Believe it or not: Moving non-biological stimuli believed to have human origin can be represented as human movement.

Does our brain treat non-biological movements (e.g. moving abstract shapes or robots) in the same way as human movements? The current work tested whether the movement of a non-biological rectangular object, believed to be based on a human action is represented within the observer's motor system. A novel visuomotor priming task was designed to pit true imitative compatibility, due to human action representation against more general stimulus response compatibility that has confounded previous belief experiments. Stimulus response compatibility effects were found for the object. However, imitative compatibility was found when participants repeated the object task with the belief that the object was based on a human finger movement, and when they performed the task viewing a real human hand. These results provide the first demonstration that non-biological stimuli can be represented as a human movement if they are believed to have human agency and have implications for interactions with technology and robots.

How does visuomotor priming differ for biological and non-biological stimuli? A review of the evidence.

Visuomotor priming occurs when our actions are influenced by observing a compatible or incompatible action. Here we ask whether visuomotor priming is specific to human, biological actions or generalises to non-biological movements, such as abstract shapes or robots. Reviewing the evidence indicates that priming occurs for both types of stimuli and emphasises the contributions of both bottom-up (e.g. stimulus saliency, appearance, kinematics) and top-down (e.g. attention and prior knowledge) factors. We propose a model suggesting that although bottom-up features play a critical role, the degree of difference in priming for biological versus non-biological stimuli can be ultimately shaped by top-down factors.

Exploring visuomotor priming following biological and non-biological stimuli.

Observation of human actions influences the observer's own motor system, termed visuomotor priming, and is believed to be caused by automatic activation of mirror neurons. Evidence suggests that priming effects are larger for biological (human) as opposed to non-biological (object) stimuli and enhanced when viewing stimuli in mirror compared to anatomical orientation. However, there is conflicting evidence concerning the extent of differences between biological and non-biological stimuli, which may be due to stimulus related confounds. Over three experiments, we compared how visuomotor priming for biological and non-biological stimuli was affected over views, over time and when attention to the moving stimulus was manipulated. The results indicated that the strength of priming for the two stimulus types was dependent on attentional location and load. This highlights that visuomotor priming is not an automatic process and provides a possible explanation for conflicting evidence regarding the differential effects of biological and non-biological stimuli.

Movement interference in autism-spectrum disorder.

Movement interference occurs when concurrently observing and executing incompatible actions and is believed to be due to co-activation of conflicting populations of mirror neurons. It has also been suggested that mirror neurons contribute towards the imitation of observed actions. However, the exact neural substrate of imitation may depend on task demands: a processing route for goal-directed meaningful actions may be distinct from one for non-goal-directed actions. A more controversial role proposed for these neurons is in theory of mind processing, along with the subsequent suggestion that impairment in the mirror neuron circuit can contribute to autism-spectrum disorder (ASD) where individuals have theory of mind deficits. We have therefore examined movement interference in nine ASD participants and nine matched controls while performing actions congruent and incongruent with observed meaningless arm movements. We hypothesised that if the mirror neuron system was impaired, reduced interference should be observed in the ASD group. However, control and ASD participants demonstrated an equivalent interference effect in an interpersonal condition, with greater movement variability in the incongruent compared to the congruent condition. A component of movement interference which is independent of congruency did differ between groups: ASD participants made generally more variable movements for the interpersonal task than for biological dot-motion task, while the reverse was true for the control participants. We interpret these results as evidence that the ASD participant group either rely to a greater extent on the goal-directed imitation pathway, supporting claims that they have a specific deficit of the non-goal-directed imitation pathway, or exhibit reduced visuomotor integration.

The cerebellum and motor dysfunction in neuropsychiatric disorders.

The cerebellum is densely interconnected with sensory-motor areas of the cerebral cortex, and in man, the great expansion of the association areas of cerebral cortex is also paralleled by an expansion of the lateral cerebellar hemispheres. It is therefore likely that these circuits contribute to non-motor cognitive functions, but this is still a controversial issue. One approach is to examine evidence from neuropsychiatric disorders of cerebellar involvement. In this review, we narrow this search to test whether there is evidence of motor dysfunction associated with neuropsychiatric disorders consistent with disruption of cerebellar motor function. While we do find such evidence, especially in autism, schizophrenia and dyslexia, we caution that the restricted set of motor symptoms does not suggest global cerebellar dysfunction. Moreover, these symptoms may also reflect involvement of other, extra-cerebellar circuits and detailed examination of specific sub groups of individuals within each disorder may help to relate such motor symptoms to cerebellar morphology.

Differentiation between external and internal cuing: an fMRI study comparing tracing with drawing.

Externally cued movement is thought to preferentially involve cerebellar and premotor circuits whereas internally generated movement recruits basal ganglia, pre-supplementary motor cortex (pre-SMA) and dorsolateral prefrontal cortex (DLPFC). Tracing and drawing are exemplar externally and internally guided actions and Parkinson's patients and cerebellar patients show deficits in tracking and drawing, respectively. In this study we aimed to examine this external/internal distinction in healthy subjects using functional imaging. Ten healthy subjects performed tracing and drawing of simple geometric shapes using pencil and paper while in a 3-T fMRI scanner. Results indicated that compared to tracing, drawing generated greater activation in the right cerebellar crus I, bilateral pre-SMA, right dorsal premotor cortex and right frontal eye field. Tracing did not recruit any additional activation compared to drawing except in striate and extrastriate visual areas. Therefore, drawing recruited areas more frequently associated with cognitively challenging tasks, attention and memory, but basal ganglia and cerebellar activity did not differentiate tracing from drawing in the hypothesised manner. As our paradigm was of a simple, repetitive and static design, these results suggest that the task familiarity and the temporal nature of visual feedback in tracking tasks, compared to tracing, may be important contributing factors towards the degree of cerebellar involvement. Future studies comparing dynamic with static external cues and visual feedback may clarify the role of the cerebellum and basal ganglia in the visual guidance of drawing actions.

Modulation of saccadic intrusions by exogenous and endogenous attention.

Primary gaze fixation in healthy individuals is frequently interrupted by microsaccades and saccadic intrusions (SI). The neural systems responsible for the control of attention and eye movements are believed to overlap and in line with this, the behaviour of microsaccades appears to be affected by exogenous and endogenous attention shifts. In the current work we wished to establish whether SI would also be influenced by attention in order to provide evidence that SI and microsaccades exhibit similar behaviour and further investigate the extent of overlap between attention and eye movement systems. Twelve participants performed a cue-target task where they were cued exogenously or endogenously and had to respond to the appearance of a peripheral target with either a button press or saccade. Our results replicate earlier microsaccade research, indicating that SI are also influenced by exogenous and endogenous attention. In all conditions, SI frequency initially decreased following the cue, then rose to a maximum before falling to below baseline levels. Following the exogenous cue, SI were more frequently directed away from the cue as predicted by inhibition of return. Additionally, SI direction following the endogenous cue was biased towards the cue for the saccadic response mode only, suggesting that the degree to which the eye movement and attention systems overlap depends on whether an eye movement is required. In summary, our findings indicate that SI characteristics are modulated by exogenous and endogenous attention and in a similar way to microsaccades, suggesting that SI and microsaccades may lie on a continuum of fixational instabilities. Furthermore, as with microsaccades, SI are likely to provide additional insights into the relationship between attention and the oculomotor systems.

Paying attention to saccadic intrusions.

Fixation to a target in primary gaze is invariably interrupted by physiological conjugate saccadic intrusions (SI). These small idiosyncratic eye movements (usually <1 degrees in amplitude) take the form of an initial horizontal fast eye movement away from the desired eye position, followed after a variable duration by a return saccade or drift. As the aetiology of SI is still unclear, it was the aim of this study to investigate whether SI are related to exogenous or endogenous attentional processes. This was achieved by varying (a) the "bottom-up" target viewing conditions (target presence, servo control of the target, target background, target size) and (b) the 'top-down' attentional state (instruction change--'look' or 'hold eyes steady' and passive fixation versus active--'respond to change' fixation) in 13 subjects (the number of participants in each task varied between 7 and 11). We also manipulated the orientation of pure exogenous attention through a cue-target task, during which subjects were required to respond to a target, preceded by a non-informative cue by either pressing a button or making a saccade towards the target. SI amplitude, duration, frequency and direction were measured. SI amplitude was found to be significantly higher when the target was absent and SI frequency significantly lower during open loop conditions. Target size and background influenced SI behaviour in an idiosyncratic manner, although there was a trend for subjects to exhibit lower SI frequencies and amplitudes when a patterned background was present and larger SI amplitudes with larger target sizes. SI frequency decreased during the "hold eyes steady" passive command as well as during active fixation but SI direction was not influenced by the exogenous cue-target task. These results suggest that SI are related to endogenous rather than exogenous attention mechanisms. Our experiments lead us to propose that SI represent shifts in endogenous attention that reflect a baseline attention state present during laboratory fixation tasks and may prove to be a useful tool to explore higher cortical control of fixation.

Saccadic instabilities and voluntary saccadic behaviour.

Primary gaze fixation is never perfectly stable but can be interrupted by involuntary, conjugate saccadic intrusions (SI). SI have a high prevalence in the normal population and are characterised by a horizontal fast eye movement away from the desired eye position, followed, after a variable duration, by a return saccade or drift. Amplitudes are usually below 1 degrees and they often exhibit a directional bias. The aim of the present study was to investigate the aetiology of SI in relation to saccadic behaviour. It was hypothesised that if SI resulted from deficits in the saccadic system (i.e. reduced inhibitory mechanisms), changes in voluntary saccade behaviour may be apparent and related to SI frequency. To examine this, synchrony (no gap), gap, overlap and antisaccade tasks were conducted on ten normal subjects. No significant correlations were found between SI frequency and voluntary saccade latencies, the percentage of express saccades, or the percentage of antisaccade errors. In addition, no significant correlations were found between SI directional biases and saccade latency directional biases, express saccade biases or antisaccade error biases. These results suggest that an underlying alteration to saccadic behaviour is unlikely to be involved in SI production, and that the SI command signal may arise from the influence of attention on an intact saccadic system. Specifically, descending corticofugal signals relating to attention level and orientation may alter the balance between fixation and saccade generation, so determining SI characteristics.

Characteristics of saccadic intrusions.

Primary fixation is never perfectly stable, but is frequently interrupted by slow drifts, microsaccades and saccadic intrusions (SI). SI are involuntary, conjugate movements which take the form of an initial fast movement away from the desired eye position and followed after a short duration, by either a return secondary saccade or a drift. The purpose of this study was to examine the prevalence and metrics of SI in a population of 50 healthy subjects. Using both one and two dimensional recordings we find that all 50 members of the subject group exhibited SI. The SI were bilateral, conjugate and horizontal. No purely vertical SI were detected when examined in three subjects. SI amplitude mean and range was 0.6 degrees +/-0.5 degrees, 0.1 degrees -4.1 degrees; SI frequency mean and range was 18.0+/-14.3 per min, 1.0-54.8 per min; SI duration mean and range was 225+/-150, 20-870 ms. The mean SI amplitude and frequency when SI<0.5 degrees were removed was 0.97 degrees +/-0.56 degrees and 7.0+/-11.4 per min respectively. Age was positively correlated with SI amplitude (p<0.01), but there was no correlation between age and SI frequency. Three of four types of SI monophasic square wave intrusions (MSWI), biphasic square wave intrusions (BSWI) and double saccadic pulses (DSP) were found to be exclusively saccadic, whilst the fourth type, the single saccadic pulses (SSP), were confirmed to exhibit a slow secondary component. MSWI were the most frequently observed SI occurring in 47 out of 50 (94%) of the subjects with a mean amplitude, frequency and duration of 0.7 degrees +/-0.5 degrees, 11.5+/-11.6 per min, and 255+/-147 ms respectively. Mean amplitudes and frequencies for BSWI (n=20), SSP (n=11) and DSP (n=34) were found to be 0.50 degrees +/-0.2 degrees, 1.2+/-2.5 per min; 0.40 degrees +/-0.20 degrees, 0.4+/-1.0 per min and 0.3 degrees +/-0.4 degrees, 5.0+/-8.7 per min respectively. No differences in MSWI characteristics were found between binocular and monocular viewing. Possible explanations for SI occurrence include experimental viewing conditions, subject fatigue and covert shifts in attention.