Imprecise perception of hand position during early motor adaptation.

Localizing one's body parts is important for movement control and motor learning. Recent studies have shown that the precision with which people localize their hand places constraints on motor adaptation. Although these studies have assumed that hand localization remains equally precise across learning, we show that precision decreases rapidly during early motor learning. In three experiments, healthy young participants (n = 92) repeatedly adapted to a 45° visuomotor rotation for a cycle of two to four reaches, followed by a cycle of two to four reaches with veridical feedback. Participants either used an aiming strategy that fully compensated for the rotation (experiment 1), or always aimed directly at the target, so that adaptation was implicit (experiment 2). We omitted visual feedback for the last reach of each cycle, after which participants localized their unseen hand. We observed an increase in the variability of angular localization errors when subjects used a strategy to counter the visuomotor rotation (experiment 1). This decrease in precision was less pronounced in the absence of reaiming (experiment 2), and when subjects knew that they would have to localize their hand on the upcoming trial, and could thus focus on hand position (experiment 3). We propose that strategic reaiming decreases the precision of perceived hand position, possibly due to attention to vision rather than proprioception. We discuss how these dynamics in precision during early motor learning could impact on motor control and shape the interplay between implicit and strategy-based motor adaptation.NEW & NOTEWORTHY Recent studies indicate that the precision with which people localize their hand limits implicit visuomotor learning. We found that localization precision is not static, but decreases early during learning. This decrease is pronounced when people apply a reaiming strategy to compensate for a visuomotor perturbation and is partly resistant to allocation of attention to the hand. We propose that these dynamics in position sense during learning may influence how implicit and strategy-based motor adaption interact.

Rapid Compensation for Noisy Voluntary Movements in Adults with Primary Tic Disorders.

BACKGROUND: It has been proposed that tics and premonitory urges in primary tic disorders (PTD), like Tourette syndrome, are a manifestation of sensorimotor noise. However, patients with tics show no obvious movement imprecision in everyday life. One reason could be that patients have strategies to compensate for noise that disrupts performance (ie, noise that is task-relevant). OBJECTIVES: Our goal was to unmask effects of elevated sensorimotor noise on the variability of voluntary movements in patients with PTD. METHODS: We tested 30 adult patients with PTD (23 male) and 30 matched controls in a reaching task designed to unmask latent noise. Subjects reached to targets whose shape allowed for variability either in movement direction or extent. This enabled us to decompose variability into task-relevant versus less task-relevant components, where the latter should be less affected by compensatory strategies than the former. In alternating blocks, the task-relevant target dimension switched, allowing us to explore the temporal dynamics with which participants adjusted movement variability to changes in task demands. RESULTS: Both groups accurately reached to targets, and adjusted movement precision based on target shape. However, when task-relevant dimensions of the target changed, patients initially produced movements that were more variable than controls, before regaining precision after several reaches. This effect persisted across repeated changes in the task-relevant dimension across the experiment, and therefore did not reflect an effect of novelty, or differences in learning. CONCLUSIONS: Our results suggest that patients with PTD generate noisier voluntary movements compared with controls, but rapidly compensate according to current task demands. © 2024 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Strategy-based motor learning decreases the post-movement ß power.

Motor learning depends on the joint contribution of several processes including cognitive strategies aiming at goal achievement and prediction error-driven implicit adaptation. Understanding this functional interplay and its clinical implications requires insight into the individual learning processes, including at a neural level. Here, we set out to examine the impact of learning a cognitive strategy, over and above implicit adaptation, on the oscillatory post-movement ß rebound (PMBR), which typically decreases in power following (visuo)motor perturbations. Healthy participants performed reaching movements towards a target, with online visual feedback replacing the view of their moving hand. The feedback was sometimes rotated, either relative to their movements (visuomotor rotation) or invariant to their movements (and relative to the target; clamped feedback), always for two consecutive trials interspersed between non-rotated trials. In both conditions, the first trial with a rotation was unpredictable. On the second trial, the task was either to re-aim, and thereby compensate for the rotation experienced in the first trial (visuomotor rotation; Compensate condition), or to ignore the rotation and keep on aiming at the target (clamped feedback; Ignore condition). After-effects did not differ between conditions, indicating that the amount of implicit learning was similar, while large differences in movement direction in the second rotated trial between conditions indicated that participants successfully acquired re-aiming strategies. Importantly, PMBR power following the first rotated trial was modulated differently in the two conditions. Specifically, it decreased in both conditions, but this effect was larger when participants had to acquire a cognitive strategy and prepare to re-aim. Our results therefore suggest that the PMBR is modulated by cognitive demands of motor learning, possibly reflecting the evaluation of a behaviourally significant goal achievement error.

Can moving in a redundant workspace accelerate motor adaptation?

Variability in behavior can be a manifestation of unwanted noise. However, variability can also reflect exploration and benefit learning. For example, it has been shown that interindividual differences in motor learning can be partly explained by differences in movement variability at baseline. Here, we examined whether permitting versus constraining movement variability via target shape alters motor learning rate in one and the same individual. Healthy young subjects made reaching movements to visual targets in two-dimensional space with their unseen hand. During an initial priming phase, the shape of targets allowed for movement variability either in direction (arc-shaped targets), or, in a separate session, in extent (radially oriented line-shaped targets), while requiring highly precise movements in the other spatial dimension, respectively. In subsequent test phases in each session, we quantified the rate of (single-trial) motor adaptation to visuomotor perturbations along these two spatial dimensions (rotation and gain). During priming, we observed higher variability in movement direction for arc-shaped targets, compared with radial line-shaped targets, and vice versa for variability in movement extent. As predicted, participants adapted more to a visuomotor rotation following priming with arc-shaped targets, compared with radial line-shaped targets, and vice versa for adaptation to a change in visuomotor gain. This effect was prominent in the part of the examined workspace where variability in initial movement trajectories was highest, suggesting high planning noise. Our results suggest that workspace redundancy can modulate motor adaptation in a spatially specific manner, however, this modulation may depend on the level of planning noise.NEW & NOTEWORTHY Interindividual differences in motor adaptation are partly explained by differences in movement variability. Movement variability is higher in a redundant workspace. Can workspace redundancy increase adaptation? In a within-subject experiment, we show that moving in a workspace that permits versus constrains movement variability in a given spatial dimension modulates adaptation rate in that dimension, at least in part of the workspace where initial movement trajectories vary most, indicating planning noise. Redundant workspaces might aid rehabilitation.

Non-invasive recording of high-frequency signals from the human spinal cord.

Throughout the somatosensory system, neuronal ensembles generate high-frequency signals in the range of several hundred Hertz in response to sensory input. High-frequency signals have been related to neuronal spiking, and could thus help clarify the functional architecture of sensory processing. Recording high-frequency signals from subcortical regions, however, has been limited to clinical pathology whose treatment allows for invasive recordings. Here, we demonstrate the feasibility to record 200-1200 Hz signals from the human spinal cord non-invasively, and in healthy individuals. Using standard electroencephalography equipment in a cervical electrode montage, we observed high-frequency signals between 200 and 1200 Hz in a time window between 8 and 16 ms after electric median nerve stimulation (n = 15). These signals overlapped in latency, and, partly, in frequency, with signals obtained via invasive, epidural recordings from the spinal cord in a patient with neuropathic pain. Importantly, the observed high-frequency signals were dissociable from classic spinal evoked responses. A spatial filter that optimized the signal-to-noise ratio of high-frequency signals led to submaximal amplitudes of the evoked response, and vice versa, ruling out the possibility that high-frequency signals are merely a spectral representation of the evoked response. Furthermore, we observed spontaneous fluctuations in the amplitude of high-frequency signals over time, in the absence of any concurrent, systematic change to the evoked response. High-frequency, "spike-like" signals from the human spinal cord thus carry information that is complementary to the evoked response. The possibility to assess these signals non-invasively provides a novel window onto the neurophysiology of the human spinal cord, both in a context of top-down control over perception, as well as in pathology.

A Psychophysical Window onto the Subjective Experience of Compulsion.

In this perspective, we follow the idea that an integration of cognitive models with sensorimotor theories of compulsion is required to understand the subjective experience of compulsive action. We argue that cognitive biases in obsessive-compulsive disorder may obscure an altered momentary, pre-reflective experience of sensorimotor control, whose detection thus requires an implicit experimental operationalization. We propose that a classic psychophysical test exists that provides this implicit operationalization, i.e., the intentional binding paradigm. We show how intentional binding can pit two ideas against each other that are fundamental to current sensorimotor theories of compulsion, i.e., the idea of excessive conscious monitoring of action, and the idea that patients with obsessive-compulsive disorder compensate for diminished conscious access to "internal states", including states of the body, by relying on more readily observable proxies. Following these ideas, we develop concrete, testable hypotheses on how intentional binding changes under the assumption of different sensorimotor theories of compulsion. Furthermore, we demonstrate how intentional binding provides a touchstone for predictive coding accounts of obsessive-compulsive disorder. A thorough empirical test of the hypotheses developed in this perspective could help explain the puzzling, disabling phenomenon of compulsion, with implications for the normal subjective experience of human action.

Spatial Filtering of Electroencephalography Reduces Artifacts and Enhances Signals Related to Spinal Cord Stimulation (SCS).

OBJECTIVES: How spinal cord stimulation (SCS) in its different modes suppresses pain is poorly understood. Mechanisms of action may reside locally in the spinal cord, but also involve a larger network including subcortical and cortical brain structures. Tonic, burst, and high-frequency modes of SCS can, in principle, entrain distinct temporal activity patterns in this network, but finally have to yield specific effects on pain suppression. Here, we employ high-density electroencephalography (EEG) and recently developed spatial filtering techniques to reduce SCS artifacts and to enhance EEG signals specifically related to neuromodulation by SCS. MATERIALS AND METHODS: We recorded high-density resting-state EEGs in patients suffering from pain of various etiologies under different modes of SCS. We established a pipeline for the robust spectral analysis of oscillatory brain activity during SCS, which includes spatial filtering for attenuation of pulse artifacts and enhancement of brain activity potentially modulated by SCS. RESULTS: In sensor regions responsive to SCS, neuromodulation strongly reduced activity in the theta and low alpha range (6-10 Hz) in all SCS modes. Results were consistent in all patients, and in accordance with thalamocortical dysrhythmia hypothesis of pain. Only in the tonic mode showing paresthesia as side effect, SCS also consistently and strongly reduced high-gamma activity (>84 Hz). CONCLUSIONS: EEG spectral analysis combined with spatial filtering allows for a spatially and temporally specific assessment of SCS-related, neuromodulatory EEG activity, and may help to disentangle therapeutic and side effects of SCS.

Error-Related Dynamics of Reaction Time and Frontal Midline Theta Activity in Attention Deficit Hyperactivity Disorder (ADHD) During a Subliminal Motor Priming Task.

Post-error slowing (PES) is an established performance monitoring readout. Several previous studies have found that PES is reduced in children and adolescents with attention-deficit hyperactivity disorder (ADHD). We analyzed reaction time data, along with electroencephalography (EEG) data, from a response priming experiment in children and adolescents with ADHD (N = 28) and typically developing (TD) controls (N = 15) between 10 and 17 years of age. We report dynamic reaction time changes before and after errors: whereas TD controls readjusted their response speed to their individual average speed after committing an error, this reaction time adjustment appeared to be delayed and decreased in ADHD patients. In the EEG, error trials were accompanied by increased frontal midline theta activity, which was attenuated in ADHD compared to TD. We conclude that PES has a different time course rather than being fully absent in ADHD and discuss relationships with our EEG findings and potential implications for performance monitoring in ADHD.

Intact automatic motor inhibition in patients with tourette syndrome.

BACKGROUND: Behavioral disinhibition has been proposed as a key mechanism in Tourette syndrome. Yet classic inhibition tasks have yielded inconsistent results, likely reflecting interference by strategies compensating for tic release. METHODS: We examined a core inhibitory function that is immune to such interference because it suppresses movements automatically. We measured automatic motor inhibition behaviorally in 21 adults with Tourette syndrome and 21 healthy controls via the negative compatibility effect. When a motor response is activated, for example, by a subliminal prime stimulus, but execution is delayed, activation turns into inhibition, increasing reaction time and error. Diminished automatic inhibition could underlie tic release. RESULTS: Both controls and patients showed strong automatic motor inhibition with no significant group difference. Bayesian statistics, allowing inference on the absence of effects, favored intact inhibition in patients. Our study was well powered. CONCLUSIONS: Automatic motor inhibition in Tourette syndrome is neither impaired nor harnessed by compensation. © 2018 International Parkinson and Movement Disorder Society.

Intact automatic motor inhibition in attention deficit hyperactivity disorder.

Hyperactivity and impulsivity are defining symptoms of attention-deficit hyperactivity disorder (ADHD), next to inattention. Hyperactive and impulsive behavior in ADHD is often thought to result from a deficit in inhibitory motor control. However, testing for such a deficit is complicated by coexisting deficits in ADHD, specifically an impairment in maintaining task set, e.g., due to inattention. Typical inhibition paradigms, such as Stop-signal, Go/NoGo or Flanker paradigms, are susceptible to a fundamental confound between inhibition and inattention because inhibition is an explicit goal in these tasks. We eliminate this confound by studying the negative compatibility effect (NCE), reflecting a core inhibitory function in the human motor system which, in healthy individuals, inhibits movements automatically, i.e., without deliberation or even conscious awareness. Our behavioral analysis, including Bayesian model comparison, as well as the time-course of the lateralized readiness potential (LRP), consistently show that this function is intact in children with ADHD compared to healthy controls, independent of the presence or absence of prominent hyperactive-impulsive symptoms. We conclude that hyperactivity and impulsivity in ADHD do not result from a low-level deficit in motor inhibition.

Acting without being in control: Exploring volition in Parkinson's disease with impulsive compulsive behaviours.

BACKGROUND: Several aspects of volitional control of action may be relevant in the pathophysiology of impulsive-compulsive behaviours (ICB) in Parkinson's disease (PD). We aimed to explore multiple aspects of action control, assessing reward-related behaviour, inhibition (externally and internally triggered) and sense of agency in PD patients, with and without ICB compared to healthy subjects. METHODS: Nineteen PD patients with ICB (PD-ICB), 19 PD without ICB (PD-no-ICB) and 19 healthy controls (HC) underwent a battery of tests including: Intentional Binding task which measures sense of agency; Stop Signal Reaction Time (SSRT) measuring capacity for reactive inhibition; the Marble task, assessing intentional inhibition; Balloon Analog Risk Task for reward sensitivity. RESULTS: One-way ANOVA showed significant main effect of group for action binding (p = 0.004, F = 6.27). Post hoc analysis revealed that PD-ICB had significantly stronger action binding than HC (p = 0.004), and PD-no-ICB (p = 0.04). There was no difference between PD-no-ICB and HC. SSRT did not differ between PD groups, whereas a significant difference between PD-no-ICB and HC was detected (p = 0.01). No other differences were found among groups in the other tasks. CONCLUSIONS: PD patients with ICB have abnormal performance on a psychophysical task assessing sense of agency, which might be related to a deficit in action representation at cognitive/experiential level. Yet, they have no deficit on tasks evaluating externally and internally triggered inhibitory control, or in reward-based decision-making. We conclude that impaired sense of agency may be a factor contributing to ICB in PD patients.

Perimovement decrease of alpha/beta oscillations in the human nucleus accumbens.

The human nucleus accumbens is thought to play an important role in guiding future action selection via an evaluation of current action outcomes. Here we provide electrophysiological evidence for a more direct, i.e., online, role during action preparation. We recorded local field potentials from the nucleus accumbens in patients with epilepsy undergoing surgery for deep brain stimulation. We found a consistent decrease in the power of alpha/beta oscillations (10-30 Hz) before and around the time of movements. This perimovement alpha/beta desynchronization was observed in seven of eight patients and was present both before instructed movements in a serial reaction time task as well as before self-paced, deliberate choices in a decision making task. A similar beta decrease over sensorimotor cortex and in the subthalamic nucleus has been directly related to movement preparation and execution. Our results support the idea of a direct role of the human nucleus accumbens in action preparation and execution.

Changing pattern in the basal ganglia: motor switching under reduced dopaminergic drive.

Action selection in the basal ganglia is often described within the framework of a standard model, associating low dopaminergic drive with motor suppression. Whilst powerful, this model does not explain several clinical and experimental data, including varying therapeutic efficacy across movement disorders. We tested the predictions of this model in patients with Parkinson's disease, on and off subthalamic deep brain stimulation (DBS), focussing on adaptive sensory-motor responses to a changing environment and maintenance of an action until it is no longer suitable. Surprisingly, we observed prolonged perseverance under on-stimulation, and high inter-individual variability in terms of the motor selections performed when comparing the two conditions. To account for these data, we revised the standard model exploring its space of parameters and associated motor functions and found that, depending on effective connectivity between external and internal parts of the globus pallidus and saliency of the sensory input, a low dopaminergic drive can result in increased, dysfunctional, motor switching, besides motor suppression. This new framework provides insight into the biophysical mechanisms underlying DBS, allowing a description in terms of alteration of the signal-to-baseline ratio in the indirect pathway, which better account of known electrophysiological data in comparison with the standard model.

No unified reward prediction error in local field potentials from the human nucleus accumbens: evidence from epilepsy patients.

Functional magnetic resonance imaging (fMRI), cyclic voltammetry, and single-unit electrophysiology studies suggest that signals measured in the nucleus accumbens (Nacc) during value-based decision making represent reward prediction errors (RPEs), the difference between actual and predicted rewards. Here, we studied the precise temporal and spectral pattern of reward-related signals in the human Nacc. We recorded local field potentials (LFPs) from the Nacc of six epilepsy patients during an economic decision-making task. On each trial, patients decided whether to accept or reject a gamble with equal probabilities of a monetary gain or loss. The behavior of four patients was consistent with choices being guided by value expectations. Expected value signals before outcome onset were observed in three of those patients, at varying latencies and with nonoverlapping spectral patterns. Signals after outcome onset were correlated with RPE regressors in all subjects. However, further analysis revealed that these signals were better explained as outcome valence rather than RPE signals, with gamble gains and losses differing in the power of beta oscillations and in evoked response amplitudes. Taken together, our results do not support the idea that postsynaptic potentials in the Nacc represent a RPE that unifies outcome magnitude and prior value expectation. We discuss the generalizability of our findings to healthy individuals and the relation of our results to measurements of RPE signals obtained from the Nacc with other methods.

Cortical drive of low-frequency oscillations in the human nucleus accumbens during action selection.

The nucleus accumbens is thought to contribute to action selection by integrating behaviorally relevant information from multiple regions, including prefrontal cortex. Studies in rodents suggest that information flow to the nucleus accumbens may be regulated via task-dependent oscillatory coupling between regions. During instrumental behavior, local field potentials (LFP) in the rat nucleus accumbens and prefrontal cortex are coupled at delta frequencies (Gruber AJ, Hussain RJ, O'Donnell P. PLoS One 4: e5062, 2009), possibly mediating suppression of afferent input from other areas and thereby supporting cortical control (Calhoon GG, O'Donnell P. Neuron 78: 181-190, 2013). In this report, we demonstrate low-frequency cortico-accumbens coupling in humans, both at rest and during a decision-making task. We recorded LFP from the nucleus accumbens in six epilepsy patients who underwent implantation of deep brain stimulation electrodes. All patients showed significant coherence and phase-synchronization between LFP and surface EEG at delta and low theta frequencies. Although the direction of this coupling as indexed by Granger causality varied between subjects in the resting-state data, all patients showed a cortical drive of the nucleus accumbens during action selection in a decision-making task. In three patients this was accompanied by a significant coherence increase over baseline. Our results suggest that low-frequency cortico-accumbens coupling represents a highly conserved regulatory mechanism for action selection.

Dynamic tuning of tactile localization to body posture.

Localizing touch in space is essential for goal-directed action. Because body posture changes, the brain must transform tactile coordinates from an initial skin-based representation to external space by integrating information about current posture. This process, referred to as tactile remapping, generally results in accurate localization, but accuracy drops when skin-based and external spatial representations of touch are conflicting, e.g., after crossing the limbs. Importantly, frequent experience of such postures can improve localization. This suggests that remapping may not only integrate current sensory input but also prior experience. Here, we demonstrate that this can result in rapid changes in localization performance over the course of few trials. We obtained an implicit measure of tactile localization by studying the perceived temporal order of two touches, one on each hand. Crucially, we varied the number of consecutive trials during which participants held their arms crossed or uncrossed. As expected, accuracy dropped immediately after the arms had been crossed. Importantly, this was followed by a progressive recovery if posture was maintained, despite the absence of performance feedback. Strikingly, a significant improvement was already evident in the localization of the second pair of touches. This rapid improvement required preceding touch in the same posture and did not occur merely as a function of time. Moreover, even touches that were not task relevant led to improved localization of subsequent touch. Our findings show that touches are mapped from skin to external space as a function of recent tactile experience.

Parallel processing streams for motor output and sensory prediction during action preparation.

Sensory consequences of one's own actions are perceived as less intense than identical, externally generated stimuli. This is generally taken as evidence for sensory prediction of action consequences. Accordingly, recent theoretical models explain this attenuation by an anticipatory modulation of sensory processing prior to stimulus onset (Roussel et al. 2013) or even action execution (Brown et al. 2013). Experimentally, prestimulus changes that occur in anticipation of self-generated sensations are difficult to disentangle from more general effects of stimulus expectation, attention and task load (performing an action). Here, we show that an established manipulation of subjective agency over a stimulus leads to a predictive modulation in sensory cortex that is independent of these factors. We recorded magnetoencephalography while subjects performed a simple action with either hand and judged the loudness of a tone caused by the action. Effector selection was manipulated by subliminal motor priming. Compatible priming is known to enhance a subjective experience of agency over a consequent stimulus (Chambon and Haggard 2012). In line with this effect on subjective agency, we found stronger sensory attenuation when the action that caused the tone was compatibly primed. This perceptual effect was reflected in a transient phase-locked signal in auditory cortex before stimulus onset and motor execution. Interestingly, this sensory signal emerged at a time when the hemispheric lateralization of motor signals in M1 indicated ongoing effector selection. Our findings confirm theoretical predictions of a sensory modulation prior to self-generated sensations and support the idea that a sensory prediction is generated in parallel to motor output (Walsh and Haggard 2010), before an efference copy becomes available.