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.

Cortical cellular encoding of thermotactile integration.

Recent evidence suggests that primary sensory cortical regions play a role in the integration of information from multiple sensory modalities. How primary cortical neurons integrate different sources of sensory information is unclear, partly because non-primary sensory input to a cortical sensory region is often weak or modulatory. To address this question, we take advantage of the robust representation of thermal (cooling) and tactile stimuli in mouse forelimb primary somatosensory cortex (fS1). Using a thermotactile detection task, we show that the perception of threshold-level cool or tactile information is enhanced when they are presented simultaneously, compared with presentation alone. To investigate the cortical cellular correlates of thermotactile integration, we performed in vivo extracellular recordings from fS1 in awake resting and anesthetized mice during unimodal and bimodal stimulation of the forepaw. Unimodal stimulation evoked thermal- or tactile- specific excitatory and inhibitory responses of fS1 neurons. The most prominent features of combined thermotactile stimulation are the recruitment of unimodally silent fS1 neurons, non-linear integration features, and response dynamics that favor longer response durations with additional spikes. Together, we identify quantitative and qualitative changes in cortical encoding that may underlie the improvement in perception of thermotactile surfaces during haptic exploration.

Active self-touch restores bodily proprioceptive spatial awareness following disruption by 'rubber hand illusion'.

Bodily self-awareness relies on a constant integration of visual, tactile, proprioceptive, and motor signals. In the 'rubber hand illusion' (RHI), conflicting visuo-tactile stimuli lead to changes in self-awareness. It remains unclear whether other, somatic signals could compensate for the alterations in self-awareness caused by visual information about the body. Here, we used the RHI in combination with robot-mediated self-touch to systematically investigate the role of tactile, proprioceptive and motor signals in maintaining and restoring bodily self-awareness. Participants moved the handle of a leader robot with their right hand and simultaneously received corresponding tactile feedback on their left hand from a follower robot. This self-touch stimulation was performed either before or after the induction of a classical RHI. Across three experiments, active self-touch delivered after-but not before-the RHI, significantly reduced the proprioceptive drift caused by RHI, supporting a restorative role of active self-touch on bodily self-awareness. The effect was not present during involuntary self-touch. Unimodal control conditions confirmed that both tactile and motor components of self-touch were necessary to restore bodily self-awareness. We hypothesize that active self-touch transiently boosts the precision of proprioceptive representation of the touched body part, thus counteracting the visual capture effects that underlie the RHI.

Autonomous behaviour and the limits of human volition.

Humans and some other animals can autonomously generate action choices that contribute to solving complex problems. However, experimental investigations of the cognitive bases of human autonomy are challenging, because experimental paradigms typically constrain behaviour using controlled contexts, and elicit behaviour by external triggers. In contrast, autonomy and freedom imply unconstrained behaviour initiated by endogenous triggers. Here we propose a new theoretical construct of adaptive autonomy, meaning the capacity to make behavioural choices that are free from constraints of both immediate external triggers and of routine response patterns, but nevertheless show appropriate coordination with the environment. Participants (N = 152) played a competitive game in which they had to choose the right time to act, in the face of an opponent who punished (in separate blocks) either choice biases (such as always responding early), sequential patterns of action timing across trials (such as early, late, early, late…), or predictable action-outcome dependence (such as win-stay, lose-shift). Adaptive autonomy was quantified as the ability to maintain performance when each of these influences on action selection was punished. We found that participants could become free from habitual choices regarding when to act and could also become free from sequential action patterns. However, they were not able to free themselves from influences of action-outcome dependence, even when these resulted in poor performance. These results point to a new concept of autonomous behaviour as flexible adaptation of voluntary action choices in a way that avoids stereotypy. In a sequential analysis, we also demonstrated that participants increased their reliance on belief learning in which they attempt to understand the competitor's beliefs and intentions, when transition bias and reinforcement bias were punished. Taken together, our study points to a cognitive mechanism of adaptive autonomy in which competitive interactions with other agents could promote both social cognition and volition in the form of non-stereotyped action choices.

Revisiting a classical theory of sensory specificity: assessing consistency and stability of thermosensitive spots.

Thermal sensitivity is not uniform across the skin, and is particularly high in small (∼1 mm2) regions termed "thermosensitive spots." These spots are thought to reflect the anatomical location of specialized thermosensitive nerve endings from single primary afferents. Thermosensitive spots provide foundational support for "labeled line" or specificity theory of sensory perception, which states that different sensory qualities are transmitted by separate and specific neural pathways. This theory predicts a highly stable relation between repetitions of a thermal stimulus and the resulting sensory quality, yet these predictions have rarely been tested systematically. Here, we present the qualitative, spatial, and repeatability properties of 334 thermosensitive spots on the dorsal forearm sampled across four separate sessions. In line with previous literature, we found that spots associated with cold sensations (112 cold spots, 34%) were more frequent than spots associated with warm sensations (41 warm spots, 12%). Still more frequent (165 spots, 49%) were spots that elicited inconsistent sensations when repeatedly stimulated by the same temperature. Remarkably, only 13 spots (4%) conserved their position between sessions. Overall, we show unexpected inconsistency of both the perceptual responses elicited by spot stimulation and of spot locations across time. These observations suggest reappraisals of the traditional view that thermosensitive spots reflect the location of individual thermosensitive, unimodal primary afferents serving as specific labeled lines for corresponding sensory qualities.NEW & NOTEWORTHY Thermosensitive spots are clustered rather than randomly distributed and have the highest density near the wrist. Surprisingly, we found that thermosensitive spots elicit inconsistent sensory qualities and are unstable over time. Our results question the widely believed notion that thermosensitive spots reflect the location of individual thermoreceptive, unimodal primary afferents that serve as labelled lines for corresponding sensory qualities.

Quantifying spatial acuity of frequency resolved midair ultrasound vibrotactile stimuli.

Spatial acuity is a fundamental property of any sensory system. In the case of the somatosensory system, the two-point discrimination (2PD) test has long been used to investigate tactile spatial resolution. However, the somatosensory system comprises three main mechanoreceptive channels: the slowly adapting channel (SA) responds to steady pressure, the rapidly adapting channel (RA) responds to low-frequency vibration, and the Pacinian channel (PC) responds to high-frequency vibration. The use of mechanical stimuli in the classical 2PD test means that previous studies on tactile acuity have primarily focussed on the pressure-sensitive channel alone, while neglecting other submodalities. Here, we used a novel ultrasound stimulation to systematically investigate the spatial resolution of the two main vibrotactile channels. Contrary to the textbook view of poor spatial resolution for PC-like stimuli, across four experiments we found that high-frequency vibration produced surprisingly good spatial acuity. This effect remained after controlling for interchannel differences in stimulus detectability and perceived intensity. Laser doppler vibrometry experiments confirmed that the acuity of the PC channel was not simply an artifact of the skin's resonance to high-frequency mechanical stimulation. Thus, PC receptors may transmit substantial spatial information, despite their sparse distribution, deep location, and large receptive fields.

Metacognition and sense of agency.

Intelligent agents need to understand how they can change the world, and how they cannot change it, in order to make rational decisions for their forthcoming actions, and to adapt to their current environment. Previous research on the sense of agency, based largely on subjective ratings, failed to dissociate the sensitivity of sense of agency (i.e., the extent to which individual sense of agency tracks actual instrumental control over external events) from judgment criteria (i.e., the extent to which individuals self-attribute agency independent of their actual influence over external events). Furthermore, few studies have examined whether individuals have metacognitive access to the internal processes underlying the sense of agency. We developed a novel two-alternative-forced choice (2FAC) control detection task, in which participants identified which of two visual objects was more strongly controlled by their voluntary movement. The actual level of control over the target object was manipulated by adjusting the proportion of its motion that was driven by the participant's movement, compared to the proportion driven by a pre-recorded movement by another agent, using a staircase to hold 2AFC control detection accuracy at 70%. Participants identified which of the two visual objects they controlled, and also made a binary confidence judgment regarding their control detection judgment. We calculated a bias-free measure of first-order sensitivity (d') for detection control at any given level of participant's own movement. The proportion of pre-recorded movements determined by the stairecase could then be used as an index of control detection ability. We identified two distinct processes underlying first-order detection of control: one based on instantaneous sensory predictions for the current movement, and one based on detection of a regular motor-visual relation across a series of movements. Further, we found large individual differences across 40 particpants in metacognitive sensitivity (meta-d') even though first-order sensitivity of control detection was well controlled. Using structural equation modelling (SEM), we showed that metacognition was negatively correlated with the predictive process component of detection of control. This result is inconsistent with previous hypotheses that detection of control relies on metacognitive monitoring of a predictive circuit. Instead, it suggests that predictive mechanisms that compute sense of agency may operate unconsciously.

The perception of pain, discriminative touch and affective touch in patients suffering from Borderline Personality Disorder.

Borderline Personality Disorder (BPD) is often characterized by self-injurious behaviors, with one-half to two-third of these patients reporting hypalgesic or analgesic phenomena during self-harming. Research on pain perception in BPD suggested abnormal processing of nociception either within the sensory-discriminative and/or motivational-affective systems of pain. Nevertheless, it is still unclear whether pain insensitivity could be generalized to other somatosensory submodalities. To investigate this question, 30 BPD patients and 30 matched healthy controls were enrolled in the current study and underwent a somatosensory battery composed of well-established psychophysical test assessing all the principal submodalities of somatosensation, namely pain perception (i.e., warm, cold and mechanical), discriminative touch (i.e., tactile acuity and tactile sensitivity) as well as affective touch. Results showed abnormal warm detection threshold, warm pain threshold, mechanical pain perception, and tactile sensitivity in BPD patients, but no differences emerged neither for tactile acuity nor for cold pain thresholds, cold tolerance, or for affective touch perception. Findings point to a deficit in nociception, as well as in tactile sensitivity in BPD individuals, and were discussed in relation to BPD clinical features including self-injurious behaviors.

Implicit signatures of voluntary action reduce with repeated motor practice.

The sense of controlling one's actions and their consequences is a critical aspect of successful motor activity. While motor performance typically improves with learning, it is unclear whether, how, and why higher order aspects of motor cognition are also affected. Here, we used an implicit measure of sense of agency-the 'intentional binding' effect-as participants learned to make a skilled action involving precise control of thumb adduction. These actions were predictably followed by a tone (the outcome). At pre-test, we showed the perceived time of the tone was shifted towards the thumb action, compared to a control condition in which tones occurred without actions. Next, a relevant training group learned to refine the direction of the thumb movement, while an irrelevant training group was trained on another movement. Manipulation checks demonstrated that, as expected, the relevant training group improved performance of the trained movement, while the irrelevant training group did not. Critically, while both groups still showed binding of the tone towards the thumb action at post-test, the relevant training group showed less binding than the irrelevant training group. Given the link between intentional binding and volitional control of action, we suggest our result demonstrates subjective agency over the outcome of a skilled action decreases as practice makes the skilled action more fluent. We suggest that this reduction in sense of agency over movement outcomes is consistent with the decreasing cognitive engagement, or automatization, that occurs during skill learning.

Human primary motor cortex indexes the onset of subjective intention in brain-machine-interface mediated actions.

Self-initiated behavior is accompanied by the experience of willing our actions. Here, we leverage the unique opportunity to examine the full intentional chain - from will (W) to action (A) to environmental effects (E) - in a tetraplegic person fitted with a primary motor cortex (M1) brain machine interface (BMI) generating hand movements via neuromuscular electrical stimulation (NMES). This combined BMI-NMES approach allowed us to selectively manipulate each element of the intentional chain (W, A, and E) while performing extra-cellular recordings and probing subjective experience. Our results reveal single-cell, multi-unit, and population-level dynamics in human M1 that encode W and may predict its subjective onset. Further, we show that the proficiency of a neural decoder in M1 reflects the degree of W-A binding, tracking the participant's subjective experience of intention in (near) real time. These results point to M1 as a critical node in forming the subjective experience of intention and demonstrate the relevance of intention-related signals for translational neuroprosthetics.

Mistaking opposition for autonomy: psychophysical studies on detecting choice bias.

Do people know when they act freely and autonomously versus when their actions are influenced? While the human aspiration to freedom is widespread, little research has investigated how people perceive whether their choices are biased. Here, we explored how actions congruent or incongruent with suggestions are perceived as influenced or free. Across three experiments, participants saw directional stimuli cueing left or right manual responses. They were instructed to follow the cue's suggestion, oppose it or ignore it entirely to make a 'free' choice. We found that we could bias participants' 'free responses' towards adherence or opposition, by making one instruction more frequent than the other. Strikingly, participants consistently reported feeling less influenced by cues to which they responded incongruently, even when response habits effectively biased them towards such opposition behaviour. This effect was so compelling that cues that were frequently presented with the Oppose instruction became systematically judged as having less influence on behaviour, artificially increasing the sense of freedom of choice. Taken together, these findings demonstrate that acting contrarian distorts the perception of autonomy. Crucially, we demonstrate the existence of a novel illusion of freedom evoked by trained opposition. Our results have important implications for understanding mechanisms of persuasion.

A framework for focal and connectomic mapping of transiently disrupted brain function.

The distributed nature of the neural substrate, and the difficulty of establishing necessity from correlative data, combine to render the mapping of brain function a far harder task than it seems. Methods capable of combining connective anatomical information with focal disruption of function are needed to disambiguate local from global neural dependence, and critical from merely coincidental activity. Here we present a comprehensive framework for focal and connective spatial inference based on sparse disruptive data, and demonstrate its application in the context of transient direct electrical stimulation of the human medial frontal wall during the pre-surgical evaluation of patients with focal epilepsy. Our framework formalizes voxel-wise mass-univariate inference on sparsely sampled data within the statistical parametric mapping framework, encompassing the analysis of distributed maps defined by any criterion of connectivity. Applied to the medial frontal wall, this transient dysconnectome approach reveals marked discrepancies between local and distributed associations of major categories of motor and sensory behaviour, revealing differentiation by remote connectivity to which purely local analysis is blind. Our framework enables disruptive mapping of the human brain based on sparsely sampled data with minimal spatial assumptions, good statistical efficiency, flexible model formulation, and explicit comparison of local and distributed effects.

Feeling ready: neural bases of prospective motor readiness judgements.

The idea that human agents voluntarily control their actions, including their spontaneous movements, strongly implies an anticipatory awareness of action. That is, agents should be aware they are about to act before actually executing a movement. Previous research has identified neural signals that could underpin prospective conscious access to motor preparation, including the readiness potential and the beta-band event-related desynchronization. In this study, we ran two experiments to test whether these two neural precursors of action also tracka subjective feeling of readiness. In Experiment 1, we combined a self-paced action task with an intention-probing design where participants gave binary responses to indicate whether they felt they had been about to move when a probe was presented. In Experiment 2, participants reported their feeling of readiness on a graded scale. We found that the feeling of readiness reliably correlates with the beta-band amplitude, but not with the readiness potential.

A novel method to selectively elicit cold sensations without touch.

BACKGROUND: Thermal and tactile stimuli are transduced by different receptor classes. However, mechano- and thermo-sensitive afferents interact at spinal and supraspinal levels. Yet, most studies on responses to cooling stimuli are confounded by mechanical contact, making these interactions difficult to isolate. Methods for precise control of non-mechanical thermal stimulations remain challenging, particularly in the cold range. NEW METHOD: We developed a non-tactile, focal, temperature-controlled, multi-purpose cooling stimulator. This method controls the exposure of a target skin region to a dry-ice source. Using a thermal camera to monitor skin temperature, and adjusting the source-skin distance accordingly, we could deliver non-tactile cooling stimuli with customisable profiles, for studying different aspects of cold sensation. RESULTS: To validate our method, we measured absolute and relative thresholds for cold sensation without mechanical contact in 13 human volunteer participants, using the method of limits. We found that the absolute cold detection threshold was 32.71 oC ± 0.88 oC. This corresponded to a threshold relative to each participant's baseline skin temperature of - 1.08 oC ± 0.37 oC. COMPARISONS WITH EXISTING METHOD: Our method allows cooling stimulation without the confound of mechanical contact, in a controllable and focal manner. CONCLUSIONS: We report a non-contact cooling stimulator and accompanying control system. We used this to measure cold thresholds in the absence of confounding touch. Our method enables more targeted studies of both cold sensory pathways, and of cold-touch interactions.

Interhemispheric communication during haptic self-perception.

During the haptic exploration of a planar surface, slight resistances against the hand's movement are illusorily perceived as asperities (bumps) in the surface. If the surface being touched is one's own skin, an actual bump would also produce increased tactile pressure from the moving finger onto the skin. We investigated how kinaesthetic and tactile signals combine to produce haptic perceptions during self-touch. Participants performed two successive movements with the right hand. A haptic force-control robot applied resistances to both movements, and participants judged which movement was felt to contain the larger bump. An additional robot delivered simultaneous but task-irrelevant tactile stroking to the left forearm. These strokes contained either increased or decreased tactile pressure synchronized with the resistance-induced illusory bump encountered by the right hand. We found that the size of bumps perceived by the right hand was enhanced by an increase in left tactile pressure, but also by a decrease. Tactile event detection was thus transferred interhemispherically, but the sign of the tactile information was not respected. Randomizing (rather than blocking) the presentation order of left tactile stimuli abolished these interhemispheric enhancement effects. Thus, interhemispheric transfer during bimanual self-touch requires a stable model of temporally synchronized events, but does not require geometric consistency between hemispheric information, nor between tactile and kinaesthetic representations of a single common object.

Aesthetic experience enhances first-person spatial representation.

Episodic autobiographical memories are characterized by a spatial context and an affective component. But how do affective and spatial aspects interact? Does affect modulate the way we encode the spatial context of events? We investigated how one element of affect, namely aesthetic liking, modulates memory for location, in three online experiments (n = 124, 79, and 80). Participants visited a professionally curated virtual art exhibition. They then relocated previously viewed artworks on the museum map and reported how much they liked them. Across all experiments, liking an artwork was associated with increased ability to recall the wall on which it was hung. The effect was not explained by viewing time and appeared to modulate recognition speed. The liking-wall memory effect remained when participants attended to abstractness, rather than liking, and when testing occurred 24 h after the museum visit. Liking also modulated memory for the room where a work of art was hung, but this effect primarily involved reduced room memory for disliked artworks. Further, the liking-wall memory effect remained after controlling for effects of room memory. Recalling the wall requires recalling one's facing direction, so our findings suggest that positive aesthetic experiences enhance first-person spatial representations. More generally, a first-person component of positive affect transfers to wider spatial representation and facilitates the encoding of locations in a subject-centered reference frame. Affect and spatial representations are therefore important, and linked, elements of sentience and subjectivity. Memories of aesthetic experiences are also spatial memories of how we encountered a work of art. This linkage may have implications for museum design.

The sense of agency in emerging technologies for human-computer integration: A review.

Human-computer integration is an emerging area in which the boundary between humans and technology is blurred as users and computers work collaboratively and share agency to execute tasks. The sense of agency (SoA) is an experience that arises by a combination of a voluntary motor action and sensory evidence whether the corresponding body movements have somehow influenced the course of external events. The SoA is not only a key part of our experiences in daily life but also in our interaction with technology as it gives us the feeling of "I did that" as opposed to "the system did that," thus supporting a feeling of being in control. This feeling becomes critical with human-computer integration, wherein emerging technology directly influences people's body, their actions, and the resulting outcomes. In this review, we analyse and classify current integration technologies based on what we currently know about agency in the literature, and propose a distinction between body augmentation, action augmentation, and outcome augmentation. For each category, we describe agency considerations and markers of differentiation that illustrate a relationship between assistance level (low, high), agency delegation (human, technology), and integration type (fusion, symbiosis). We conclude with a reflection on the opportunities and challenges of integrating humans with computers, and finalise with an expanded definition of human-computer integration including agency aspects which we consider to be particularly relevant. The aim this review is to provide researchers and practitioners with guidelines to situate their work within the integration research agenda and consider the implications of any technologies on SoA, and thus overall user experience when designing future technology.

No exaggerated tremor severity perception in functional tremor.

BACKGROUND: Symptoms of functional neurological disorder tend to be variable, yet patients often report them being present constantly and of permanently severe intensity. Furthermore, they typically worsen when they are mentioned or during clinical examination. Such phenomena are sometimes interpreted as indicating symptom exaggeration or even fabrication. METHODS: To test the notion of inaccurate symptom perception or reporting, we directly compared subjective to objective tremulousness of reaching movements in people with a functional action tremor, people with an organic action tremor and healthy controls. Identical subjective and objective measures were used, thus eliminating any potential metacognitive confounders. Furthermore, we assessed both immediate perceptual experience with a real-time perceptual task, offering the most direct comparison; and near-time retrospective reports as the latter contribute to peoples' overall judgement of their condition. RESULTS: There was no significant difference in subjective compared to objective tremor severity between the three groups for either the real-time or retrospective conditions. CONCLUSION: People with functional tremor do not perceive or report their tremor in an exaggerated manner, compared to people with an organic tremor or healthy controls. We propose that symptom exacerbation through attentional mechanisms provides an alternative explanation for findings that are frequently attributed to 'exaggeration'.