The role of self–other distinction in understanding others' mental and emotional states: neurocognitive mechanisms in children and adults

Social interactions come with the fundamental problem of trying to understand others'' mental and affective states while under the overpowering influence of one''s own concurrent thoughts and feelings. The ability to distinguish between simultaneous representations of others'' current experiences as well as our own is crucial to navigate our complex social environments successfully. The developmental building blocks of this ability and how this is given rise to by functional and structural brain development remains poorly understood. In this review, I outline some of the key findings on the role of self–other distinction in understanding others'' mental as well as emotional states in children and adults. I will begin by clarifying the crucial role for self–other distinction in avoiding egocentric attributions of one''s own cognitive as well as affective states to others in adults and outline the underlying neural circuitry in overcoming such egocentricity. This will provide the basis for a discussion of the emergence of self–other distinction in early childhood as well as developmental changes therein throughout childhood and into adulthood. I will demonstrate that self–other distinction of cognitive and emotional states is already dissociable early in development. Concomitantly, I will show that processes of self–other distinction in cognitive and affective domains rely on adjacent but distinct neural circuitry each with unique connectivity profiles, presumably related to the nature of the distinction that needs to be made.     

If I Were You: Perceptual Illusion of Body Swapping

The concept of an individual swapping his or her body with that of another person has captured the imagination of writers and artists for decades. Although this topic has not been the subject of investigation in science, it exemplifies the fundamental question of why we have an ongoing experience of being located inside our bodies. Here we report a perceptual illusion of body-swapping that addresses directly this issue. Manipulation of the visual perspective, in combination with the receipt of correlated multisensory information from the body was sufficient to trigger the illusion that another person''s body or an artificial body was one''s own. This effect was so strong that people could experience being in another person''s body when facing their own body and shaking hands with it. Our results are of fundamental importance because they identify the perceptual processes that produce the feeling of ownership of one''s body.     

Action Possibility Judgments of People with Varying Motor Abilities Due to Spinal Cord Injury

Predictions about one''s own action capabilities as well as the action capabilities of others are thought to be based on a simulation process involving linked perceptual and motor networks. Given the central role of motor experience in the formation of these networks, one''s present motor capabilities are thought to be the basis of their perceptual judgments about actions. However, it remains unknown whether the ability to form these action possibility judgments is affected by performance related changes in the motor system. To determine if judgments of action capabilities are affected by long-term changes in one''s own motor capabilities, participants with different degrees of upper-limb function due to their level (cervical vs. below cervical) of spinal cord injury (SCI) were tested on a perceptual-motor judgment task. Participants observed apparent motion videos of reciprocal aiming movements with varying levels of difficulty. For each movement, participants determined the shortest movement time (MT) at which they themselves and a young adult could perform the task while maintaining accuracy. Participants also performed the task. Analyses of MTs revealed that perceptual judgments for participant''s own movement capabilities were consistent with their actual performance- people with cervical SCI had longer judged and actual MTs than people with below cervical SCI. However, there were no between-group differences in judged MTs for the young adult. Although it is unclear how the judgments were adjusted (altered simulation vs. threshold modification), the data reveal that people with different motor capabilities due to SCI are not completely biased by their present capabilities and can effectively adjust their judgments to estimate the actions of others.     

Common Premotor Regions for the Perception and Production of Prosody and Correlations with Empathy and Prosodic Ability

Background

Prosody, the melody and intonation of speech, involves the rhythm, rate, pitch and voice quality to relay linguistic and emotional information from one individual to another. A significant component of human social communication depends upon interpreting and responding to another person''s prosodic tone as well as one''s own ability to produce prosodic speech. However there has been little work on whether the perception and production of prosody share common neural processes, and if so, how these might correlate with individual differences in social ability.

Methods

The aim of the present study was to determine the degree to which perception and production of prosody rely on shared neural systems. Using fMRI, neural activity during perception and production of a meaningless phrase in different prosodic intonations was measured. Regions of overlap for production and perception of prosody were found in premotor regions, in particular the left inferior frontal gyrus (IFG). Activity in these regions was further found to correlate with how high an individual scored on two different measures of affective empathy as well as a measure on prosodic production ability.

Conclusions

These data indicate, for the first time, that areas that are important for prosody production may also be utilized for prosody perception, as well as other aspects of social communication and social understanding, such as aspects of empathy and prosodic ability.     

Am I seeing my hand? Visual appearance and knowledge of controllability both contribute to the visual capture of a person's own body

When confronted with complex visual scenes in daily life, how do we know which visual information represents our own hand? We investigated the cues used to assign visual information to one''s own hand. Wrist tendon vibration elicits an illusory sensation of wrist movement. The intensity of this illusion attenuates when the actual motionless hand is visually presented. Testing what kind of visual stimuli attenuate this illusion will elucidate factors contributing to visual detection of one''s own hand. The illusion was reduced when a stationary object was shown, but only when participants knew it was controllable with their hands. In contrast, the visual image of their own hand attenuated the illusion even when participants knew that it was not controllable. We suggest that long-term knowledge about the appearance of the body and short-term knowledge about controllability of a visual object are combined to robustly extract our own body from a visual scene.     

Brain Regions Associated to a Kinesthetic Illusion Evoked by Watching a Video of One's Own Moving Hand

It is well known that kinesthetic illusions can be induced by stimulation of several sensory systems (proprioception, touch, vision…). In this study we investigated the cerebral network underlying a kinesthetic illusion induced by visual stimulation by using functional magnetic resonance imaging (fMRI) in humans. Participants were instructed to keep their hand still while watching the video of their own moving hand (Self Hand) or that of someone else''s moving hand (Other Hand). In the Self Hand condition they experienced an illusory sensation that their hand was moving whereas the Other Hand condition did not induce any kinesthetic illusion. The contrast between the Self Hand and Other Hand conditions showed significant activation in the left dorsal and ventral premotor cortices, in the left Superior and Inferior Parietal lobules, at the right Occipito-Temporal junction as well as in bilateral Insula and Putamen. Most strikingly, there was no activation in the primary motor and somatosensory cortices, whilst previous studies have reported significant activation in these regions for vibration-induced kinesthetic illusions. To our knowledge, this is the first study that indicates that humans can experience kinesthetic perception without activation in the primary motor and somatosensory areas. We conclude that under some conditions watching a video of one''s own moving hand could lead to activation of a network that is usually involved in processing copies of efference, thus leading to the illusory perception that the real hand is indeed moving.     

Looking for Myself: Current Multisensory Input Alters Self-Face Recognition

How do I know the person I see in the mirror is really me? Is it because I know the person simply looks like me, or is it because the mirror reflection moves when I move, and I see it being touched when I feel touch myself? Studies of face-recognition suggest that visual recognition of stored visual features inform self-face recognition. In contrast, body-recognition studies conclude that multisensory integration is the main cue to selfhood. The present study investigates for the first time the specific contribution of current multisensory input for self-face recognition. Participants were stroked on their face while they were looking at a morphed face being touched in synchrony or asynchrony. Before and after the visuo-tactile stimulation participants performed a self-recognition task. The results show that multisensory signals have a significant effect on self-face recognition. Synchronous tactile stimulation while watching another person''s face being similarly touched produced a bias in recognizing one''s own face, in the direction of the other person included in the representation of one''s own face. Multisensory integration can update cognitive representations of one''s body, such as the sense of ownership. The present study extends this converging evidence by showing that the correlation of synchronous multisensory signals also updates the representation of one''s face. The face is a key feature of our identity, but at the same time is a source of rich multisensory experiences used to maintain or update self-representations.     

Motor Preparatory Activity in Posterior Parietal Cortex is Modulated by Subjective Absolute Value

For optimal response selection, the consequences associated with behavioral success or failure must be appraised. To determine how monetary consequences influence the neural representations of motor preparation, human brain activity was scanned with fMRI while subjects performed a complex spatial visuomotor task. At the beginning of each trial, reward context cues indicated the potential gain and loss imposed for correct or incorrect trial completion. FMRI-activity in canonical reward structures reflected the expected value related to the context. In contrast, motor preparatory activity in posterior parietal and premotor cortex peaked in high “absolute value” (high gain or loss) conditions: being highest for large gains in subjects who believed they performed well while being highest for large losses in those who believed they performed poorly. These results suggest that the neural activity preceding goal-directed actions incorporates the absolute value of that action, predicated upon subjective, rather than objective, estimates of one''s performance.     

The Emotional and Attentional Impact of Exposure to One's Own Body in Bulimia Nervosa: A Physiological View

Background

Body dissatisfaction is the most relevant body image disturbance in bulimia nervosa (BN). Research has shown that viewing one''s own body evokes negative thoughts and emotions in individuals with BN. However, the psychophysiological mechanisms involved in this negative reaction have not yet been clearly established. Our aim was to examine the emotional and attentional processes that are activated when patients with BN view their own bodies.

Method

We examined the effects of viewing a video of one''s own body on the physiological (eye-blink startle, cardiac defense, and skin conductance) and subjective (pleasure, arousal, and control ratings) responses elicited by a burst of 110 dB white noise of 500 ms duration. The participants were 30 women with BN and 30 healthy control women. The experimental task consisted of two consecutive and counterbalanced presentations of the auditory stimulus preceded, alternatively, by a video of the participant''s own body versus no such video.

Results

The results showed that, when viewing their own bodies, women with BN experienced (a) greater inhibition of the startle reflex, (b) greater cardiac acceleration in the first component of the defense reaction, (c) greater skin conductance response, and (d) less subjective pleasure and control combined with greater arousal, compared with the control participants.

Conclusion

Our findings suggest that, for women with BN, peripheral-physiological responses to self-images are dominated by attentional processes, which provoke an immobility reaction caused by a dysfunctional negative response to their own body.     

The Crossmodal Congruency Task as a Means to Obtain an Objective Behavioral Measure in the Rubber Hand Illusion Paradigm

The rubber hand illusion (RHI) is a popular experimental paradigm. Participants view touch on an artificial rubber hand while the participants'' own hidden hand is touched. If the viewed and felt touches are given at the same time then this is sufficient to induce the compelling experience that the rubber hand is one''s own hand. The RHI can be used to investigate exactly how the brain constructs distinct body representations for one''s own body. Such representations are crucial for successful interactions with the external world. To obtain a subjective measure of the RHI, researchers typically ask participants to rate statements such as "I felt as if the rubber hand were my hand". Here we demonstrate how the crossmodal congruency task can be used to obtain an objective behavioral measure within this paradigm.The variant of the crossmodal congruency task we employ involves the presentation of tactile targets and visual distractors. Targets and distractors are spatially congruent (i.e. same finger) on some trials and incongruent (i.e. different finger) on others. The difference in performance between incongruent and congruent trials - the crossmodal congruency effect (CCE) - indexes multisensory interactions. Importantly, the CCE is modulated both by viewing a hand as well as the synchrony of viewed and felt touch which are both crucial factors for the RHI.The use of the crossmodal congruency task within the RHI paradigm has several advantages. It is a simple behavioral measure which can be repeated many times and which can be obtained during the illusion while participants view the artificial hand. Furthermore, this measure is not susceptible to observer and experimenter biases. The combination of the RHI paradigm with the crossmodal congruency task allows in particular for the investigation of multisensory processes which are critical for modulations of body representations as in the RHI.     

Being Moved by the Self and Others: Influence of Empathy on Self-Motion Perception

Background

The observation of conspecifics influences our bodily perceptions and actions: Contagious yawning, contagious itching, or empathy for pain, are all examples of mechanisms based on resonance between our own body and others. While there is evidence for the involvement of the mirror neuron system in the processing of motor, auditory and tactile information, it has not yet been associated with the perception of self-motion.

Methodology/Principal Findings

We investigated whether viewing our own body, the body of another, and an object in motion influences self-motion perception. We found a visual-vestibular congruency effect for self-motion perception when observing self and object motion, and a reduction in this effect when observing someone else''s body motion. The congruency effect was correlated with empathy scores, revealing the importance of empathy in mirroring mechanisms.

Conclusions/Significance

The data show that vestibular perception is modulated by agent-specific mirroring mechanisms. The observation of conspecifics in motion is an essential component of social life, and self-motion perception is crucial for the distinction between the self and the other. Finally, our results hint at the presence of a “vestibular mirror neuron system”.     

Mirror adaptation in sensory-motor simultaneity

Background

When one watches a sports game, one may feel her/his own muscles moving in synchrony with the player''s. Such parallels between observed actions of others and one''s own has been well supported in the latest progress in neuroscience, and coined “mirror system.” It is likely that due to such phenomena, we are able to learn motor skills just by observing an expert''s performance. Yet it is unknown whether such indirect learning occurs only at higher cognitive levels, or also at basic sensorimotor levels where sensorimotor delay is compensated and the timing of sensory feedback is constantly calibrated.

Methodology/Principal Findings

Here, we show that the subject''s passive observation of an actor manipulating a computer mouse with delayed auditory feedback led to shifts in subjective simultaneity of self mouse manipulation and auditory stimulus in the observing subjects. Likewise, self adaptation to the delayed feedback modulated the simultaneity judgment of the other subjects manipulating a mouse and an auditory stimulus. Meanwhile, subjective simultaneity of a simple visual disc and the auditory stimulus (flash test) was not affected by observation of an actor nor self-adaptation.

Conclusions/Significance

The lack of shift in the flash test for both conditions indicates that the recalibration transfer is specific to the action domain, and is not due to a general sensory adaptation. This points to the involvement of a system for the temporal monitoring of actions, one that processes both one''s own actions and those of others.     

Predictive motor activation during action observation in human infants

Certain regions of the human brain are activated both during action execution and action observation. This so-called ‘mirror neuron system’ has been proposed to enable an observer to understand an action through a process of internal motor simulation. Although there has been much speculation about the existence of such a system from early in life, to date there is little direct evidence that young infants recruit brain areas involved in action production during action observation. To address this question, we identified the individual frequency range in which sensorimotor alpha-band activity was attenuated in nine-month-old infants'' electroencephalographs (EEGs) during elicited reaching for objects, and measured whether activity in this frequency range was also modulated by observing others'' actions. We found that observing a grasping action resulted in motor activation in the infant brain, but that this activity began prior to observation of the action, once it could be anticipated. These results demonstrate not only that infants, like adults, display overlapping neural activity during execution and observation of actions, but that this activation, rather than being directly induced by the visual input, is driven by infants'' understanding of a forthcoming action. These results provide support for theories implicating the motor system in action prediction.     

Meditation Experience Predicts Introspective Accuracy

The accuracy of subjective reports, especially those involving introspection of one''s own internal processes, remains unclear, and research has demonstrated large individual differences in introspective accuracy. It has been hypothesized that introspective accuracy may be heightened in persons who engage in meditation practices, due to the highly introspective nature of such practices. We undertook a preliminary exploration of this hypothesis, examining introspective accuracy in a cross-section of meditation practitioners (1–15,000 hrs experience). Introspective accuracy was assessed by comparing subjective reports of tactile sensitivity for each of 20 body regions during a ‘body-scanning’ meditation with averaged, objective measures of tactile sensitivity (mean size of body representation area in primary somatosensory cortex; two-point discrimination threshold) as reported in prior research. Expert meditators showed significantly better introspective accuracy than novices; overall meditation experience also significantly predicted individual introspective accuracy. These results suggest that long-term meditators provide more accurate introspective reports than novices.     

Vestibular humanoid postural control

Many of our motor activities require stabilization against external disturbances. This especially applies to biped stance since it is inherently unstable. Disturbance compensation is mainly reactive, depending on sensory inputs and real-time sensor fusion. In humans, the vestibular system plays a major role. When there is no visual space reference, vestibular-loss clearly impairs stance stability. Most humanoid robots do not use a vestibular system, but stabilize upright body posture by means of center of pressure (COP) control. We here suggest using in addition a vestibular sensor and present a biologically inspired vestibular sensor along with a human-inspired stance control mechanism. We proceed in two steps. First, in an introductory review part, we report on relevant human sensors and their role in stance control, focusing on own models of transmitter fusion in the vestibular sensor and sensor fusion in stance control. In a second, experimental part, the models are used to construct an artificial vestibular system and to embed it into the stance control of a humanoid. The robot’s performance is investigated using tilts of the support surface. The results are compared to those of humans. Functional significance of the vestibular sensor is highlighted by comparing vestibular-able with vestibular-loss states in robot and humans. We show that a kinematic body-space sensory feedback (vestibular) is advantageous over a kinetic one (force cues) for dynamic body-space balancing. Our embodiment of human sensorimotor control principles into a robot is more than just bionics. It inspired our biological work (neurorobotics: ‘learning by building’, proof of principle, and more). We envisage a future clinical use in the form of hardware-in-the-loop simulations of neurological symptoms for improving diagnosis and therapy and designing medical assistive devices.     

Social cognition and psychopathology: a critical overview

The philosophical and interdisciplinary debate about the nature of social cognition, and the processes involved, has important implications for psychiatry. On one account, mindreading depends on making theoretical inferences about another person''s mental states based on knowledge of folk psychology, the so-called “theory theory” (TT). On a different account, “simulation theory” (ST), mindreading depends on simulating the other''s mental states within one''s own mental or motor system. A third approach, “interaction theory” (IT), looks to embodied processes (involving movement, gesture, facial expression, vocal intonation, etc.) and the dynamics of intersubjective interactions (joint attention, joint action, and processes not confined to an individual system) in highly contextualized situations to explain social cognition, and disruptions of these processes in some psychopathological conditions. In this paper, we present a brief summary of these three theoretical frameworks (TT, ST, IT). We then focus on impaired social abilities in autism and schizophrenia from the perspective of the three approaches. We discuss the limitations of such approaches in the scientific studies of these and other pathologies, and we close with a short reflection on the future of the field. In this regard we argue that, to the extent that TT, ST and IT offer explanations that capture different (limited) aspects of social cognition, a pluralist approach might be best.     

The Effect of Self-Efficacy on Visual Discrimination Sensitivity

Can subjective belief about one''s own perceptual competence change one''s perception? To address this question, we investigated the influence of self-efficacy on sensory discrimination in two low-level visual tasks: contrast and orientation discrimination. We utilised a pre-post manipulation approach whereby two experimental groups (high and low self-efficacy) and a control group made objective perceptual judgments on the contrast or the orientation of the visual stimuli. High and low self-efficacy were induced by the provision of fake social-comparative performance feedback and fictional research findings. Subsequently, the post-manipulation phase was performed to assess changes in visual discrimination thresholds as a function of the self-efficacy manipulations. The results showed that the high self-efficacy group demonstrated greater improvement in visual discrimination sensitivity compared to both the low self-efficacy and control groups. These findings suggest that subjective beliefs about one''s own perceptual competence can affect low-level visual processing.     

Hebbian learning and predictive mirror neurons for actions,sensations and emotions

Spike-timing-dependent plasticity is considered the neurophysiological basis of Hebbian learning and has been shown to be sensitive to both contingency and contiguity between pre- and postsynaptic activity. Here, we will examine how applying this Hebbian learning rule to a system of interconnected neurons in the presence of direct or indirect re-afference (e.g. seeing/hearing one''s own actions) predicts the emergence of mirror neurons with predictive properties. In this framework, we analyse how mirror neurons become a dynamic system that performs active inferences about the actions of others and allows joint actions despite sensorimotor delays. We explore how this system performs a projection of the self onto others, with egocentric biases to contribute to mind-reading. Finally, we argue that Hebbian learning predicts mirror-like neurons for sensations and emotions and review evidence for the presence of such vicarious activations outside the motor system.     

The Conforming Brain and Deontological Resolve

Our personal values are subject to forces of social influence. Deontological resolve captures how strongly one relies on absolute rules of right and wrong in the representation of one''s personal values and may predict willingness to modify one''s values in the presence of social influence. Using fMRI, we found that a neurobiological metric for deontological resolve based on relative activity in the ventrolateral prefrontal cortex (VLPFC) during the passive processing of sacred values predicted individual differences in conformity. Individuals with stronger deontological resolve, as measured by greater VLPFC activity, displayed lower levels of conformity. We also tested whether responsiveness to social reward, as measured by ventral striatal activity during social feedback, predicted variability in conformist behavior across individuals but found no significant relationship. From these results we conclude that unwillingness to conform to others'' values is associated with a strong neurobiological representation of social rules.     

Neural signatures for sustaining object representations attributed to others in preverbal human infants

A major feat of social beings is to encode what their conspecifics see, know or believe. While various non-human animals show precursors of these abilities, humans perform uniquely sophisticated inferences about other people''s mental states. However, it is still unclear how these possibly human-specific capacities develop and whether preverbal infants, similarly to adults, form representations of other agents'' mental states, specifically metarepresentations. We explored the neurocognitive bases of eight-month-olds'' ability to encode the world from another person''s perspective, using gamma-band electroencephalographic activity over the temporal lobes, an established neural signature for sustained object representation after occlusion. We observed such gamma-band activity when an object was occluded from the infants'' perspective, as well as when it was occluded only from the other person (study 1), and also when subsequently the object disappeared, but the person falsely believed the object to be present (study 2). These findings suggest that the cognitive systems involved in representing the world from infants'' own perspective are also recruited for encoding others'' beliefs. Such results point to an early-developing, powerful apparatus suitable to deal with multiple concurrent representations, and suggest that infants can have a metarepresentational understanding of other minds even before the onset of language.