Motor imagery, forward models and the cerebellum: a commentary on Rieger et al., 2023.

In this commentary on Rieger et al., Psychological Research Psychologische Forschung, 2023, I discuss possible ways to test the hypothesis that action imagery is achieved by simulations of actions through an internal forward model. These include brain imaging, perturbation through TMS, and psychophysical tests of adaptation of intended reach actions.

Identifying the causal mechanisms of the quiet eye.

Scientists who have examined the gaze strategies employed by athletes have determined that longer quiet eye (QE) durations (QED) are characteristic of skilled compared to less-skilled performers. However, the cognitive mechanisms of the QE and, specifically, how the QED affects performance are not yet fully understood. We review research that has examined the functional mechanism underlying QE and discuss the neural networks that may be involved. We also highlight the limitations surrounding QE measurement and its definition and propose future research directions to address these shortcomings. Investigations into the behavioural and neural mechanisms of QE will aid the understanding of the perceptual and cognitive processes underlying expert performance and the factors that change as expertise develops.

Modulation of linguistic prediction by TDCS of the right lateral cerebellum.

It has been postulated recently that the cerebellum contributes the same prediction and learning functions to linguistic processing as it does towards motor control. For example, repetitive TMS over posterior-lateral cerebellum caused a significant loss in predictive language processing, as assessed by the latency of saccades to target items of spoken sentences, using the Visual World task. We aimed to assess the polarity-specific effects of cerebellar TDCS, hypothesising that cathodal TDCS should impair linguistic prediction, and anodal TDCS facilitate it. Our design also tested whether TDCS modulated associative learning in this task. A between groups (sham, anodal, cathodal) design was used, with concurrent stimulation during performance of a manual variation of the Visual World paradigm, and with assessment of latency reduction over repeated presentations of the spoken sentences. Mixed model ANOVA was used to analyse change in response latency. Cathodal TDCS decreased participants' response time advantage for the predictable sentence items without change for non-predictable items, consistent with the previous TMS results. Furthermore, anodal stimulation enhanced the response time advantage for the predictable items, again without change in latencies for non-predictive items. We found a clear practice-based effect over 4 blocks. However, this difference was not significantly modulated by either anodal or cathodal stimulation. Our results therefore support the hypothesis that cerebellum contributes to predictive language processing, mirroring its predictive role in motor control, but we do not yet have evidence that the learning process was affected by cerebellar TDCS.

The influence of stimulus format on drawing--a functional imaging study of decision making in portrait drawing.

To copy a natural visual image as a line drawing, visual identification and extraction of features in the image must be guided by top-down decisions, and is usually influenced by prior knowledge. In parallel with other behavioral studies testing the relationship between eye and hand movements when drawing, we report here a functional brain imaging study in which we compared drawing of faces and abstract objects: the former can be strongly guided by prior knowledge, the latter less so. To manipulate the difficulty in extracting features to be drawn, each original image was presented in four formats including high contrast line drawings and silhouettes, and as high and low contrast photographic images. We confirmed the detailed eye-hand interaction measures reported in our other behavioral studies by using in-scanner eye-tracking and recording of pen movements with a touch screen. We also show that the brain activation pattern reflects the changes in presentation formats. In particular, by identifying the ventral and lateral occipital areas that were more highly activated during drawing of faces than abstract objects, we found a systematic increase in differential activation for the face-drawing condition, as the presentation format made the decisions more challenging. This study therefore supports theoretical models of how prior knowledge may influence perception in untrained participants, and lead to experience-driven perceptual modulation by trained artists.

Non-invasive cerebellar stimulation--a consensus paper.

The field of neurostimulation of the cerebellum either with transcranial magnetic stimulation (TMS; single pulse or repetitive (rTMS)) or transcranial direct current stimulation (tDCS; anodal or cathodal) is gaining popularity in the scientific community, in particular because these stimulation techniques are non-invasive and provide novel information on cerebellar functions. There is a consensus amongst the panel of experts that both TMS and tDCS can effectively influence cerebellar functions, not only in the motor domain, with effects on visually guided tracking tasks, motor surround inhibition, motor adaptation and learning, but also for the cognitive and affective operations handled by the cerebro-cerebellar circuits. Verbal working memory, semantic associations and predictive language processing are amongst these operations. Both TMS and tDCS modulate the connectivity between the cerebellum and the primary motor cortex, tuning cerebellar excitability. Cerebellar TMS is an effective and valuable method to evaluate the cerebello-thalamo-cortical loop functions and for the study of the pathophysiology of ataxia. In most circumstances, DCS induces a polarity-dependent site-specific modulation of cerebellar activity. Paired associative stimulation of the cerebello-dentato-thalamo-M1 pathway can induce bidirectional long-term spike-timing-dependent plasticity-like changes of corticospinal excitability. However, the panel of experts considers that several important issues still remain unresolved and require further research. In particular, the role of TMS in promoting cerebellar plasticity is not established. Moreover, the exact positioning of electrode stimulation and the duration of the after effects of tDCS remain unclear. Future studies are required to better define how DCS over particular regions of the cerebellum affects individual cerebellar symptoms, given the topographical organization of cerebellar symptoms. The long-term neural consequences of non-invasive cerebellar modulation are also unclear. Although there is an agreement that the clinical applications in cerebellar disorders are likely numerous, it is emphasized that rigorous large-scale clinical trials are missing. Further studies should be encouraged to better clarify the role of using non-invasive neurostimulation techniques over the cerebellum in motor, cognitive and psychiatric rehabilitation strategies.

Graph network analysis of immediate motor-learning induced changes in resting state BOLD.

Recent studies have demonstrated that following learning tasks, changes in the resting state activity of the brain shape regional connections in functionally specific circuits. Here we expand on these findings by comparing changes induced in the resting state immediately following four motor tasks. Two groups of participants performed a visuo-motor joystick task with one group adapting to a transformed relationship between joystick and cursor. Two other groups were trained in either explicit or implicit procedural sequence learning. Resting state BOLD data were collected immediately before and after the tasks. We then used graph theory-based approaches that include statistical measures of functional integration and segregation to characterize changes in biologically plausible brain connectivity networks within each group. Our results demonstrate that motor learning reorganizes resting brain networks with an increase in local information transfer, as indicated by local efficiency measures that affect the brain's small world network architecture. This was particularly apparent when comparing two distinct forms of explicit motor learning: procedural learning and the joystick learning task. Both groups showed notable increases in local efficiency. However, a change in local efficiency in the inferior frontal and cerebellar regions also distinguishes between the two learning tasks. Additional graph analytic measures on the "non-learning" visuo-motor performance task revealed reversed topological patterns in comparison with the three learning tasks. These findings underscore the utility of graph-based network analysis as a novel means to compare both regional and global changes in functional brain connectivity in the resting state following motor learning tasks.

Secondary tasks impair adaptation to step- and gradual-visual displacements.

Motor adaptation is impaired by the performance of a secondary task which divides cognitive resources. Additionally, we previously reported slowed adaptation when participants were required to switch from one visual displacement adaptation task to another. Here, we examined whether a dividing secondary task had a similar effect on adaptation as switching between opposing visual displacements. The resource-dividing task involved simultaneously adapting to a step-visual displacement whilst vocally shadowing an auditory stimulus. The switching task required participants to adapt to opposing visual displacements in an alternating manner with the left and right hands. We found that both manipulations had a detrimental effect on adaptation rate. We then integrated these tasks and found the combination caused a greater decrease in adaptation rate than either manipulation in isolation. A second set of experiments showed that adaptation to a gradually imposed visual displacement was influenced in a similar manner to step adaptation. In summary, step adaptation slows the learning rate of gradual adaptation to a large degree, whereas gradual adaptation only slightly slows the learning rate of step adaptation. Therefore, although gradual adaptation involves minimal awareness it can still be disrupted with a cognitively demanding secondary task. We propose that awareness and cognitive resource can be regarded as qualitatively different, but that awareness may be a marker of the amount of resource required. For example, large errors are both noticed and require substantial cognitive resource. However, a lack of awareness does not mean an adaptation task will be resistant to interference from a resource-consuming secondary task.

The precision of temporal judgement: milliseconds, many minutes, and beyond.

The principle that the standard deviation of estimates scales with the mean estimate, commonly known as the scalar property, is one of the most broadly accepted fundamentals of interval timing. This property is measured using the coefficient of variation (CV) calculated as the ratio between the standard deviation and the mean. In 1997, John Gibbon suggested that different time measurement mechanisms may have different levels of absolute precision, and would therefore be associated with different CVs. Here, we test this proposal by examining the CVs produced by human subjects timing a broad range of intervals (68 ms to 16.7 min). Our data reveal no evidence for multiple mechanisms, but instead show a continuous logarithmic decrease in CV as timed intervals increase. This finding joins other recent reports in demonstrating a systematic violation of the scalar property in timing data. Interestingly, the estimated CV of circadian judgements fits onto the regression of decreasing CV, suggesting a link between short interval and circadian timing mechanisms.

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.

Asymmetric interlimb transfer of concurrent adaptation to opposing dynamic forces.

Interlimb transfer of a novel dynamic force has been well documented. It has also been shown that unimanual adaptation to opposing novel environments is possible if they are associated with different workspaces. The main aim of this study was to test if adaptation to opposing velocity dependent viscous forces with one arm could improve the initial performance of the other arm. The study also examined whether this interlimb transfer occurred across an extrinsic, spatial, coordinative system or an intrinsic, joint based, coordinative system. Subjects initially adapted to opposing viscous forces separated by target location. Our measure of performance was the correlation between the speed profiles of each movement within a force condition and an 'average' trajectory within null force conditions. Adaptation to the opposing forces was seen during initial acquisition with a significantly improved coefficient in epoch eight compared to epoch one. We then tested interlimb transfer from the dominant to non-dominant arm (D --> ND) and vice-versa (ND --> D) across either an extrinsic or intrinsic coordinative system. Interlimb transfer was only seen from the dominant to the non-dominant limb across an intrinsic coordinative system. These results support previous studies involving adaptation to a single dynamic force but also indicate that interlimb transfer of multiple opposing states is possible. This suggests that the information available at the level of representation allowing interlimb transfer can be more intricate than a general movement goal or a single perceived directional error.

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.

Evidence for stronger visuo-motor than visuo-proprioceptive conflict during mirror drawing performed by a deafferented subject and control subjects.

It has been proposed that mirror drawing is difficult because of the conflict between visual and proprioceptive signals from the arm. However, even without proprioception, there should be difficulties in planning movements to visual targets observed in a mirror, as the mirror-reversed spatial information must be translated into appropriate hand actions. Mirror drawing tasks suggest these planning conflicts are likely to be most obvious at corners, when encountering sharp changes in direction. We have therefore tested the speed of mirror drawing in a chronically deafferented man and in a control group of normal subjects, and hypothesized that increases in template complexity (number of corners) would result in reduced drawing speeds in all subjects. Indeed, all subjects, including the deafferented man, showed movement durations that increased linearly as the complexity of the drawings increased. However, the deafferented man was significantly faster than the control subjects at tracing curved templates. We suggest that the major difficulty in mirror tracking is in the visuo-motor planning of actions based on mirror-reversed visual information, and is not a conflict between visual and proprioceptive signals about arm motion.

Concurrent adaptation to opposing visual displacements during an alternating movement.

It has been suggested that, during tasks in which subjects are exposed to a visual rotation of cursor feedback, alternating bimanual adaptation to opposing rotations is as rapid as unimanual adaptation to a single rotation (Bock et al. in Exp Brain Res 162:513-519, 2005). However, that experiment did not test strict alternation of the limbs but short alternate blocks of trials. We have therefore tested adaptation under alternate left/right hand movement with opposing rotations. It was clear that the left and right hand, within the alternating conditions, learnt to adapt to the opposing displacements at a similar rate suggesting that two adaptive states were formed concurrently. We suggest that the separate limbs are used as contextual cues to switch between the relevant adaptive states. However, we found that during online correction the alternating conditions had a significantly slower rate of adaptation in comparison to the unimanual conditions. Control conditions indicate that the results are not directly due the alternation between limbs or to the constant switching of vision between the two eyes. The negative interference may originate from the requirement to dissociate the visual information of these two alternating displacements to allow online control of the two arms.

Adaptation to visual feedback delays in manual tracking: evidence against the Smith Predictor model of human visually guided action.

We report adaptation to delayed visual feedback during a manual tracking task, testing the nature of the adapted responses with frequency analysis. Two groups of seven subjects tracked unpredictable targets using a handheld joystick, alternating between pursuit and compensatory display trials. The test group then practised for 1 h per day with a visual feedback delay of 300 ms; the control group practice under normal undelayed conditions. Introduction of the visual feedback delay significantly disrupted tracking performance, with an increase in errors and a reduction in frequency of corrective movements. Subjects showed clear evidence of adaptation during the 5 day experiment, decreasing tracking error and decreasing the mean power of intermittent corrections. However, there was no evidence of a return towards the initial high frequency intermittent tracking. We suggest that the adaptation observed in this study reflects the modification of predictive feedforward actions, but that these data do not support control based on Smith Prediction.

A right hemispheric prefrontal system for cognitive time measurement.

Despite a growing body of neuroimaging data, little consensus has been reached regarding the neural correlates of temporal processing in humans. This paper presents a reanalysis of two previously published neuroimaging experiments, which used two different cognitive timing tasks and examined both sub- and supra-second intervals. By processing these data in an identical manner, this reanalysis allows valid comparison and contrasting across studies. Conjunction of these studies using inclusive masking reveals shared activity in right hemispheric dorsolateral and ventrolateral prefrontal cortex and anterior insula, supporting a general-purpose system for cognitive time measurement in the right hemispheric prefrontal cortex. Consideration of the patterns of activity in each dataset with respect to the others, and taking task characteristics into account, provides insight into the possible role of dorsolateral prefrontal cortex in working memory and of posterior parietal cortex and anterior cingulate in attentional processing during cognitive time measurement tasks.

Two waves of a long-lasting aftereffect of prism adaptation measured over 7 days.

Prism adaptation is a useful paradigm to study the integration and reorganization of various sensory modalities involved in sensory-motor tasks. By prolonging the prismatic aftereffect and well-timed observation, we aimed to dissociate the components and mechanisms involved in human prism adaptation by their differential decay and development time courses. Here, we show that a single session of prism adaptation training, combining small increments of prism strength below the subjects' awareness threshold, during a pointing task with a free walk session with total prism exposure duration of 75 min, generated a surprisingly long-lasting aftereffect. The aftereffect was measured by the magnitude of the proprioceptive shift (assessed by straight-ahead pointing in the dark) for 7 days. An aftereffect was observed, which lasted for more than 6 days, by a single prism adaptation session. The aftereffect did not decay gradually. Unlike previous descriptions, the aftereffect showed two separate time-courses of decay and increase. After a significant initial decay within 6 h, the aftereffect increased again from 1 day up to 3 days. The novel decay and delayed development profile of this adaptation aftereffect suggests two separate underlying neural mechanisms with different time scales. Our experimental paradigms promise to reveal directly the temporal characteristics of early versus late long-term neural plasticity in complex human adaptive behavior.

Performing hand actions assists the visual discrimination of similar hand postures.

Recent theoretical work has suggested that internal predictive signals are used for motor control and coordination. The predictive signal - proposed to be the output of a forward model - would be a sensory representation of action. Hence, these sensory representations could potentially influence other sensory processes. We report here how performance of hand actions assisted the visual discrimination of target hand postures presented at random times within an on-going series of hand images. Reaction times to discriminate the targets were significantly shorter when the displayed images were both sequential and congruent with the action being performed. Hence, the planning or execution of action appears to allow better prediction of a displayed series of congruent images. In further control experiments, we show that the motor-visual priming effect is unlikely to be due to differential attentional demands and it is specific to a first person perspective display; it is short lasting, being lost if a 500 ms delay is introduced between successive stimulus presentations. The data are interpreted as evidence supporting the hypothesis that forward models in the motor system provide action-specific sensory predictions that are available to cognitive processes.

Functional imaging of changes in cerebellar activity related to learning during a novel eye-hand tracking task.

Coordination between the eyes and the hand is likely to be based on a process of motor learning, so that the interactions between the two systems can be accurately controlled. By using an unusual tracking task we measured the change in brain activation levels, as recorded with 3T functional magnetic resonance imaging (fMRI), between naïve human subjects and the same subjects after a period of extended training. Initially the performance of the two groups was similar. One subject group was then trained in a synchronous, coordinated, eye-hand task; the other group trained with a 304 ms temporal offset between hand and eye tracking movements. After training, different patterns of performance were observed for the groups, and different functional activation profiles. Significant change in the relationship between functional activation levels and eye-hand task conditions was predominantly restricted to visuo-motor areas of the lateral and vermal cerebellum. In an additional test with one of the subject groups, we show that there was increased cerebellar activation after learning, irrespective of change in performance error. These results suggest that two factors contribute to the measured blood oxygen level-dependent (BOLD) signal. One declined with training and may be directly related to performance error. The other increased after training, in the test conditions nearest to the training condition, and may therefore be related to acquisition of experience in the task. The loci of activity changes suggest that improved performance is because of selective modified processing of ocular and manual control signals within the cerebellum. These results support the suggestion that coordination between eye and hand movement is based on an internal model acquired by the cerebellum that provides predictive signals linking the control of the two effectors.