Phasic modulation of beta power at movement-related frequencies during visuomotor conflict.

Rhythmic cortical activity is thought to underlie many cognitive functions including the flexible weighting of sensory information depending on the current behavioral context. Here, we tested for potential oscillatory alignment and power modulation at behaviorally relevant frequencies in magnetoencephalography (MEG) data acquired during a virtual reality-based, rhythmic hand-target phase matching task. The task contained conditions differing in terms of visuomotor incongruence and whether or not behavior (grasping movements) had to be adapted to keep vision aligned with the target. We tested for potential oscillatory alignment with movement frequencies and cross-frequency coupling with oscillations in the alpha, beta, and gamma bands. Our results revealed local peaks at 1 Hz power, corresponding to the frequency at which hand movements alternated between open and close; thus, potentially indicating an "entrainment" of neural oscillations at key movement frequencies. We found 1 Hz power was selectively enhanced when participants needed to align incongruent vision with the target. Moreover, the phase of the "movement-entrained" 1 Hz oscillations coupled significantly with the momentary amplitude of beta band oscillations-again, this coupling was selectively enhanced when incongruent vision was task relevant. We propose that this reflected a top-down mechanism, most likely related to selective attention and rhythmic sensory sampling. Thus, phasic low-frequency (beta) power suppression likely indicated a variable (attentional) sampling of visual movement feedback; i.e., related to increased sensitivity for visually matching alternating hand movements to a phasic target at ecologically important time points, rather than continually during the grasping cycle.NEW & NOTEWORTHY Our results reveal an increased spectral power at movement frequencies in a rhythmic hand-target phase matching task under visuomotor conflict; this effect was strongest when incongruent visual movement feedback was required to guide action. Moreover, the phase of these slow frequencies coupled with the momentary power beta oscillations; again, this coupling was selectively strengthened when incongruent vision was task relevant.

The computational neurology of movement under active inference.

We propose a computational neurology of movement based on the convergence of theoretical neurobiology and clinical neurology. A significant development in the former is the idea that we can frame brain function as a process of (active) inference, in which the nervous system makes predictions about its sensory data. These predictions depend upon an implicit predictive (generative) model used by the brain. This means neural dynamics can be framed as generating actions to ensure sensations are consistent with these predictions-and adjusting predictions when they are not. We illustrate the significance of this formulation for clinical neurology by simulating a clinical examination of the motor system using an upper limb coordination task. Specifically, we show how tendon reflexes emerge naturally under the right kind of generative model. Through simulated perturbations, pertaining to prior probabilities of this model's variables, we illustrate the emergence of hyperreflexia and pendular reflexes, reminiscent of neurological lesions in the corticospinal tract and cerebellum. We then turn to the computational lesions causing hypokinesia and deficits of coordination. This in silico lesion-deficit analysis provides an opportunity to revisit classic neurological dichotomies (e.g. pyramidal versus extrapyramidal systems) from the perspective of modern approaches to theoretical neurobiology-and our understanding of the neurocomputational architecture of movement control based on first principles.

I overthink-Therefore I am not: An active inference account of altered sense of self and agency in depersonalisation disorder.

This paper considers the phenomenology of depersonalisation disorder, in relation to predictive processing and its associated pathophysiology. To do this, we first establish a few mechanistic tenets of predictive processing that are necessary to talk about phenomenal transparency, mental action, and self as subject. We briefly review the important role of 'predicting precision' and how this affords mental action and the loss of phenomenal transparency. We then turn to sensory attenuation and the phenomenal consequences of (pathophysiological) failures to attenuate or modulate sensory precision. We then consider this failure in the context of depersonalisation disorder. The key idea here is that depersonalisation disorder reflects the remarkable capacity to explain perceptual engagement with the world via the hypothesis that "I am an embodied perceiver, but I am not in control of my perception". We suggest that individuals with depersonalisation may believe that 'another agent' is controlling their thoughts, perceptions or actions, while maintaining full insight that the 'other agent' is 'me' (the self). Finally, we rehearse the predictions of this formal analysis, with a special focus on the psychophysical and physiological abnormalities that may underwrite the phenomenology of depersonalisation.

Attentional Modulation of Vision Versus Proprioception During Action.

To control our actions efficiently, our brain represents our body based on a combination of visual and proprioceptive cues, weighted according to how (un)reliable-how precise-each respective modality is in a given context. However, perceptual experiments in other modalities suggest that the weights assigned to sensory cues are also modulated "top-down" by attention. Here, we asked whether during action, attention can likewise modulate the weights (i.e., precision) assigned to visual versus proprioceptive information about body position. Participants controlled a virtual hand (VH) via a data glove, matching either the VH or their (unseen) real hand (RH) movements to a target, and thus adopting a ``visual'' or ``proprioceptive'' attentional set, under varying levels of visuo-proprioceptive congruence and visibility. Functional magnetic resonance imaging (fMRI) revealed increased activation of the multisensory superior parietal lobe (SPL) during the VH task and increased activation of the secondary somatosensory cortex (S2) during the RH task. Dynamic causal modeling (DCM) showed that these activity changes were the result of selective, diametrical gain modulations in the primary visual cortex (V1) and the S2. These results suggest that endogenous attention can balance the gain of visual versus proprioceptive brain areas, thus contextualizing their influence on multisensory areas representing the body for action.

Action-Dependent Processing of Touch in the Human Parietal Operculum and Posterior Insula.

Somatosensory input generated by one's actions (i.e., self-initiated body movements) is generally attenuated. Conversely, externally caused somatosensory input is enhanced, for example, during active touch and the haptic exploration of objects. Here, we used functional magnetic resonance imaging (fMRI) to ask how the brain accomplishes this delicate weighting of self-generated versus externally caused somatosensory components. Finger movements were either self-generated by our participants or induced by functional electrical stimulation (FES) of the same muscles. During half of the trials, electrotactile impulses were administered when the (actively or passively) moving finger reached a predefined flexion threshold. fMRI revealed an interaction effect in the contralateral posterior insular cortex (pIC), which responded more strongly to touch during self-generated than during FES-induced movements. A network analysis via dynamic causal modeling revealed that connectivity from the secondary somatosensory cortex via the pIC to the supplementary motor area was generally attenuated during self-generated relative to FES-induced movements-yet specifically enhanced by touch received during self-generated, but not FES-induced movements. Together, these results suggest a crucial role of the parietal operculum and the posterior insula in differentiating self-generated from externally caused somatosensory information received from one's moving limb.

Cortical beta oscillations reflect the contextual gating of visual action feedback.

In sensorimotor integration, the brain needs to decide how its predictions should accommodate novel evidence by 'gating' sensory data depending on the current context. Here, we examined the oscillatory correlates of this process by recording magnetoencephalography (MEG) data during a new task requiring action under intersensory conflict. We used virtual reality to decouple visual (virtual) and proprioceptive (real) hand postures during a task in which the phase of grasping movements tracked a target (in either modality). Thus, we rendered visual information either task-relevant or a (to-be-ignored) distractor. Under visuo-proprioceptive incongruence, occipital beta power decreased (relative to congruence) when vision was task-relevant but increased when it had to be ignored. Dynamic causal modeling (DCM) revealed that this interaction was best explained by diametrical, task-dependent changes in visual gain. These results suggest a crucial role for beta oscillations in the contextual gating (i.e., gain or precision control) of visual vs proprioceptive action feedback, depending on current behavioral demands.

Different responses of the right superior temporal sulcus to visual movement feedback during self-generated vs. externally generated hand movements.

An important implication of several recent accounts of motor control is that sensory feedback from self-generated movements is relatively attenuated based on predictions issued by the agent's motor system. Such a relative attenuation of sensory information during actions has already been demonstrated in the somatosensory domain. Here, we used functional magnetic resonance imaging (fMRI) and a virtual reality-based setup to investigate a potential attenuation of brain responses to realistic visual movement feedback during active vs. passive right-hand movements. The participants' right unseen hand was rotated either by the participants themselves or by the experimenter, while the participants received visual movement feedback via a photorealistic virtual 3D hand driven by their real hand movements, or received no visual feedback. We observed a significant interaction between movement type (active vs. passive) and movement feedback (vision vs. no vision) in the right superior temporal sulcus (STS), which showed relatively attenuated blood-oxygen-level-dependent (BOLD) signal differences in movements with vs. without visual feedback when those movements were actively vs. passively executed. This finding suggests that STS activity caused by visual feedback from the moving body may be attenuated based on the agent's motor predictions.

Integration of Visual and Proprioceptive Limb Position Information in Human Posterior Parietal, Premotor, and Extrastriate Cortex.

The brain constructs a flexible representation of the body from multisensory information. Previous work on monkeys suggests that the posterior parietal cortex (PPC) and ventral premotor cortex (PMv) represent the position of the upper limbs based on visual and proprioceptive information. Human experiments on the rubber hand illusion implicate similar regions, but since such experiments rely on additional visuo-tactile interactions, they cannot isolate visuo-proprioceptive integration. Here, we independently manipulated the position (palm or back facing) of passive human participants' unseen arm and of a photorealistic virtual 3D arm. Functional magnetic resonance imaging (fMRI) revealed that matching visual and proprioceptive information about arm position engaged the PPC, PMv, and the body-selective extrastriate body area (EBA); activity in the PMv moreover reflected interindividual differences in congruent arm ownership. Further, the PPC, PMv, and EBA increased their coupling with the primary visual cortex during congruent visuo-proprioceptive position information. These results suggest that human PPC, PMv, and EBA evaluate visual and proprioceptive position information and, under sufficient cross-modal congruence, integrate it into a multisensory representation of the upper limb in space. SIGNIFICANCE STATEMENT: The position of our limbs in space constantly changes, yet the brain manages to represent limb position accurately by combining information from vision and proprioception. Electrophysiological recordings in monkeys have revealed neurons in the posterior parietal and premotor cortices that seem to implement and update such a multisensory limb representation, but this has been difficult to demonstrate in humans. Our fMRI experiment shows that human posterior parietal, premotor, and body-selective visual brain areas respond preferentially to a virtual arm seen in a position corresponding to one's unseen hidden arm, while increasing their communication with regions conveying visual information. These brain areas thus likely integrate visual and proprioceptive information into a flexible multisensory body representation.

Neuronal correlates of continuous manual tracking under varying visual movement feedback in a virtual reality environment.

To accurately guide one's actions online, the brain predicts sensory action feedback ahead of time based on internal models, which can be updated by sensory prediction errors. The underlying operations can be experimentally investigated in sensorimotor adaptation tasks, in which moving under perturbed sensory action feedback requires internal model updates. Here we altered healthy participants' visual hand movement feedback in a virtual reality setup, while assessing brain activity with functional magnetic resonance imaging (fMRI). Participants tracked a continually moving virtual target object with a photorealistic, three-dimensional (3D) virtual hand controlled online via a data glove. During the continuous tracking task, the virtual hand's movements (i.e., visual movement feedback) were repeatedly periodically delayed, which participants had to compensate for to maintain accurate tracking. This realistic task design allowed us to simultaneously investigate processes likely operating at several levels of the brain's motor control hierarchy. FMRI revealed that the length of visual feedback delay was parametrically reflected by activity in the inferior parietal cortex and posterior temporal cortex. Unpredicted changes in visuomotor mapping (at transitions from synchronous to delayed visual feedback periods or vice versa) activated biological motion-sensitive regions in the lateral occipitotemporal cortex (LOTC). Activity in the posterior parietal cortex (PPC), focused on the contralateral anterior intraparietal sulcus (aIPS), correlated with tracking error, whereby this correlation was stronger in participants with higher tracking performance. Our results are in line with recent proposals of a wide-spread cortical motor control hierarchy, where temporoparietal regions seem to evaluate visuomotor congruence and thus possibly ground a self-attribution of movements, the LOTC likely processes early visual prediction errors, and the aIPS computes action goal errors and possibly corresponding motor corrections.

Network activity underlying the illusory self-attribution of a dummy arm.

Neuroimaging has demonstrated that the illusory self-attribution of body parts engages frontal and intraparietal brain areas, and recent evidence further suggests an involvement of visual body-selective regions in the occipitotemporal cortex. However, little is known about the principles of information exchange within this network. Here, using automated congruent versus incongruent visuotactile stimulation of distinct anatomical locations on the participant's right arm and a realistic dummy counterpart in an fMRI scanner, we induced an illusory self-attribution of the dummy arm. The illusion consistently activated a left-hemispheric network comprising ventral premotor cortex (PMv), intraparietal sulcus (IPS), and body-selective regions of the lateral occipitotemporal cortex (LOC). Importantly, during the illusion, the functional coupling of the PMv and the IPS with the LOC increased substantially, and dynamic causal modeling revealed a significant enhancement of connections from the LOC and the secondary somatosensory cortex to the IPS. These results comply with the idea that the brain's inference mechanisms rely on the hierarchical propagation of prediction error. During illusory self-attribution, unpredicted ambiguous sensory input about one's body configuration may result in the generation of such prediction errors in visual and somatosensory areas, which may be conveyed to parietal integrative areas.

The extrastriate body area is involved in illusory limb ownership.

The Rubber Hand Illusion (RHI) is an established paradigm for studying body ownership, and several studies have implicated premotor and temporo-parietal brain regions in its neuronal foundation. Here we used an automated setup to induce a novel multi-site version of the RHI in healthy human participants inside an MR-scanner, with a RHI and control condition that were matched in terms of synchrony of visual and tactile stimulation. Importantly, as previous research has shown that most of the ownership-related brain areas also respond to observed human actions and touch, or body parts of others, here such potential effects of the experimenter were eliminated by the automated procedure. The RHI condition induced a strong ownership illusion; we found correspondingly stronger brain activity during the RHI versus control condition in contralateral middle occipital gyrus (mOCG) and bilateral anterior insula, which have previously been related to illusory body ownership. Using independent functional localizers, we confirmed that the activity in mOCG was located within the body-part selective extrastriate body area (EBA). Crucially, activity differences in participants' peak voxels within the left EBA correlated strongly positively with their behavioral illusion scores. Thus EBA activity also reflected interindividual differences in the experienced intensity of illusory limb ownership. Moreover, psychophysiological interaction analyses (PPI) revealed that contralateral primary somatosensory cortex had stronger brain connectivity with EBA during the RHI versus control condition, while EBA was more strongly interacting with temporo-parietal multisensory regions. In sum, our findings demonstrate a direct involvement of EBA in limb ownership.

Forgetting ourselves in flow: an active inference account of flow states and how we experience ourselves within them.

Flow has been described as a state of optimal performance, experienced universally across a broad range of domains: from art to athletics, gaming to writing. However, its phenomenal characteristics can, at first glance, be puzzling. Firstly, individuals in flow supposedly report a loss of self-awareness, even though they perform in a manner which seems to evince their agency and skill. Secondly, flow states are felt to be effortless, despite the prerequisite complexity of the tasks that engender them. In this paper, we unpick these features of flow, as well as others, through the active inference framework, which posits that action and perception are forms of active Bayesian inference directed at sustained self-organisation; i.e., the minimisation of variational free energy. We propose that the phenomenology of flow is rooted in the deployment of high precision weight over (i) the expected sensory consequences of action and (ii) beliefs about how action will sequentially unfold. This computational mechanism thus draws the embodied cognitive system to minimise the ensuing (i.e., expected) free energy through the exploitation of the pragmatic affordances at hand. Furthermore, given the challenging dynamics the flow-inducing situation presents, attention must be wholly focussed on the unfolding task whilst counterfactual planning is restricted, leading to the attested loss of the sense of self-as-object. This involves the inhibition of both the sense of self as a temporally extended object and higher-order, meta-cognitive forms of self-conceptualisation. Nevertheless, we stress that self-awareness is not entirely lost in flow. Rather, it is pre-reflective and bodily. Our approach to bodily-action-centred phenomenology can be applied to similar facets of seemingly agentive experience beyond canonical flow states, providing insights into the mechanisms of so-called selfless experiences, embodied expertise and wellbeing.

Precision control for a flexible body representation.

Adaptive body representation requires the continuous integration of multisensory inputs within a flexible 'body model' in the brain. The present review evaluates the idea that this flexibility is augmented by the contextual modulation of sensory processing 'top-down'; which can be described as precision control within predictive coding formulations of Bayesian inference. Specifically, I focus on the proposal that an attenuation of proprioception may facilitate the integration of conflicting visual and proprioceptive bodily cues. Firstly, I review empirical work suggesting that the processing of visual vs proprioceptive body position information can be contextualised 'top-down'; for instance, by adopting specific attentional task sets. Building up on this, I review research showing a similar contextualisation of visual vs proprioceptive information processing in the rubber hand illusion and in visuomotor adaptation. Together, the reviewed literature suggests that proprioception, despite its indisputable importance for body perception and action control, can be attenuated top-down (through precision control) to facilitate the contextual adaptation of the brain's body model to novel visual feedback.

A Crucial Role of the Frontal Operculum in Task-Set Dependent Visuomotor Performance Monitoring.

For adaptive goal-directed action, the brain needs to monitor action performance and detect errors. The corresponding information may be conveyed via different sensory modalities; for instance, visual and proprioceptive body position cues may inform about current manual action performance. Thereby, contextual factors such as the current task set may also determine the relative importance of each sensory modality for action guidance. Here, we analyzed human behavioral, functional magnetic resonance imaging (fMRI), and magnetoencephalography (MEG) data from two virtual reality-based hand-target phase-matching studies to identify the neuronal correlates of performance monitoring and error processing under instructed visual or proprioceptive task sets. Our main result was a general, modality-independent response of the bilateral frontal operculum (FO) to poor phase-matching accuracy, as evident from increased BOLD signal and increased source-localized gamma power. Furthermore, functional connectivity of the bilateral FO to the right posterior parietal cortex (PPC) increased under a visual versus proprioceptive task set. These findings suggest that the bilateral FO generally monitors manual action performance; and, moreover, that when visual action feedback is used to guide action, the FO may signal an increased need for control to visuomotor regions in the right PPC following errors.

Does temporal irregularity drive prediction failure in schizophrenia? temporal modelling of ERPs.

Schizophrenia subjects often suffer from a failure to properly predict incoming inputs; most notably, some patients exhibit impaired prediction of the sensory consequences of their own actions. The mechanisms underlying this deficit remain unclear, though. One possible mechanism could consist in aberrant predictive processing, as schizophrenic patients show relatively less attenuated neuronal activity to self-produced tones, than healthy controls. Here, we tested the hypothesis that this aberrant predictive mechanism would manifest itself in the temporal irregularity of neuronal signals. For that purpose, we here introduce an event-related potential (ERP) study model analysis that consists of an EEG real-time model equation, eeg(t) and a frequency Laplace transformed Transfer Function (TF) equation, eeg(s). Combining circuit analysis with control and cable theory, we estimate the temporal model representations of auditory ERPs to reveal neural mechanisms that make predictions about self-generated sensations. We use data from 49 schizophrenic patients (SZ) and 32 healthy control (HC) subjects in an auditory 'prediction' paradigm; i.e., who either pressed a button to deliver a sound tone (epoch a), or just heard the tone without button press (epoch b). Our results show significantly higher degrees of temporal irregularity or imprecision between different trials of the ERP from the Cz electrode (N100, P200) in SZ compared to HC (Levene's test, p < 0.0001) as indexed by altered latency, lower similarity/correlation of single trial time courses (using dynamic time warping), and longer settling times to reach steady state in the intertrial interval. Using machine learning, SZ vs HC could be highly accurately classified (92%) based on the temporal parameters of their ERPs' TF models, using as features the poles of the TF rational functions. Together, our findings show temporal irregularity or imprecision between single trials to be abnormally increased in SZ. This may indicate a general impairment of SZ, related to precisely predicting the sensory consequences of one's actions.

Active inference under visuo-proprioceptive conflict: Simulation and empirical results.

It has been suggested that the brain controls hand movements via internal models that rely on visual and proprioceptive cues about the state of the hand. In active inference formulations of such models, the relative influence of each modality on action and perception is determined by how precise (reliable) it is expected to be. The 'top-down' affordance of expected precision to a particular sensory modality is associated with attention. Here, we asked whether increasing attention to (i.e., the precision of) vision or proprioception would enhance performance in a hand-target phase matching task, in which visual and proprioceptive cues about hand posture were incongruent. We show that in a simple simulated agent-based on predictive coding formulations of active inference-increasing the expected precision of vision or proprioception improved task performance (target matching with the seen or felt hand, respectively) under visuo-proprioceptive conflict. Moreover, we show that this formulation captured the behaviour and self-reported attentional allocation of human participants performing the same task in a virtual reality environment. Together, our results show that selective attention can balance the impact of (conflicting) visual and proprioceptive cues on action-rendering attention a key mechanism for a flexible body representation for action.

Fronto-Parietal Brain Responses to Visuotactile Congruence in an Anatomical Reference Frame.

Spatially and temporally congruent visuotactile stimulation of a fake hand together with one's real hand may result in an illusory self-attribution of the fake hand. Although this illusion relies on a representation of the two touched body parts in external space, there is tentative evidence that, for the illusion to occur, the seen and felt touches also need to be congruent in an anatomical reference frame. We used functional magnetic resonance imaging and a somatotopical, virtual reality-based setup to isolate the neuronal basis of such a comparison. Participants' index or little finger was synchronously touched with the index or little finger of a virtual hand, under congruent or incongruent orientations of the real and virtual hands. The left ventral premotor cortex responded significantly more strongly to visuotactile co-stimulation of the same versus different fingers of the virtual and real hand. Conversely, the left anterior intraparietal sulcus responded significantly more strongly to co-stimulation of different versus same fingers. Both responses were independent of hand orientation congruence and of spatial congruence of the visuotactile stimuli. Our results suggest that fronto-parietal areas previously associated with multisensory processing within peripersonal space and with tactile remapping evaluate the congruence of visuotactile stimulation on the body according to an anatomical reference frame.

'Seeing the Dark': Grounding Phenomenal Transparency and Opacity in Precision Estimation for Active Inference.

One of the central claims of the Self-model Theory of Subjectivity is that the experience of being someone - even in a minimal form - arises through a transparent phenomenal self-model, which itself can in principle be reduced to brain processes. Here, we consider whether it is possible to distinguish between phenomenally transparent and opaque states in terms of active inference. We propose a relationship of phenomenal opacity to expected uncertainty or precision; i.e., the capacity for introspective attention and implicit mental action. Thus we associate introspective attention with the deployment of 'precision' that may render the perceptual evidence (for action) opaque, while treating transparency as a necessary aspect of beliefs about action, i.e., 'what I am' doing. We conclude by proposing how we may have to nuance our conception of minimal phenomenal selfhood and agency in light of this active inference conception of transparency-opacity.