Don't do it! Cortical inhibition and self-attribution during action observation

Numerous studies suggest that both self-generated and observed actions of others activate overlapping neural networks, implying a shared, agent-neutral representation of self and other. Contrary to the shared representation hypothesis, we recently showed that the human motor system is not neutral with respect to the agent of an observed action [Schütz-Bosbach, S., Mancini, B., Aglioti, S. M., & Haggard, P. Self and other in the human motor system. Current Biology, 16, 1830-1834, 2006]. Observation of actions attributed to another agent facilitated the motor system, whereas observation of identical actions linked to the self did not. Here we investigate whether the absence of motor facilitation for observing one's own actions reflects a specific process of cortical inhibition associated with self-representation. We analyzed the duration of the silent period induced by transcranial magnetic stimulation of the motor cortex in active muscles as an indicator of motor inhibition. We manipulated whether an observed action was attributed to another agent, or to the subjects themselves, using a manipulation of body ownership on the basis of the rubber hand illusion. Observation of actions linked to the self led to longer silent periods than observation of a static hand, but the opposite effect occurred when observing identical actions attributed to another agent. This finding suggests a specific inhibition of the motor system associated with self-representation. Cortical suppression for actions linked to the self might prevent inappropriate perseveration within the motor system.     

Neural correlates of the misattribution of self-generated speech

Auditory hallucinations are thought to arise through the misidentification of self-generated verbal material as alien. The neural mechanisms that normally mediate the differentiation of self-generated from nonself speech are unclear. We investigated this in healthy volunteers using functional MRI. Eleven healthy volunteers were scanned whilst listening to a series of prerecorded words. The source (self/nonself) and acoustic quality (undistorted/distorted) of the speech was varied across trials. Participants indicated whether the words were spoken in their own or another person's voice via a button press. Listening to self-generated words was associated with more activation in the left inferior frontal and right anterior cingulate cortex than words in another person's voice, which was associated with greater engagement of the lateral temporal cortex bilaterally. Listening to distorted speech was associated with activation in the inferior frontal and anterior cingulate cortex. There was an interaction between the effects of source of speech and distortion on activation in the left temporal cortex. In the presence of distortion participants were more likely to misidentify their voice as that of another. This misattribution of self-generated speech was associated with reduced engagement of the cingulate and prefrontal cortices. The evaluation of auditory speech involves a network including the inferior frontal, anterior cingulate, and lateral temporal cortex. The degree to which different areas within this network are engaged varies with the source and acoustic quality of the speech. Accurate identification of one's own speech appears to depend on cingulate and prefrontal activity.     

The influence of intrapersonal sensorimotor experiences on the corticospinal responses during action–observation

The coupling of perception and action has been strongly indicated by evidence that the observation of an action primes a response in the observer. It has been proposed that these primed responses may be inhibited when the observer is able to more closely distinguish between self- and other-generated actions – the greater the distinction, then the greater the inhibition of the primed response. This self–other distinction is shown to be enhanced following a period of visual feedback of self-generated action. The present study was designed to examine how sensorimotor experiences pertaining to self-generated action affect primed responses from observed actions. Single-pulse transcranial magnetic stimulation was used to investigate corticospinal activity elicited during the observation of index- and little-finger actions before and after training (self-generated action). For sensorimotor training, participants executed finger movements with or without visual feedback of their own movement. Results showed that the increases in muscle-specific corticospinal activity elicited from action–observation persisted after training without visual feedback, but did not emerge following training with visual feedback. This inhibition in corticospinal activity during action–observation following training with vision could have resulted from the refining of internal models of self-generated action, which then led to a greater distinction between “self” and “other” actions.     

Increased Functional Connectivity of the Intraparietal Sulcus Underlies the Attenuation of Numerosity Estimations for Self-Generated Words

Previous studies have shown that self-generated stimuli in auditory, visual, and somatosensory domains are attenuated, producing decreased behavioral and neural responses compared with the same stimuli that are externally generated. Yet, whether such attenuation also occurs for higher-level cognitive functions beyond sensorimotor processing remains unknown. In this study, we assessed whether cognitive functions such as numerosity estimations are subject to attenuation in 56 healthy participants (32 women). We designed a task allowing the controlled comparison of numerosity estimations for self-generated (active condition) and externally generated (passive condition) words. Our behavioral results showed a larger underestimation of self-generated compared with externally generated words, suggesting that numerosity estimations for self-generated words are attenuated. Moreover, the linear relationship between the reported and actual number of words was stronger for self-generated words, although the ability to track errors about numerosity estimations was similar across conditions. Neuroimaging results revealed that numerosity underestimation involved increased functional connectivity between the right intraparietal sulcus and an extended network (bilateral supplementary motor area, left inferior parietal lobule, and left superior temporal gyrus) when estimating the number of self-generated versus externally generated words. We interpret our results in light of two models of attenuation and discuss their perceptual versus cognitive origins.SIGNIFICANCE STATEMENT We perceive sensory events as less intense when they are self-generated compared with when they are externally generated. This phenomenon, called attenuation, enables us to distinguish sensory events from self and external origins. Here, we designed a novel fMRI paradigm to assess whether cognitive processes such as numerosity estimations are also subject to attenuation. When asking participants to estimate the number of words they had generated or passively heard, we found bigger underestimation in the former case, providing behavioral evidence of attenuation. Attenuation was associated with increased functional connectivity of the intraparietal sulcus, a region involved in numerosity processing. Together, our results indicate that the attenuation of self-generated stimuli is not limited to sensory consequences but is also impact cognitive processes such as numerosity estimations.     

Neural activity related to self- versus externally generated painful stimuli reveals distinct differences in the lateral pain system in a parametric fMRI study

Self-generated sensory stimulation can be distinguished from externally generated stimulation that is otherwise identical. To determine how the brain differentiates external from self-generated noxious stimulation and which structures of the lateral pain system use neural signals to predict the sensory consequences of self-generated painful stimulation, we used functional magnetic resonance imaging to examine healthy human subjects who received thermal-contact stimuli with noxious and non-noxious temperatures on the resting right hand in random order. These stimuli were internally (self-generated) or externally generated. Two additional conditions served as control conditions: to account for stimulus onset uncertainty, acoustic stimuli preceding the same thermal stimuli were used with variable or fixed delays but without any stimulus-eliciting movements. Whereas graded pain-related activity in the insula and secondary somatosensory cortex (SII) was independent of how the stimulus was generated, it was attenuated in the primary somatosensory cortex (SI) during self-generated stimulation. These data agree with recent concepts of the parallel processing of nociceptive signals to the primary and secondary somatosensory cortices. They also suggest that brain areas that encode pain intensity do not distinguish between internally or externally applied noxious stimuli, i.e., this adaptive biological mechanism prevents harm to the individual. The attenuated activation of SI during self-generated painful stimulation might be a result of the predictability of the sensory consequences of the pain-related action.     

Psychopathological and neuropsychological correlates of source monitoring impairment in schizophrenia

Schizophrenic patients are known to show a deficit in the source monitoring function, which refers to the set of processes involved in the attribution of an origin to memories and beliefs. A failure in source monitoring was found to be associated with Schneiderian delusions in the recent literature. This study aimed to explore in a sample of schizophrenic patients and controls two aspects of the source monitoring process-recognition and source attribution- and their possible correlation with psychopathology and basic neuropsychological performances. A group of 45 stabilized schizophrenic patients and 54 normal volunteers were studied with a Source Monitoring Task and a battery of neurocognitive functions known to be disturbed in schizophrenia. Recognition of self-generated items was significantly worse than control values in Schneiderian delusional patients only, while source attribution of recognized self-generated items was significantly biased towards the external sources in all delusional patients in comparison to controls. Among schizophrenic patients, source misattribution of self-generated items was significantly correlated to an executive, planning performance. Both performances were correlated to verbal memory in controls. Results confirm an impairment of different subcomponents of source monitoring performance in schizophrenia, heterogeneously related to psychopathological features and neuropsychological performances known to be impaired in schizophrenia.     

Considerations for analysis of source monitoring data when investigating hallucinations in schizophrenia research

Self/other (i.e., internal/external) source monitoring is one of the leading paradigms for the study of hallucinations in schizophrenia. The cognitive processes that underlie hallucinations are theorized to transform self-generated (internal) cognitive events into other-generated (external) cognitive events. These proposed cognitive operations also appear to play a role in producing analogous types of errors in self/other source monitoring, namely a memory bias whereby recalled material that was self-generated is misremembered as other-generated, referred to as an externalization bias. Externalization biases are more frequent in groups of hallucinating schizophrenia patients than in other groups. One source of measurement error that is inherent in the study of the externalization bias is that, even for never-previously viewed items, there is a tendency to guess an external source under conditions of uncertainty. If such guessing takes place in response to self-generated but forgotten items, these guesses will be summed along with true externalization biases in the frequency count of externalizations, producing measurement error. Multinomial modeling is a statistical technique that has been used to estimate the influence of external-source guessing in order to separate it from true externalization bias estimates. However, a number of challenges related to model choice and model validation are involved, and these challenges may render multinomial modeling impractical. We instead recommend analysis of covariance (ANCOVA), or difference score methodology, as an appropriate method for partialling external-source guessing rates (external-source false positives) out of externalization bias rates.     

Auditory hallucinations, source monitoring, and the belief that "voices" are real

The term source monitoring refers to a variety of cognitive processes individuals use to determine whether an experience originated within the self or came from an external source. A belief that auditory hallucinations are real entities independent of the self may be considered an error in source monitoring. The Source Monitoring Framework (SMF) is the most developed and empirically validated model of how ordinary individuals judge whether an event was self-generated or occurred in the outside world. This study of 41 acute inpatients is a first attempt to apply the SMF to autobiographical reports of auditory hallucinations in a clinical setting. Consistent with the SMF, results suggest that similarities between "voices" and real speakers may offer a partial explanation of why patients believe the voices are real. While the SMF provides a useful conceptual background for examining the phenomenology of these voices, the types of source monitoring errors typically encountered in normal individuals do not fully account for this belief as it occurs in psychotic individuals.     

Attentional Modulation of Source Attribution in First-Episode Psychosis: A Functional Magnetic Resonance Imaging Study

Background: In patients with schizophrenia, the misattribution of self-generated events to an external source is associated with the presence of psychotic symptoms. The aim of this study was to investigate how this misattribution is influenced by dysfunction of attentional processing, which is also impaired in schizophrenia. Methods: Participants underwent functional Magnetic Resonance Imaging (fMRI) while listening to prerecorded speech. Their expectancies were manipulated using visual cues that were either congruent (valid) or incongruent (invalid) with the speech. The source (self/other) and the acoustic quality (undistorted/distorted) of the speech were also manipulated. Twenty patients with first-episode psychosis (FEP) and 20 matched healthy controls (HC) were tested. Results: When listening to self-generated speech preceded by an invalid (other speech) cue, relative to HC, FEP patients showed a trend to misidentify their own speech as that of another person. Analysis of fMRI data showed that FEP patients had reduced activation in the right middle temporal gyrus (MTG) and left precuneus (Pc) relative to HC. Within the FEP group, the level of activation in the right MTG was negatively correlated with the severity of their positive psychotic symptoms. Conclusions: Impaired attentional modulation in schizophrenia may contribute to the tendency for FEP patients to misattribute the source of self-generated material, and this may be mediated by the right MTG and Pc, regions that are involved in both self-referential processing and the integration of sensory information.Key words: psychosis, schizophrenia, speech, self-recognition, attention, top-down, bottom-up     

Deficits in sensory prediction are related to delusional ideation in healthy individuals

Motor control strongly relies on neural processes that predict the sensory consequences of self-generated actions. Previous research has demonstrated deficits in such sensory-predictive processes in schizophrenic patients and these low-level deficits are thought to contribute to the emergence of delusions of control. Here, we examined the extent to which individual differences in sensory prediction are associated with a tendency towards delusional ideation in healthy participants. We used a force-matching task to quantify sensory-predictive processes, and administered questionnaires to assess schizotypy and delusion-like thinking. Individuals with higher levels of delusional ideation showed more accurate force matching suggesting that such thinking is associated with a reduced tendency to predict and attenuate the sensory consequences of self-generated actions. These results suggest that deficits in sensory prediction in schizophrenia are not simply consequences of the deluded state and are not related to neuroleptic medication. Rather they appear to be stable, trait-like characteristics of an individual, a finding that has important implications for our understanding of the neurocognitive basis of delusions.     

Exploring psychotic symptoms: a comparison of motor related neuronal activation during and after acute psychosis

ABSTRACT: BACKGROUND: Delusions and hallucinations are classic positive symptoms of schizophrenia. A contemporary cognitive theory called the 'forward output model' suggests that the misattribution of self-generated actions may underlie some of these types of symptoms, such as delusions of control [EN DASH] the experience of self-generated action being controlled by an external agency. In order to examine the validity of this suggestion, we performed a longitudinal functional magnetic resonance imaging (fMRI) study examining neuronal activation associated with motor movement during acute psychosis. METHODS: We studied brain activation using fMRI during a motor task in 11 patients with schizophrenia and 9 healthy controls. The patient group was tested at two time points separated by 6[EN DASH]8 weeks. RESULTS: At initial testing, the patient group had a mean Positive and Negative Syndrome Scale score of 56.3, and showed significantly increased activation within the left inferior parietal lobe (IPL) compared to controls. Patients reported significantly decreased positive symptoms at 6[EN DASH]8 week followup and IPL activation had returned to normal. Our results demonstrate that first-rank positive symptoms are associated with hyperactivation in the secondary somatosensory cortex (IPL). CONCLUSIONS: These findings lend further credence to the theory that a dysfunction in the sensory feedback system located in the IPL, and which is thought to underlie our sense of agency, may contribute to the aetiology of delusions of control.     

New insights into corollary discharges mediated by identified neural pathways

Sensory systems respond not only to stimuli from the environment but also to cues generated by an animal's own behaviour. This leads to problems of sensory processing because self-generated information can occur at the same time as external sensory information. However, in motor regions of the CNS corollary discharges are generated during behaviour. These signals are not used to generate movements directly but, instead, interact with the processing of self-generated sensory signals. Corollary discharges transiently modulate self-generated sensory responses and can prevent self-induced desensitization or help distinguish between self-generated and externally generated sensory information. Here, we review recent work that has identified corollary discharge pathways at different levels of the CNS in vertebrates and invertebrates.     

Misattribution of self-generated speech in relation to hallucinatory proneness and delusional ideation in healthy volunteers

When patients with hallucinations and delusions encounter their own distorted speech they tend to mistakenly attribute it to someone else. This external misattribution of self-generated material is thought to be associated with 'positive' psychotic symptoms. The aim of the present study was to examine this process in relation to the predisposition to hallucination-like experiences and unusual beliefs in a healthy population. Fifty-seven volunteers completed assessments of hallucination proneness and delusional ideation and performed a source-monitoring task. Participants listened to a series of pre-recorded words for which the source (self/non-self) and acoustic quality (undistorted/distorted) of the speech were varied across trials. Participants indicated whether the words were spoken in their own or another person's voice via a button press. Misattribution errors were greatest when participants made source judgements about their own distorted speech (p < 0.01) and were positively correlated with delusional ideation scores, particularly the level of conviction with which delusional ideas were held (p = 0.03), and there was a trend for a positive correlation with hallucination proneness scores. There was a negative correlation between unsure responses and delusional ideation when participants were processing their own distorted speech (p = -0.03). The misattribution of self-generated speech occurs in healthy individuals with high levels of psychotic-like experiences. This suggests that the same cognitive impairments may underlie psychotic phenomena in healthy individuals as in patients with psychotic disorders, consistent with a continuum model of psychosis.     

Toward Robot Self-Consciousness (II): Brain-Inspired Robot Bodily Self Model for Self-Recognition

The neural correlates and nature of self-consciousness is an advanced topic in Cognitive Neuroscience. Only a few animal species have been testified to be with this cognitive ability. From artificial intelligence and robotics point of view, few efforts are deeply rooted in the neural correlates and brain mechanisms of biological self-consciousness. Despite the fact that the scientific understanding of biological self-consciousness is still in preliminary stage, we make our efforts to integrate and adopt known biological findings of self-consciousness to build a brain-inspired model for robot self-consciousness. In this paper, we propose a brain-inspired robot bodily self model based on extensions to primate mirror neuron system and apply it to humanoid robot for self recognition. In this model, the robot firstly learns the correlations between self-generated actions and visual feedbacks in motion by learning with spike timing dependent plasticity (STDP), and then learns the appearance of body part with the expectation that the visual feedback is consistent with its motion. Based on this model, the robot uses multisensory integration to learn its own body in real world and in mirror. Then it can distinguish itself from others. In a mirror test setting with three robots with the same appearance, with the proposed brain-inspired robot bodily self model, each of them can recognize itself in the mirror after these robots make random movements at the same time. The theoretic modeling and experimental validations indicate that the brain-inspired robot bodily self model is biologically inspired, and computationally feasible as a foundation for robot self recognition.     

Relationship between source monitoring in episodic memory and executive function in normal aging

Age-related source monitoring decline in episodic memory has been traditionally attributed to executive dysfunctioning. However, the literature does not reveal whether all source monitoring categories are impaired at the same level in the elderly. It is also unclear whether the source monitoring decline can be attributed to a specific executive function. In the present paper, we address these shortcomings by using specific source monitoring and executive tasks. Twenty four young and 22 older healthy adults, paired by sex and vocabulatory level, were assessed with original and simple source monitoring tasks tapping reality monitoring (discrimination between self- vs. other-generated sources), external monitoring (discrimination between external sources), and internal monitoring (discrimination between self-generated sources). They were also given specific executive measures assessing inhibition, flexibility, and updating. Relatively to the younger adults, poor source monitoring was found in the older participants. This decline was more pronounced for external monitoring. The latter performance was further predicted by inhibition. Our results emphasize the role of inhibitory processes in older adults' source monitoring decline.     

Lateralization of the posterior parietal cortex for internal monitoring of self- versus externally generated movements

Internal monitoring or state estimation of movements is essential for human motor control to compensate for inherent delays and noise in sensorimotor loops. Two types of internal estimation of movements exist: self-generated movements, and externally generated movements. We used functional magnetic resonance imaging to investigate differences in brain activity for internal monitoring of self- versus externally generated movements during visual occlusion. Participants tracked a sinusoidally moving target with a mouse cursor. On some trials, vision of either target (externally generated) or cursor (self-generated) movement was transiently occluded, during which subjects continued tracking by estimating current position of either the invisible target or cursor on screen. Analysis revealed that both occlusion conditions were associated with increased activity in the presupplementary motor area and decreased activity in the right lateral occipital cortex compared to a control condition with no occlusion. Moreover, the right and left posterior parietal cortex (PPC) showed greater activation during occlusion of target and cursor movements, respectively. This study suggests lateralization of the PPC for internal monitoring of internally versus externally generated movements, fully consistent with previously reported clinical findings.     

Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations

Several studies report that patients with schizophrenia who experience auditory verbal hallucinations (AVH) tend to misidentify their own speech as that of somebody else. We tested the hypothesis that this tendency is associated with poor functional integration within the network of regions that mediate the evaluation of speech. Using functional magnetic resonance imaging, we measured brain responses from 11 schizophrenics with AVH, 10 schizophrenics without AVH, and 10 healthy controls. Stimuli comprised prerecorded words, which varied for their source (self, alien) and acoustic quality (undistorted, distorted). Participants had to indicate whether each word was spoken in their own or another person's voice via a button press. Using dynamic causal modeling, we estimated the impact of one region over another ("effective connectivity") and how this was modulated by source and distortion. In controls and in patients without AVH, the connectivity between left superior temporal and anterior cingulate cortex was significantly greater for alien- than for self-generated speech; in contrast, the reverse trend was found in schizophrenic patients with AVH. In conclusion, when patients with AVH appraise their own speech we find impaired functional integration between left superior temporal and anterior cingulate cortex. Although this finding is based on external rather than internal speech, the same mechanism may contribute to the faulty appraisal of inner speech that putatively underlies AVH.     

Disturbances of self–other distinction after stimulation of the extrastriate body area in the human brain

Abstract

In a recent experiment with functional magnetic-resonance imaging, we found that brain activity in the extrastriate body area (EBA) distinguished between observed self- and other-generated movements, being significantly higher during observation of someone else's movement. Here, we investigated further the role of EBA in self–other distinctions using low-frequency repetitive transcranial magnetic stimulation (rTMS). As compared with rTMS applied over a control site, rTMS applied over the EBA increased reaction times, without affecting accuracy, for the detection of other-generated movements. Performance on a control motion-direction detection task was unaffected. These findings provide additional evidence for the role of the EBA in processing information necessary for identifying ourselves as agents of self-generated movements.     

Prehension Kinematics,Grasping Forces,and Independent Finger Control in Mildly Affected Patients with Essential Tremor

Although the pathophysiology of essential tremor (ET), one of the most common movement disorders, is not fully understood, evidence increasingly points to cerebellar involvement. To confirm this connection, we assessed the everyday hand and finger movements of patients with ET, as these movements are known to be affected in cerebellar diseases. In 26 mildly affected patients with ET (compared to age- and gender-matched controls), kinematic and finger force parameters were assessed in a precision grip. In a second task, independent finger movements were recorded. The active finger had to press and release against a force-sensitive keypad while the other fingers stayed inactive. Finally, control of grip force to movement-induced, self-generated load changes was studied. Transport and shaping components during prehension were significantly impaired in patients with ET compared to controls. No significant group differences were observed in independent finger movements and grip force adjustments to self-generated load force changes. However, in the latter two tasks, more severely affected ET patients performed worse than less affected. Although observed deficits in hand and finger movement tasks were small, they are consistent with cerebellar dysfunction in ET. Findings need to be confirmed in future studies examining more severely affected ET patients.     

Abnormalities of motor imagery associated with somatic passivity phenomena in schizophrenia

Some patients with schizophrenia report that their limbs are under the control of an alien force (motor passivity). This is hypothesised to be due to the dysfunction of an internal self-monitoring system that normally permits distinctions between internally generated and external influences on intentional behaviour. Motor imagery is the mental simulation of specific motor actions and it is based upon the internal representation of intended but unexecuted motor actions. Therefore, the generation of motor imagery should be impaired in schizophrenia characterised by passivity phenomena. The generation of motor imagery was compared using the visually guided pointing task (VGPT) and the Florida praxis imagery questionnaire (FPIQ) between patients with schizophrenia characterised by high levels of passivity symptoms (passivity) and patients without passivity symptoms (no-passivity). In both the passivity and no-passivity groups, the speed of real motor sequences on the VGPT was constrained by the distance of the movement and the width of the target in accordance with Fitts' law. For the no-passivity group, the same relationship was found for imagined movements. However, in the passivity group, imagined movements were not constrained by Fitts' law. The effect of a 2-kg load to the limb performing real or imagined movements on the VGPT was identical in both groups. The duration of imagined movements was slowed although the duration of real movements was unaffected. The FPIQ showed that the passivity group had difficulty answering questions that required them to imagine kinaesthetic aspects of performing simple gestures. These results suggest that passivity phenomena in schizophrenia are associated with a specific inability to represent the timing of motor actions internally. This is consistent with the hypothesis that patients with passivity phenomena have difficulty with maintaining an internal representation of intentional behaviour.