Sensory Attenuation Research Articles

12. Sensory Attenuation Elicited by Inner Speech and its Role for Auditory Hallucinations in Schizophrenia

12. Sensory Attenuation Elicited by Inner Speech and its Role for Auditory Hallucinations in Schizophrenia

The auditory P2 differentiates self- from partner-produced sounds during joint action: Contributions of self-specific attenuation and temporal orienting of attention

Sensory attenuation of the auditory P2 event-related potential (ERP) has been shown to differentiate the sensory consequences of one's own from others' action in joint action contexts. However, recent evidence suggests that when people coordinate joint actions over time, temporal orienting of attention might simultaneously contribute to enhancing the auditory P2. The current study employed a joint tapping task in which partners produced tone sequences together to examine whether temporal orienting influences auditory ERP amplitudes during the time window of self-other differentiation. Our findings demonstrate that the combined requirements of coordinating with a partner toward a joint goal and immediately adjusting to the partner's tone timing enhance P2 amplitudes elicited by the partner's tone onsets. Furthermore, our findings replicate prior evidence for self-specific sensory attenuation of the auditory P2 in joint action, and additionally demonstrate that it occurs regardless of the coordination requirements between partners. Together, these findings provide evidence that temporal orienting and sensory attenuation both modulate the auditory P2 during joint action and suggest that both processes play a role in facilitating precise interpersonal coordination between partners.

Role of selective attention in fatigue in neurological disorders.

Chronic fatigue is a significant symptom in several diseases including traumatic and degenerative neurological disorders. While several studies have investigated the correlates of chronic fatigue, there is as yet no unifying framework to explain chronic fatigue. In this narrative review, I investigate the role of selective attention in the development of chronic fatigue and discuss results within the framework of the sensory attenuation model of fatigue, which posits that fatigue is the phenomenological output of altered attention to sensory input. Following a short introduction of this framework, I present results from investigations that address attentional mechanisms in fatigue in multiple sclerosis, stroke, traumatic brain injury and Parkinson's disease. Attention was quantified in all four disease models using a variety of outcome measures, including behavioural, neurophysiological, structural and functional brain connectivity. The range of measures precluded direct comparison of results across disease conditions; however, in all four disease models there was evidence of poor selective attention that explained levels of chronic fatigue, supporting the sensory attenuation model of fatigue as a disease-independent mechanism of fatigue. Evidence was lacking to draw any conclusions about the direction of causality. The role of selective attention in development of fatigue is indicated. Future studies must focus on establishing causality and exploring attentional circuitry as a potential therapeutic target.

Turn-Taking Mechanisms in Imitative Interaction: Robotic Social Interaction Based on the Free Energy Principle

This study explains how the leader-follower relationship and turn-taking could develop in a dyadic imitative interaction by conducting robotic simulation experiments based on the free energy principle. Our prior study showed that introducing a parameter during the model training phase can determine leader and follower roles for subsequent imitative interactions. The parameter is defined as w, the so-called meta-prior, and is a weighting factor used to regulate the complexity term versus the accuracy term when minimizing the free energy. This can be read as sensory attenuation, in which the robot's prior beliefs about action are less sensitive to sensory evidence. The current extended study examines the possibility that the leader-follower relationship shifts depending on changes in w during the interaction phase. We identified a phase space structure with three distinct types of behavioral coordination using comprehensive simulation experiments with sweeps of w of both robots during the interaction. Ignoring behavior in which the robots follow their own intention was observed in the region in which both ws were set to large values. One robot leading, followed by the other robot was observed when one w was set larger and the other was set smaller. Spontaneous, random turn-taking between the leader and the follower was observed when both ws were set at smaller or intermediate values. Finally, we examined a case of slowly oscillating w in anti-phase between the two agents during the interaction. The simulation experiment resulted in turn-taking in which the leader-follower relationship switched during determined sequences, accompanied by periodic shifts of ws. An analysis using transfer entropy found that the direction of information flow between the two agents also shifted along with turn-taking. Herein, we discuss qualitative differences between random/spontaneous turn-taking and agreed-upon sequential turn-taking by reviewing both synthetic and empirical studies.

The predictive brain: Linking motor and sensory attenuation using combined TMS-EEG

The predictive brain: Linking motor and sensory attenuation using combined TMS-EEG

Virtual occlusion effects on the perception of self-initiated visual stimuli

Virtual reality (VR) has established itself as a useful tool in the study of human perception in the laboratory. A recent study introduced a new approach to examine visual sensory attenuation (SA) effects in VR. Hand movements triggered the appearance of Gabor stimuli, which were either presented behind the participant’s hand – not rendered in VR (“virtual occlusion”) - or elsewhere on the display. Virtual occlusion led to a rightward shift of the psychometric curve, suggesting that self-generated hand movements reduced the perceived contrast of the stimulus. Since such attenuation effects might provide a window into the predictive processing of the sensory and cognitive apparatus, we sought to better understand the nature of the virtual occlusion effects. In our study, the presentation of test stimuli was either self-initiated, self-initiated with a variable delay, or triggered externally; the test stimuli were occluded or not. In conflict with our hypothesis, we found moderate to strong evidence for an absence of any horizontal shifts between the psychometric curves. However, virtual occlusion was associated with a decrease in the slope of the psychometric function. Our results suggest that virtual occlusion attenuated the relative perceptual sensitivity, so that participants had more difficulty discriminating contrast differences when the test stimulus was presented behind the hand. We tentatively conclude that, in the visual domain, the discriminability of stimulus intensity is modified by internal predictive cues (i.e., proprioception), possibly linked to shifts in covert spatial attention.

Disrupted auditory N1, theta power and coherence suppression to willed speech in people with schizophrenia

The phenomenon of sensory self-suppression - also known as sensory attenuation - occurs when a person generates a perceptible stimulus (such as a sound) by performing an action (such as speaking). The sensorimotor control system is thought to actively predict and then suppress the vocal sound in the course of speaking, resulting in lowered cortical responsiveness when speaking than when passively listening to an identical sound. It has been hypothesized that auditory hallucinations in schizophrenia result from a reduction in self-suppression due to a disruption of predictive mechanisms required to anticipate and suppress a specific, self-generated sound. It has further been hypothesized that this suppression is evident primarily in theta band activity. Fifty-one people, half of whom had a diagnosis of schizophrenia, were asked to repeatedly utter a single syllable, which was played back to them concurrently over headphones while EEG was continuously recorded. In other conditions, recordings of the same spoken syllables were played back to participants while they passively listened, or were played back with their onsets preceded by a visual cue. All participants experienced these conditions with their voice artificially shifted in pitch and also with their unaltered voice. Suppression was measured using event-related potentials (N1 component), theta phase coherence and power. We found that suppression was generally reduced on all metrics in the patient sample, and when voice alteration was applied. We additionally observed reduced theta coherence and power in the patient sample across all conditions. Visual cueing affected theta coherence only. In aggregate, the results suggest that sensory self-suppression of theta power and coherence is disrupted in schizophrenia.

Tactile pre-motor attention induces sensory attenuation for sounds

Tactile pre-motor attention induces sensory attenuation for sounds

Active inference, morphogenesis, and computational psychiatry.

Active inference is a leading theory in neuroscience that provides a simple and neuro-biologically plausible account of how action and perception are coupled in producing (Bayes) optimal behavior; and has been recently used to explain a variety of psychopathological conditions. In parallel, morphogenesis has been described as the behavior of a (non-neural) cellular collective intelligence solving problems in anatomical morphospace. In this article, we establish a link between the domains of cell biology and neuroscience, by analyzing disorders of morphogenesis as disorders of (active) inference. The aim of this article is three-fold. We want to: (i) reveal a connection between disorders of morphogenesis and disorders of active inference as apparent in psychopathological conditions; (ii) show how disorders of morphogenesis can be simulated using active inference; (iii) suggest that active inference can shed light on developmental defects or aberrant morphogenetic processes, seen as disorders of information processing, and perhaps suggesting novel intervention and repair strategies. We present four simulations illustrating application of these ideas to cellular behavior during morphogenesis. Three of the simulations show that the same forms of aberrant active inference (e.g., deficits of sensory attenuation and low sensory precision) that have been used to explain psychopathological conditions (e.g., schizophrenia and autism) also produce familiar disorders of development and morphogenesis when implemented at the level of the collective behavior of a group of cells. The fourth simulation involves two cells with too high precision, in which we show that the reduction of concentration signaling and sensitivity to the signals of other cells treats the development defect. Finally, we present the results of an experimental test of one of the model's predictions in early Xenopus laevis embryos: thioridazine (a dopamine antagonist that may reduce sensory precision in biological systems) induced developmental (anatomical) defects as predicted. The use of conceptual and empirical tools from neuroscience to understand the morphogenetic behavior of pre-neural agents offers the possibility of new approaches in regenerative medicine and evolutionary developmental biology.

Sensory attenuation from action observation

A central claim of many embodied approaches to cognition is that understanding others' actions is achieved by covertly simulating the observed actions and their consequences in one's own motor system. If such a simulation occurs, it may be accomplished through forward models, a component of the motor system already known to perform simulations of actions and their consequences in order to support sensory-monitoring of one's own actions. Forward-model simulations cause an attenuation of sensory intensity, so if the simulations hypothesized by embodied cognition are indeed provided by forward models, then action observation should trigger this sensory attenuation. To test this hypothesis, the experiments reported here measured the perceived intensity of a touch sensation on the finger when participants observed an active touch (a finger reaching to touch a ball) vs. a passive touch (a ball rolling to touch an unmoving finger). The touch sensation was perceived as less intense during observation of active touch in comparison with observation of passive touch, providing evidence that forward models are indeed engaged during action observation. The strength of this sensory attenuation is compared and contrasted with a well-established sensory-amplification effect caused by visual attention. This sensory-amplification effect has not generally been considered in studies related to sensory attenuation in action observation, which may explain conflicting results reported in the field.

Action-based predictions affect visual perception, neural processing, and pupil size, regardless of temporal predictability

Sensory consequences of one's own action are often perceived as less intense, and lead to reduced neural responses, compared to externally generated stimuli. Presumably, such sensory attenuation is due to predictive mechanisms based on the motor command (efference copy). However, sensory attenuation has also been observed outside the context of voluntary action, namely when stimuli are temporally predictable. Here, we aimed at disentangling the effects of motor and temporal predictability-based mechanisms on the attenuation of sensory action consequences. During fMRI data acquisition, participants (N = 25) judged which of two visual stimuli was brighter. In predictable blocks, the stimuli appeared temporally aligned with their button press (active) or aligned with an automatically generated cue (passive). In unpredictable blocks, stimuli were presented with a variable delay after button press/cue, respectively. Eye tracking was performed to investigate pupil-size changes and to ensure proper fixation. Self-generated stimuli were perceived as darker and led to less neural activation in visual areas than their passive counterparts, indicating sensory attenuation for self-generated stimuli independent of temporal predictability. Pupil size was larger during self-generated stimuli, which correlated negatively with the blood oxygenation level dependent (BOLD) response: the larger the pupil, the smaller the BOLD amplitude in visual areas. Our results suggest that sensory attenuation in visual cortex is driven by action-based predictive mechanisms rather than by temporal predictability. This effect may be related to changes in pupil diameter. Altogether, these results emphasize the role of the efference copy in the processing of sensory action consequences.

Emergence of sensory attenuation based upon the free-energy principle

The brain attenuates its responses to self-produced exteroceptions (e.g., we cannot tickle ourselves). Is this phenomenon, known as sensory attenuation, enabled innately, or acquired through learning? Here, our simulation study using a multimodal hierarchical recurrent neural network model, based on variational free-energy minimization, shows that a mechanism for sensory attenuation can develop through learning of two distinct types of sensorimotor experience, involving self-produced or externally produced exteroceptions. For each sensorimotor context, a particular free-energy state emerged through interaction between top-down prediction with precision and bottom-up sensory prediction error from each sensory area. The executive area in the network served as an information hub. Consequently, shifts between the two sensorimotor contexts triggered transitions from one free-energy state to another in the network via executive control, which caused shifts between attenuating and amplifying prediction-error-induced responses in the sensory areas. This study situates emergence of sensory attenuation (or self-other distinction) in development of distinct free-energy states in the dynamic hierarchical neural system.

Methodological considerations for the force-matching task

The force-matching task integrates haptic technology and electrical engineering to determine an individual’s level of sensory attenuation to somatic stimuli. The task requires a detailed methodology to facilitate reliable and replicable estimates, and there has been a distinct lack of re-evaluation of the methodological processes related to this paradigm. In this task, participants are asked to match a force delivered to their finger, either by pressing directly on their own finger with their other hand (known as the direct condition) or by controlling the device using an external potentiometer to control the force indirectly through a torque motor (known as the slider condition). We analysed 138 participants to determine 1) the optimal number of replications (2, 4, 6, or 8 replications) of the target force, 2) the optimal time window (1–1.5 s, 1.5–2 s, 2–2.5 s and 2.5–3 s) to extract the estimate of sensory attenuation, 3) if participants’ performance during the task improved, worsened or was stable across the experimental period regardless of condition, and 4) if learning effects were related to psychological traits. Results showed that the number of replications of the target forces may be reduced from 8 without compromising the estimate of sensory attenuation, the optimal time window for the extraction of the matched force is 2.5–3 s, the performance is stable over the duration of the experiment and not impacted by the measured psychological traits. In conclusion, we present a number of methodological considerations which improve the efficiency and reliability of the force-matching task.Highlights• The force-matching task determines an individual’s level of sensory attenuation• The optimal number of replications of the target force may be reduced from 8• The optimal time window to extract the matched force is 2.5–3.0 s• The estimate of sensory attenuation is stable across the duration of the task

Temporal context modulates sensory attenuation magnitude

In studies with self-produced sensory events, sensitivity for these events has been found to be reduced. This phenomenon is called sensory attenuation, and it has been assumed that the crucial factor is the self-production of the event. However, this factor may be confounded with the temporal predictability of the event, as well as with attentional focus on the event. In this study, we wondered about the influence of temporal stimulus predictably on sensory attenuation. We asked observers to discriminate the orientation of Gabor patches that were presented randomly at various times around a button press. Despite the unpredictability of stimulus occurrence, attenuation for these stimuli was tuned to the time of the button press. However, temporal expectations determined attenuation magnitude. Sensory attenuation was stronger when stimuli were expected to occur more often before the button press. When stimuli were expected to occur more often after the button press, no sensory attenuation was found. Our results show first that sensory attenuation occurs mandatorily even if stimulus occurrence cannot be predicted temporally. Second, temporal attention, guided by temporal stimulus probabilities, modulates sensory attenuation magnitude.

Tactile motor attention induces sensory attenuation for sounds

Sensory events appear reduced in intensity when we actively produce them. Here, we investigated sensory attenuation in a virtual reality setup that allowed us to manipulate the time of tactile feedback when pressing a virtual button. We asked whether tactile motor attention might shift to the tactile location that makes contact with the button. In experiment one, we found that a tactile impulse was perceived as more intense when button pressing. In a second experiment, participants pushed a button and estimated the intensity of sounds. We found sensory attenuation for sounds only when tactile feedback was provided at the time the movement goal was reached. These data indicate that attentional prioritization for the tactile modality during a goal-directed hand movement might lead to a transient reduction in sensitivity in other modalities, resulting in sensory attenuation for sounds.

Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self-initiated stimuli.

Actions modulate sensory processing by attenuating responses to self- compared to externally generated inputs, which is traditionally attributed to stimulus-specific motor predictions. Yet, suppression has been also found for stimuli merely coinciding with actions, pointing to unspecific processes that may be driven by neuromodulatory systems. Meanwhile, the differential processing for self-generated stimuli raises the possibility of producing effects also on memory for these stimuli; however, evidence remains mixed as to the direction of the effects. Here, we assessed the effects of actions on sensory processing and memory encoding of concomitant, but unpredictable sounds, using a combination of self-generation and memory recognition task concurrently with EEG and pupil recordings. At encoding, subjects performed button presses that half of the time generated a sound (motor-auditory; MA) and listened to passively presented sounds (auditory-only; A). At retrieval, two sounds were presented and participants had to respond which one was present before. We measured memory bias and memory performance by having sequences where either both or only one of the test sounds were presented at encoding, respectively. Results showed worse memory performance - but no differences in memory bias -, attenuated responses, and larger pupil diameter for MA compared to A sounds. Critically, the larger the sensory attenuation and pupil diameter, the worse the memory performance for MA sounds. Nevertheless, sensory attenuation did not correlate with pupil dilation. Collectively, our findings suggest that sensory attenuation and neuromodulatory processes coexist during actions, and both relate to disrupted memory for concurrent, albeit unpredictable sounds.

Dissociable effects of attention and expectation on perceptual sensitivity to action-outcomes

Self-generated sensations evoke attenuated neural response - physiological attenuation - and is perceived with less intensity - perceptual attenuation. This phenomenon is referred as sensory attenuation and is proposed to reflect the silencing of predicted sensations. The present study aimed to investigate the independent contribution of expectation and attention on sensory attenuation. The expectation associated with the stimulus feature and the focus of attention was manipulated independently by orthogonal cues. We found pronounced sensory attenuation at the unattended location when the stimulus was self-generated (Experiment 1). When the stimulus was externally-generated (Experiment 2), sensory attenuation was observed at the attended location. Sensory attenuation of expected action-outcome was not observed when the attention cue was uninformative (Experiment 3A). The findings corroborate the claim from Bayesian models that attention mediates sensory attenuation. The results also highlight the paradoxes in Bayesian proposals of perception–action interaction.

The Role of Action-Effect Contingency on Sensory Attenuation in the Absence of Movement.

Stimuli that have been generated by a person's own willed motor actions generally elicit a suppressed electrophysiological, as well as phenomenological, response compared with identical stimuli that have been externally generated. This well-studied phenomenon, known as sensory attenuation, has mostly been studied by comparing ERPs evoked by self-initiated and externally generated sounds. However, most studies have assumed a uniform action-effect contingency, in which a motor action leads to a resulting sensation 100% of the time. In this study, we investigated the effect of manipulating the probability of action-effect contingencies on the sensory attenuation effect. In Experiment 1, participants watched a moving, marked tickertape while EEG was recorded. In the full-contingency (FC) condition, participants chose whether to press a button by a certain mark on the tickertape. If a button press had not occurred by the mark, a sound would be played a second later 100% of the time. If the button was pressed before the mark, the sound was not played. In the no-contingency (NC) condition, participants observed the same tickertape; in contrast, however, if participants did not press the button by the mark, a sound would occur only 50% of the time (NC-inaction). Furthermore, in the NC condition, if a participant pressed the button before the mark, a sound would also play 50% of the time (NC-action). In Experiment 2, the design was identical, except that a willed action (as opposed to a willed inaction) triggered the sound in the FC condition. The results were consistent across the two experiments: Although there were no differences in N1 amplitude between conditions, the amplitude of the Tb and P2 components were smaller in the FC condition compared with the NC-inaction condition, and the amplitude of the P2 component was also smaller in the FC condition compared with the NC-action condition. The results suggest that the effect of contingency on electrophysiological indices of sensory attenuation may be indexed primarily by the Tb and P2 components, rather than the N1 component which is most commonly studied.

Perceptual sensory attenuation in chronic pain subjects and healthy controls

We investigated whether sensory attenuation (or failure of) might be an explanation for heightened pain perceptions in individuals with chronic pain. N = 131 (50% chronic pain) individuals underwent a single experimental session, which included the force-matching task and several self-reported symptom and psychological measures. Individuals matched a force delivered to their finger, either by pressing directly on their own finger with their other hand (direct) or by using potentiometer to control the force through a torque motor (slider). All participants overestimated the target force in the direct condition reflecting the sensory attenuation phenomenon. No differences in the magnitude of sensory attenuation between chronic pain and control groups were observed (direct: Z = − 0.90, p = 0.37 and slider: Z = − 1.41, p = 0.16). An increased variance of sensory attenuation was observed in chronic pain individuals (direct: F(1, 129) = 7.22, p = 0.008 and slider: F(1, 129), p = 0.05). Performance in the slider condition was correlated with depressive symptoms (r = − 0.24, p = 0.05), high symptom count (r = − 0.25, p = 0.04) and positive affect (r = 0.28, p = 0.02). These were only identified in the chronic pain individuals. Overall, our findings reveal no clear differences in the magnitude of sensory attenuation between groups. Future research is needed to determine the relevance of sensory attenuation in neuro-cognitive models related to pain perception.

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.