orexin system beyond the pure motor activity level, but at the complex behavioral level.     

High‐frequency rTMS over the supplementary motor area for treatment of Parkinson's disease

Dysfunction of the basal ganglia‐thalamocortical motor circuit is a fundamental model to account for motor symptoms in Parkinson's disease (PD). Using high‐frequency repetitive transcranial magnetic stimulation (rTMS) over the supplementary motor area (SMA), we investigated whether modulation of SMA excitability engenders therapeutic effects on motor symptoms in PD. In this double‐blind placebo‐controlled study, 99 patients were enrolled and assigned randomly to SMA‐stimulation and sham‐stimulation groups. For SMA stimulation, 20 trains of 50 transcranial magnetic stimuli at 5 Hz were delivered at an intensity of 110% active motor threshold for leg muscles in one session. The sham stimulation was 20 trains of electric stimuli given through electrodes fixed on the head to mimic the cutaneous sensation during rTMS. Each session of intervention was carried out once a week for the first 8 weeks. The SMA stimulation, in contrast to the sham stimulation, engendered significant improvements in total scores and motor scores of the Unified Parkinson's Disease Rating Scale. Mean improvements in motor scores were 4.5 points in the SMA‐stimulation group and ?0.1 points in the sham‐stimulation group. Results indicate that 5 Hz rTMS over SMA modestly improves motor symptoms in PD patients; SMA is a potential stimulation site for PD treatment. © 2008 Movement Disorder Society     

Gaze shifts evoked by electrical stimulation of the superior colliculus in the head-unrestrained cat. I. Effect of the locus and of the parameters of stimulation

Several studies have suggested that the pattern of neuronal activity in the superior colliculus (SC) interacts with the well-known topographical coding of saccades (motor map). To further describe this interaction, we recorded gaze saccades evoked by electrical microstimulation of SC deeper layers in the head-unrestrained cat and systematically varied the collicular locus (25 sites) and parameters (intensity, frequency) of the stimulation. Long stimulation trains were used to avoid saccade truncation. We found that the direction and amplitude of evoked gaze shifts were related to the stimulation locus, describing a gaze shift map. For 18 out of 20 sites the amplitude, but not the direction, also strongly depended on stimulation strength. Indeed, gaze amplitude continuously increased when raising current intensity up to several times the threshold value T (the largest intensity tested was 6 x T), whereas varying pulse frequency from 150 to 750 pulses per second (p.p.s.) revealed an optimal frequency range (300 and 500 p.p.s.) eliciting the largest gaze shifts. Moreover, the intensity effect on amplitude increased in an orderly fashion with the rostro-caudal stimulation locus. Gaze shift amplitude was not related to the number of delivered stimulation pulses. Concerning movement initiation, increasing either intensity or frequency led to an exponential decrease in gaze latency until minimal values near 30 ms were reached, but the number of pulses delivered during the corresponding latency period remained constant within a 300-500 p.p.s. frequency range. These findings indicate that the pattern of collicular discharge evoked by electrical stimulation strongly interacts with the gaze shift map and provide evidence for a summation of collicular activities by downstream premotor neurons.     

Activation of frontoparietal attention networks by non-predictive gaze and arrow cues

Gaze and arrow cues automatically orient visual attention, even when they have no predictive value, but the neural circuitry by which they direct attention is not clear. Recent evidence has indicated that the ventral frontoparietal attention network is primarily engaged by breaches of a viewer’s cue-related expectations. Accordingly, we hypothesized that to the extent that non-predictive gaze and arrow cues automatically engender expectations with regard to cue location, they should activate the ventral attention network when they cue attention invalidly. Using event-related fMRI, we found that invalid gaze but not arrow cues activated the ventral attention network, specifically in the area of the right temporal parietal junction (TPJ), as well as nodes along the dorsal attention network associated with a redirection of attention to the correct target location. In additional whole-brain analyses, facilitation of behavioral response time by valid gaze cues was linearly associated with the degree of activation in the right TPJ. We conclude from our findings that gaze direction elicits potent expectations in humans with regard to an actor’s intention that engage attention networks if not differently from, at least more robustly than, arrow cues.     

Non-invasive brain stimulation (rTMS and tDCS) in patients with aphasia: Mode of action at the cellular level

A high proportion of patients who have suffered a stroke also suffer from aphasia. Approximately half of those affected will remain in this state despite intensive language therapy. Non-invasive brain stimulation allows us to directly and focally stimulate areas of the brain. Repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS), methods used in the treatment of aphasia, are based on an imbalance of mutual interhemispheric inhibition. In open and sham-controlled studies, a low-frequency, 1 Hz stimulation of the non-lesioned hemisphere (the homologue of Broca's area) for a week or more significantly improved spontaneous speech and anomia in patients with non-fluent aphasia. These positive outcomes from rTMS stimulation developed slowly, often over months following treatment, and persisted. Effects of intermittent theta burst stimulation (iTBS) developed faster than the low-frequency stimulation, and high-activity enhancement was detected in the left hemisphere after the stimulation of Broca's region. Both types of tDCS stimulation resulted in improved comprehension and reduced anomia, their primary modes of action are distinct, however, both share a common site of action with regard to the balance that occurs between inhibitory and excitatory neurotransmitters (synaptic and non-synaptic). Both types of non-invasive stimulation prepare the lesioned brain for better outcome.     

Do gaze behaviours during action observation predict interpersonal motor resonance?

Interpersonal motor resonance (IMR) is a common putative index of the mirror neuron system (MNS), a network containing specialised cells that fire during both action execution and observation. Visual content inputs to the MNS, however, it is unclear whether visual behaviours mediate the putative MNS response. We aimed to examine gaze effects on IMR during action observation. Neurotypical adults (N = 99; 60 female) underwent transcranial magnetic stimulation, electromyography, and eye-tracking during the observation of videos of actors performing grasping actions. IMR was measured as a percentage change in motor evoked potentials (MEPs) of the first dorsal interosseous muscle during action observation relative to baseline. MEP facilitation was observed during action observation, indicating IMR (65.43%, SE = 11.26%, P < 0.001). Fixations occurring in biologically relevant areas (face/hand/arm) yielded significantly stronger IMR (81.03%, SE = 14.15%) than non-biological areas (63.92%, SE = 14.60, P = 0.012). This effect, however, was only evident in the first of four experimental blocks. Our results suggest that gaze fixation can modulate IMR, but this may be affected by the salience and novelty of the observed action. These findings have important methodological implications for future studies in both clinical and healthy populations.     

Failure to read motor intentions from gaze in children with autism

A core feature of autism is the abnormal use of gaze to attribute mental states to others, and thus to predict others' behaviour. An untested idea is whether this dysfunction is confined to mental states having a propositional content, such as beliefs and desire or extends to motor intentional states which allow one to make inferences about the actions of others. This study used kinematics to examine the ability to use gaze to inform one about the motor states of another in normal and autistic children. In each trial two participants, a model and an observer, were seated facing each other at a table. In three experimental blocks the model was requested to grasp a stimulus, to gaze towards the same stimulus, and to gaze away from the stimulus without performing any action. The task for the observer was to grasp the stimulus after having watched the model perform her task. We observed that normal children showed facilitation effects in terms of movement speed following the observation of the model grasping or simply gazing at the object. In contrast, autistic children did not show any evidence of facilitation in these conditions. Neither normal nor autistic children showed evidence of facilitation when the model's gaze was not directed towards the stimulus. These findings demonstrate that, in contrast to normal children, children with autism fail to use information from the model's action or gaze to plan their subsequent action, and that in autism the inability to use of another person's gaze produces a lack of understanding of the motor intention of others.     

Dynamic feedback to the superior colliculus in a neural network model of the gaze control system

The role of the superior colliculus (SC) has been explored in the context of the gaze control system, with the conclusion that recent data place it inside the control loop calculating gaze error. A neural network proposed for the SC achieves both spatial and temporal integration of gaze signals. When placing the SC inside a gaze control loop, linear time-space transformations can be achieved even with restricted feedback on the edges of the map. The proposed gaze control model can reproduce all of the properties of previous head-fixed models. However, for the first time, a collicular mechanism is shown to provide plausible explanations for conflicting results upon electrical stimulation of rostral versus caudal sites on the colliculus, and can generate reasonable trajectories for both eye and head platforms in the head-free condition. The key assumption is the distribution of a common motor (gaze) error to the platforms contributing to the movement.     

Action observation and motor imagery for rehabilitation in Parkinson's disease: A systematic review and an integrative hypothesis

This article discusses recent evidence supporting the use of action observation therapy and motor imagery practice for rehabilitation of Parkinson's disease. A main question that emerges from the review regards the different effectiveness of these approaches and the possibility of integrating them into a single method to enhance motor behaviour in subjects with Parkinson’s disease. In particular, the reviewed studies suggest that action observation therapy can have a positive effect on motor facilitation of patients and that a long-term rehabilitation program based on action observation therapy or motor imagery practice can bring some benefit on their motor recovery. Moreover, the paper discusses how the research on the combined use of action observation and motor imagery for motor improvements in healthy subjects may encourage the combined use of action observation therapy and motor imagery practice for therapeutic aims in Parkinson's disease. To date, this hypothesis has never been experimented.