Opinion

Interoceptive inference, emotion, and
the embodied self
Anil K. Seth
Sackler Centre for Consciousness Science and School of Engineering and Informatics, University of Sussex, Brighton, BN1 9QJ, UK

The concept of the brain as a prediction machine has Representations of physiological conditions have fre-
enjoyed a resurgence in the context of the Bayesian brain quently been associated with basic pre-reflective forms
and predictive coding approaches within cognitive sci- of selfhood [11], with the AIC occupying a central role on
ence. To date, this perspective has been applied primari- some views [13]. Selfhood is a constellation concept that
ly to exteroceptive perception (e.g., vision, audition), and involves not only representation and control of physiologi-
action. Here, I describe a predictive, inferential perspec- cal homeostasis, but also the experience of owning and
tive on interoception: ‘interoceptive inference’ conceives identifying with a particular body, the emergence of a first-
of subjective feeling states (emotions) as arising from person perspective, intention and agency, and metacogni-
actively-inferred generative (predictive) models of the tive aspects that relate to the subjective ‘I’ and the narra-
causes of interoceptive afferents. The model generalizes tive linking of episodic memories over time [17,18]. Here, I
‘appraisal’ theories that view emotions as emerging apply the framework of interoceptive inference to the
from cognitive evaluations of physiological changes, experience of body ownership (EBO) as a central aspect
and it sheds new light on the neurocognitive mecha- of selfhood, proposing on the basis of recent data [19,20]
nisms that underlie the experience of body ownership that EBO is shaped by predictive multisensory integration
and conscious selfhood in health and in neuropsychiatric
illness. Glossary
The predictive brain, body, and self Active inference: an extension of PC (and part of the free energy principle),
The view that prediction and error correction provide which says that agents can suppress prediction errors by performing actions to
bring about sensory states in line with predictions.
fundamental principles for understanding brain operation Augmented reality: a technique in which virtual images can be combined with
is gaining increasing traction within the cognitive and real-world real-time visual input to create hybrid perceptual scenes that are
brain sciences. In the renascent guise of ‘predictive coding’ usually presented to a subject via a head-mounted display.
Appraisal theories of emotion: a long-standing tradition, dating back to James
(PC – see Glossary) or ‘predictive processing’, perceptual (but not Lange), according to which emotions depend on cognitive interpreta-
content is seen as resulting from probabilistic, knowledge- tions of physiological changes.
Emotion: an affective state with psychological, experiential, behavioral, and
driven inference on the external causes of sensory signals
visceral components. Emotional awareness refers to conscious awareness of an
[1–4]. Here, this framework is applied to interoception, the emotional state.
sense of the internal physiological condition of the body [5], Experience of body ownership (EBO): the experience of certain parts of the
world as belonging to one’s body. EBO can be distinguished into that related to
in order to elaborate a model of emotion as ‘interoceptive body parts (e.g., a hand) and a global sense of identification with a whole body.
inference’ [6–9]. Interoceptive predictive coding – equiva- Free energy principle: a generalization of PC according to which organisms
lently here, interoceptive inference – is hypothesised to minimize an upper bound on the entropy of sensory signals (the free energy).
Under specific assumptions, free energy translates to prediction error.
engage an extended autonomic neural substrate with em- Generative model: a probabilistic model that links (hidden) causes and data,
phasis on the anterior insular cortex (AIC) as a compara- usually specified in terms of likelihoods (of observing some data given their
tor. This view extends alternative frameworks for causes) and priors (on these causes). Generative models can be used to
generate inputs in the absence of external stimulation.
understanding emotion [10–14] by proposing that emotion- Interoception: the sense of the internal physiological condition of the body.
al content is generated by active ‘top-down’ inference of the Interoceptive sensitivity: a characterological trait that reflects individual sensi-
causes of interoceptive signals in a predictive coding con- tivity to interoceptive signals, usually operationalized via heartbeat detection
tasks.
text. It also extends previous models of insular cortex as Predictive coding (PC): a data processing strategy whereby signals are repre-
supporting error-based learning of feeling states and un- sented by generative models. PC is typically implemented by functional archi-
certainty [15] and as responding to interoceptive mis- tectures in which top-down signals convey predictions and bottom-up signals
convey prediction errors.
matches that underlie anxiety [16]. Rubber hand illusion (RHI): a classic experiment in which the experience of
body ownership is manipulated via perceptual correlations such that a fake
(i.e., rubber) hand is experienced as part of a subject’s body.
Corresponding author: Seth, A.K. (a.k.seth@sussex.ac.uk).
Selfhood: the experience of being a distinct, holistic entity, capable of global
Keywords: interoception; predictive coding; emotion; experience of body ownership;
self-control and attention, possessing a body and a location in space and time
rubber hand illusion; active inference.
[64]. Selfhood operates on multiple levels – from basic physiological represen-
1364-6613/$ – see front matter tations to metacognitive and narrative aspects.
ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tics.2013.09.007 Subjective feeling states: consciously experienced emotional states that under-
lie emotional awareness.
Von Economo neurons (VENs): long-range projection neurons found selectively
in hominid primates and certain other species. VENs are found preferentially in
the AIC and ACC.

Trends in Cognitive Sciences, November 2013, Vol. 17, No. 11 565

means models to accommodate unexpected sensory signals or by perform- inducing a predictive or ‘generative’ model of the sensory data. circles represent inhibitory interneurons. and carries implications for under. PC interprets bottom-up signals brain must discover information about the likely causes of sensory as conveying prediction errors and top-down signals as conveying signals (i. the causes of sensory signals. Functional architecture of predictive coding. 566 . free energy. the brain is tive domains. Applied to cortical networks. Opinion Trends in Cognitive Sciences November 2013. associated with precisions (Figure 1). According to PC. action. the model described here provides a unified ‘prediction error’ between its inputs and its emerging view of self-related processing relevant to emotional models of the causes of these inputs via neural computa- awareness and EBO. high precision-weighting of sensory signals (red) enhances their influence on the posterior (green) and expectation (dotted line) as compared to the prior (blue). in order to support adaptive responses.g. in turn. No.e. (B) The influence of precisions on Bayesian inference and predictive coding. This can be accomplished either by updating generative and prior ‘beliefs’ about probable causes. This means estimating the probable causes of data (the Key to PC is the minimization of prediction error across hierarchical posterior) given observed conditional probabilities (likelihoods) levels. 11 (A) Predicon error R1 R2 R3 Precision weighng g (B) Predicon TRENDS in Cognitive Sciences Figure 1. 17. PC. Importantly. this is accomplished via probabilistic inference on content – and underlying neural responses – can be shaped by pre- the causes of sensory signals. Although unequivocal neural evidence for PC is only information in the flux of sensory signals themselves [2]. thus and reaching recent prominence in the ‘Bayesian brain’ hypothesis enabling priors to be induced from the data stream itself (‘empirical’ [1. The proposing that affective states depend on active inference of generalization of Bayes theorem to a hierarchical context implies that interoceptive responses. Adapted from [6].. Bottom-up projections (red) originate from ‘error units’ (light orange) in superficial cortical layers and terminate on ‘state units’ (light blue) in the deep (infragranular) layers of their targets. of self-related signals across interoceptive and exterocep. (Gaussian) assumptions is equivalent to prediction error). emerge from hierarchically organized generative models of underlining a deep continuity between perception and Box 1. The present framework generalizes PC to interoception. a growing body of supportive data details how perceptual According to PC.4]. low precision-weighting of sensory signals has the opposite effect on posteriors and expectations. computed according to Bayesian stimulus expectations [1. shows how generative models can be between top-down and bottom-up signal flow (e. This Although exact Bayesian inference is computationally challenging duality underlines a strong continuity between perception. these approximations have been elaborated in Fris. Prediction errors are associated with precisions (inverse variances). Within and imagination [68]. and active inference PC has a long history. low precision on induced from data by assuming that the brain minimizes a bound on error signals corresponds to high confidence in top-down prior the evidence for this data (the ‘free energy’. In most incarnations these processes are content is specified by top-down predictive signals that assumed to unfold continuously and simultaneously. the ‘lowest’ on the left (R1) and the ‘highest’ on the right (R3). Vol. Box 1). the Bayes). which under simplifying beliefs).42]. changing the world to or feature detection. Top-down precision weighting (dashed lines) regulates the post-synaptic gain of prediction-error projection neurons possibly by neuromodulation.. which determine the relative influence of bottom-up and top-down signal flow. so that dynamic precision- ton’s ‘free energy principle’ [2. a variety of approximate methods exist. [21]). Solid black lines depict local circuit interactions wherein descending predictions are resolved with ascending prediction errors. using predictions (Figure 1). continuously attempting to minimize the discrepancy or Overall. originating with the insights of von Helmholtz posteriors at one level form the priors at one level lower. The idea is that. On the right. tions approximating Bayesian inference (Figure 1 and standing specific neuropsychiatric disorders. perception) without direct access to these causes.4. principles. Triangles represent pyramidal (projection) neurons. which. still lacking. changing the model to fit the world) or The concept of PC overturns classical notions of perception by performing actions to bring about sensory states in line as a largely ‘bottom-up’ process of evidence accumulation with predictions (active inference.65]. On the left. following seminal work by weighting (for example by attention) can modulate the balance Hinton and colleagues [66. and often intractable. The curves represent probability distributions over the value of a sensory signal (x-axis).67]. whereas top-down projections (dark blue) that convey predictions originate in deep layers and project to superficial layers of their targets. ing actions to confirm sensory predictions (active inference. This. Also important is that prediction errors are neuroscience. prediction errors can be minimized either by updating generative models (perceptual infer- Predictive inference and perception ence and learning. proposing instead that perceptual fit the model). (A) A schematic of hierarchical predictive coding across three cortical regions.

to decreased attention to these error signals. can be productively understood through the lens of PC. that is. Evidence for interoceptive inference mally causing a state of physiological arousal. More tions against bottom-up prediction errors and as a source of than a century after James and Lange. AIC. For example.16]. Schachter and Singer [24] fa- mously demonstrated that injections of adrenaline. Similarly. see [1]). there is now a anticipatory visceromotor control [6–9. proprioceptive and exteroceptive cues in formulating des- Interoceptive inference and emotion cending predictions. a framework that views emotion as selective attenuation of attention to interoceptive predic- ‘interoceptive inference’ and provides a unifying mecha. as recently suggested by Gu and colleagues [9]. operating within a rich functional network cal change and cognitive appraisal. the AIC is ideally placed both to detect and to cause encompass behavioural. balancing the relative influence of prediction can be suppressed both by modifying predictions and by errors and prior expectations on perceptual inference [2]. that is. this implies signals have diminished impact on hierarchical processing that an organism should maintain well-adapted predictive via transiently low precision weighting. and emo- generally understood along feed-forward lines. from perceptions of changes in the body. classical evidence accumulation theories of exteroception Several functional MRI (fMRI) studies have shown [23. interoception has remained involve visceral representation. cortex (AIC). one of the most relevant role for active inference. who argued that emotions arise may include socially salient signals. 11 action. This reflects a long-standing notion for motor control (e. nism for self-representation at multiple levels. discussed further below.g. with the internal dictions that engage classical motor reflexes. see later). conscious awareness and is associated with processes that Despite the above insights. No. with higher levels integrating interoceptive. This observation was supportive data are steadily accumulating. precise prediction errors would lead inducing generative models of the causes of those signals to revision of predictions rather than to action [29]. functionally. In short. [29]) which highlight descending that mental representations of selfhood are ultimately corticospinal signals as instantiating proprioceptive pre- grounded in representations of the body. These multimodal predictions under- Interoceptive concepts of emotion were crystallized by write emotional responses to exteroceptive cues (which James and Lange [10]. For example.) and of its internal physiological condition. interpretation of attention as the optimization of precision Following PC principles. which extends previous presenta- features of the world for a particular organism is the tions of this model [6–8]. to predictive modelling of external sis. would give Although there is not yet any direct confirmatory evidence rise to either anger or elation depending on the context for interoceptive inference (as for PC generally. emotion as [30]. Precisions physiological milieu providing a primary reference – a play a key role here: descending predictions can engage ‘material me’ [13] – that supports adaptive interaction motor or autonomic reflexes only if the corresponding error with the environment. interoceptive inference involves hierarchically cal processing. the AIC has been shown to encode both predicted risk 567 . both as a comparator that registers top-down predic- interpreted bodily arousal (see [25] for a precursor). This attitude underpins several contemporary oceptive and exteroceptive signals. I suggest that error within a single task [33]. This ‘most likely to be me’ [22] across interoceptive and extero. Informed by this emerging picture. similar to tional awareness relevant to selfhood (Box 2). Sub- of prediction error units) can modulate the extent to jective feeling states – experienced emotions – are which prediction errors are resolved by updating genera. in which emotional data rest on assuming a central role for the anterior insular experience is determined by the combination of physiologi. This states of the world. However. interoceptive prediction errors weighting. emotional behaviour [23]. This leads to an predictive representations across multiple levels [6]. and to integrate inter- [23. precision weighting cascading top-down interoceptive predictions that counter- (possibly implemented by post-synaptic gain modulation flow with bottom-up interoceptive prediction errors. morphology. (an irritated or elated confederate). in a gambling the role of interoception in shaping emotion and selfhood task. This approach interoceptive predictive coding (inference) proposes that evolved into ‘appraisal’ theories. tion errors. hypothesized to depend on the integrated content of these tive models or by performing actions [21]. and AIC behavioural influences to brainstem and spinal centres responses encode both predicted pain and pain prediction [26]. which corresponds models of its own physical body (its position.22]. likely internal and external causes of changes in the phys- logical changes influence subjective feeling states and iological condition of the body (Figure 2). directly parallels PC formulations organism itself [11. From a PC perspective.Opinion Trends in Cognitive Sciences November 2013. proxi. 17. Structural- consensus that emotions are psychological states that ly.26–28]. anticipatory and prediction error responses within the dence of substantial cross-talk between levels of viscero. implies that active interoceptive inference depends on the ceptive domains. including Interoceptive predictions arise from multiple hierarchi- perhaps especially those related to EBO. Without this etc. This entails transient modulation. experiential.28]. transcribing these predictions into reference points for PC has been elaborated principally in the context of autonomic reflexes that regulate physiological homeosta- exteroception. Much of these formalized in their ‘two factor’ theory. Prediction errors are associated with ‘precisions’. the AIC is activated by anticipation sensory representation. Vol. and visceral changes changes in physiological condition. which recognise that emotional content is determined by active inference on the explicit cognitions and beliefs about the causes of physio. In which determine their influence on subsequent hierarchi. This assumption is however challenged by evi. it frameworks for understanding emotion and its relation to instantiates interoceptive representations accessible to cognition and self [11–13]. interoception.15. cal levels. including top-down cortical and of painful [31] and affect-laden touch [32]. this view.

and exteroceptive signals [6. which have been associated frequently though circum. tive models of social interaction [38. the AIC contains a high density of von Economo neurons together with evidence for prediction error processing. detection. hanced AIC activity during false feedback correlated with ing prediction errors (when measured using variance) increased emotional salience attributed to previously un- scaled parametrically with AIC activation [37].9. individual areas together engage subcortical regions.70]. enjoying widespread bidirectional connectivity to of interoceptive prediction and prediction error signals. Taken together with iour. smooth muscle behaviour). though they can be contexts relate to the biological self [15. This was later confirmed by Gray and roeconomic ‘ultimatum game’. suggest the AIC as a locus for comparator mechanisms that underlie stantially with conscious awareness and selfhood [8.9. when considered ingly.75].39]. such as the periaque. A posterior-to-anterior gradient of VENs in the AIC [8.13. heart/respiratory rate. AIC responses plau. Further evidence showing the studies support the idea that interoceptive inference influence of false interoceptive feedback on the experience extends into social contexts to explain emotional behav. Interest. Box 2. prediction errors (PEs) are transcribed into actions via engagement of classical reflex arcs (motor control) and autonomic reflexes (autonomic control). amygdala. generative models are engaged which predict interoceptive (and exteroceptive) signals via corollary discharge. who found that false cardiac feedback led to showed that subjects used Bayesian rules to update increased fMRI responses in the right AIC and that en- expected feelings given economic outcomes. and that feel. nucleus accumbens. Starting with a desired or inferred physiological state (which is itself subject to update based on higher-level motivational and goal-directed factors). including the ibility to illusions of selfhood (see main text). which suggests manipulate interoceptive feedback. the expression of an emotional state the structural and functional attributes of the AIC (Box 2). Supportive evidence is also provided by studies that oceptive responses given anticipated itch. appears to support conscious access to both interoceptive informa- tional.12. (At high hierarchical levels these generative models merge into a single multimodal model.26].73]. These threatening stimuli [41]. has been proposed. and are omotor control and relays for viscerosensory afferents. differences in interoceptive sensitivity (IS). ACC) that engage brainstem regions as targets for visceromotor control and relays of afferent interoceptive signals. Holle et al. the activation on viewing movies of people scratching. Here. Vol. This provides a nice link to predic- level of reported itchiness [35]. in turn supporting emotional awareness and are large projection neurons well suited for rapid long-range consciously accessible integrated self-representations. Using the neu. 568 . compared. frontal. emotive stimuli [40]. Importantly. This process depends on the transient attenuation of the precision of interoceptive (and proprioceptive) PE signals. Sympathetic and parasympathetic outflow from the AIC and ACC are in the form of interoceptive predictions that enslave autonomic reflexes (e.. No. Blue (red) arrows signify top-down (bottom-up) connections respectively. just as proprioceptive predictions enslave classical motor reflexes in PC formulations of motor control [9]. top- parietal. For example. In PC. and orbitofrontal cortex. In the model. consistent with the layer V predominance contains a viscerotopic map [69]. are predicted by AIC activation and morphometry. which pyramidal cells (Figure 1). strongly (VENs) [72].) Interoceptive predictions are proposed to be generated. These rise to dissociable emotional feeling states [76]. motiva. Interoceptive pathways down predictions are suggested to originate in infragranular have their primary cortical representation within the insula..13. Early evidence showed an engagement of AIC in predictive inference related to that false cardiac feedback enhanced subjective ratings of mirror-system activity and empathy [36]. 17.g. interoception. Opinion Trends in Cognitive Sciences November 2013. Distinct axes of functionally differentiated [70]. as targets for viscer. as measured by heartbeat ductal gray matter and parabrachial nucleus.73]. whereby posterior regions support primary The AIC is engaged in a wide range of processes that share as (objective) mappings of interoceptive signals. 11 World Generave Motor Extero PE model control Desired / inferred state Generave Autonomic Intero PE Salience model control network Body Corollary discharge TRENDS in Cognitive Sciences Figure 2. The resulting prediction error signals are used to update the (functionally coupled) generative models and the inferred/desired state of the organism. A model of interoceptive inference. emotional responses depend on continually-updated predictions of the causes of interoceptive input.74]) – structurally and functionally with the anterior cingulate cortex (ACC) and to associated representations of how encoded objects and as part of a cortical ‘salience network’ [71]. and risk prediction error [34]. anger) elicits behavioural responses from others. the AIC (particularly on the right) subjective access [9. Applying active inference.70]. as well as also associated with reported emotional symptoms [12] and suscept- many other areas related to self and emotion. Also. sibly reflect a conflict between predicted and actual inter. with detection of which could serve to confirm predictions of the degree of activation correlating with the subjective interoceptive condition. of body ownership is described below. The AIC is closely connected tion – as reflected in subjective emotional states (though see [43. and emotional insula (AIC) supports secondary re-representations that underlie awareness [6. and updated within a salience network (orange shading) anchored on the anterior insular and anterior cingulate cortices (AIC. Xiang and colleagues colleagues.13] and integration of interoceptive. found AIC (e. VENs interoceptive inference. and limbic regions [30]. The anterior insula cortex and interoception The human insular cortex is found bilaterally beneath the temporal information integration and so may underlie the efficient registration and frontal lobes. whereas the anterior common factors visceral representation. so that the AIC can be considered a interoceptive information map onto specific insula sub-regions giving ‘limbic sensory area’ and the ACC a ‘limbic motor area’ [13. These structural and functional attributes.g.

One avenue is provided by indi- based learning of feeling states and uncertainty [15]. This is compatible with chronous tactile-visual feedback. such as selfhood and (interoceptive) prediction errors. 11 these data provide indirect support for interoceptive infer. multisensory stimulation [56. Also relevant are models of [54]. the relative weighting of differ- The present model is related to several contemporary ent information sources according to their reliability in this frameworks for understanding emotion and self. Vol. ian scheme [51]. sup. individual’s heartbeat (Figure 3).) The same setup enabled a replication of statistical correlations among sensory signals together the standard RHI by contrasting synchronous versus asyn- with visual dominance [46. although these models integrate abun. temperature [58] and increased histamine reactivity of the real hand [59]. as argued here (and as Interestingly. toring to implement a version of the RHI in which a virtual chronously with a participant’s real hand. cues for EBO that overshadowed the influence of cardiac ing high-level representations. oception underlying emotion and self. are likely to operate at relatively ence and the central involvement of the AIC in prediction abstract multisensory or amodal levels. statistical correlations among highly precision-weighted ditional experiments.57]. A second study [20] 569 . the core notion of In addition. tual correlations are not necessary for the RHI. vidual differences in ‘interoceptive sensitivity’ (IS). Experi. 17.49]. (Note that these two measures do not always events occurring in peri-personal space.50]. overall level of self-related precision-weighted prediction error by incorporating the fake hand as part of the self- Relation to other models of emotion and insula function representation. they emphasize a rity and activity of the AIC on the basis of lesion data and continuous. on the basis of correlate [62]. Par. threats to ownership the rubber hand during the RHI evoke enhanced skin A predictive model of selfhood must extend beyond subjec. with the AIC further supported by recent evidence showing that percep- emphasised in some [12. induction of the RHI leads to decreased interoceptive inference is not elaborated. er precision-weighting of interoceptive prediction errors. No. Perhaps more closely interoceptive processing on the modulation of EBO in related is the suggestion that the AIC is involved in error. In a third condition. Two recent studies have addressed directly the role of porting EBO [45]. The engagement of predictive self-models is sentations of physiological condition. Also.Opinion Trends in Cognitive Sciences November 2013. Moreover. the world perceived as belonging to one’s own body. Crucially. tive signals. Tsakiris and colleagues reported that participants insular dysfunction during anxiety [16] and psychosis [44] with lower IS are more susceptible to the RHI [55] and to that hypothesize the existence of interoceptive prediction the modulation of self–other boundaries in response to errors. are needed to test more errors in a different modality (proprioception). ments such as the ‘rubber hand illusion’ (RHI) attest to [19] combined augmented reality with physiological moni- the plasticity of EBO: stroking of an artificial hand syn. Ad. conductance responses [61]. ceptive domains in shaping EBO. Similar effects have been described for face ence of ownership of the virtual hand. However. operationalized by heartbeat detection tasks anisms of predictive coding. and Critch. The authors found that ticipant to experience the artificial hand as part of her own synchronous cardio-visual feedback enhanced the experi- body [46]. [42]). leads the par. Thus. Rather. EBO has also been associated with the integ- recently taken up by others [9]). while visual hand changed colour either in-time or out-of-time with an attention is focused on the artificial hand. Craig [13]. points for autonomic reflexes from the perspective of ticularly significant is the representation of those parts of active inference. PC inasmuch as minimization of prediction errors – such Suzuki et al. which the notion of ‘prediction error’ is expressed in terms of refers to a person’s ability to detect their own interocep- change detection and salience rather than through mech. leading to a directly interoceptive inference and the proposed role of revised multisensory predictive model that minimizes the the AIC. over time. whereas cooling the real hand The predictive self and the experience of body increases susceptibility to the RHI [60]. but largely bottom-up interoceptive functional neuroimaging in healthy subjects [53]. These effects are compatible tive feelings to integrate interoceptive and exteroceptive with descending self-related predictions tuning reference signals across multiple levels of self-representation. touch) could overcome prediction exteroceptive contexts (e. dynamic. representational hierarchy that interacts with other Experiments have begun to address the impact of perceptions to motivate behaviour. and which plausibly are closely tied to multisensory integration across interoceptive and extero- interoception in having the body as a referent.13]. possibly reflecting low- dant evidence compatible with a role for predictive inter. body-ownership. the expec- none identify emotional states with top-down inference of tation of correlated sensory input is sufficient [52].g. Priors reflect. but not all [43]. touch. and proprioception are hand by asking the participant to move a cursor to this minimized by visual capture of visual and felt (tactile) location. tations which underlie optimal cue combination in a Bayes- ley [12]. the causes of interoceptive signals. as measured both perception [47] and whole-body ownership [48. visual-proprioceptive coherence – provided strong can induce changes in self-related priors [22]. paradigms like the RHI. including process is suggestive of the deployment of precision expec- prominently those of Damasio [11].. here. subjectively by questionnaire and objectively by previously These manipulations of EBO have been explained by validated measures of ‘proprioceptive drift’ – where the models of multisensory integration. Each of these sees selfhood as grounded in repre. found that real-time remapping of finger as those induced by multisensory conflicts during the movements to the virtual hand – supporting peri-hand RHI – will update the posterior probabilities and. In the first. which propose that latter measures the perceived position of the real (hidden) conflicts between vision. Suzuki et al. perhaps based on designs utilized in sensory signals (vision. error registration underlying subjective feeling states.

Concluding remarks chrony increased identification with the virtual body.s. physical bodily just as may happen for purely exteroceptive multisensory integrity. Subjects wore a front-facing camera connected to the HMD. A 3D model of the real hand was captured by Microsoft Kinect and used to generate a real-time virtual hand that was projected into the head-mounted display (HMD) at the location of the augmented-reality (AR) marker. during which either cardio-visual or tactile-visual feedback was provided (120 s). Tactile feedback (middle) was given by a paintbrush. and – more specula- conflicts in the classic RHI. Adapted from [19]. visual) tive domains. n.59] when these changes are taken to reflect altered seen from behind. (B) Cardio-visual feedback (left) was implemented by changing the colour of the virtual hand from its natural colour towards red and back. (E) Subjective questionnaire responses that probed experience of ownership showed the same pattern as PDDs.s. (C) The experiment consisted of three blocks of four trials each.s. Opinion Trends in Cognitive Sciences November 2013. Consistent with Suzuki et al. self-related predictive coding signals can lead to updating of predictive models of self.g. No. they found that cardio-visual syn. Each bar shows the across-participant average and standard error. autonomic control. cardiac) and exteroceptive (e.001 *P < 0. tion. 17.g. Each trial ended with a questionnaire presented in the HMD. back on the ‘full body illusion’ [48.. (A) Participants sat facing a desk so that their physical (left) hand was out of sight.’s results.49]. morphology and position. extending previous theories based [21]. so they saw the camera image superimposed with the virtual hand. again This opinion article proposes that emotion and embodied when measured both objectively and subjectively. In humans. applied similar cardio-visual feedback to a virtual body as [58. replicating the classical RHI. objectively measured perceived virtual hand position by implementing a virtual measure and cursor. ** display and camera 6 Sync Async 5 * 4 3 Physical Virtual 2 hand hand 1 (B) 0 Cardiac sll Cardiac move Tacle (E) *** P < 0. including physiological homeostasis. simultaneously engages multiple levels of self-representa- related signals through minimization of prediction error.01 Kinect camera *P < 0.05 7 AR marker Head mounted Key: Propriocepve dri difference [cm] n. (D) PD differences (PDD. the framework naturally accommodates the phasic on cognitive appraisal of perceived physiological changes physiological changes that accompany RHI induction [24] and contemporary frameworks that emphasize 570 . Each trial consisted of two PD tests flanking an induction period.. Vol. whereas control questions showed no effect of cardio-visual or tactile-visual synchrony. Subjective continually probed by control signals that attempt to con. 11 (A) (D) **P < 0. thus testing the influence of such feed.05 3 Ownership Control Visuo-cardiac feedback Visuo-tacle feedback Propriocepve dri test 2 on the virtual hand by a paint brush * n. feeling states (emotional experiences) arise from active firm the currently dominant model via active inference interoceptive inference. which was rendered into the AR environment. *** Subjecve rang 1 (C) Propriocepve Quesonnaire Inducon dri test (POST) 0 Propriocepve opriocepve period dri i test (PRE) −1 Resng −2 Key: 6 items Sync period x2 n. selfhood are grounded in active inference of those signals These data suggest that statistical correlations between most likely to be ‘me’ across interoceptive and exterocep- interoceptive (e. An interoceptive rubber-hand illusion.s. Also. n. They also wore a pulse-oximeter to measure heartbeat timings and they used their right hand to make behavioural responses. A ‘proprioceptive drift’ (PD) test (right). PDDs were also significantly larger for synchronous versus asynchronous tactile-visual feedback (‘tactile’ condition). over 500 ms either synchronously or asynchronously with the heartbeat. post- induction minus pre-induction) were significantly larger for synchronous versus asynchronous cardio-visual feedback in the ‘cardiac still’ (without finger movements). Async 120s −3 x2 Sll Move Tacle Sll Move Tacle 20s TRENDS in Cognitive Sciences Figure 3.s. adapted for the AR environment. if predictive models are tively – the metacognitive and narrative ‘I’. but not the ‘cardiac move’ condition (with finger movements).

g.15]. 395 571 . a key aspect and perception. This view has been finessed in terms of Dissociative conditions. A predictive self is further supported by stimuli with respect to cardiac phase under restricted emerging paradigms that combine virtual/augmented re.S.16.80]. Image Sci. and Mumford. A. emphasizes their integration in shaping self-related experience. deficits in emotional awareness) is psychosis [79. including anxiety [12. No. which supports the work of the Sackler modulating the precision of interoceptive prediction errors [89]? Centre for Consciousness Science.16]. Keisuke Suzuki (who also helped prepare Figure 3). Paul [2]? Verschure.44]. A: Opt. 36. D. A. 1434–1448  Can interoceptive feedback provide new avenues for the treat. and influences on cognition and perception. Neurosci. self.13. J. basis further enhances the explanatory potential of this framework for suggestive of deficient interoceptive inference and consistent with psychopathology. (2003) Hierarchical Bayesian inference in modes of self-experience. alexithymia (broadly. two decades. (2013) The Predictive Mind. gration of precision-weighted interoceptive and exterocep- play between interoceptive and exteroceptive inference tive signals. oceptive) prediction errors [78]. K. members of the Sackler Centre. Human VENs express proteins linked to schizophrenia full-blown delusion (e.80]. as informing visceromotor control. disrupted interoceptive inference. Psychol. Vis.Opinion Trends in Cognitive Sciences November 2013. In psychosis. 17. attention [63].J. Soc. where the data so far common predictive mechanisms that underlie affect. as reflected in evidence to account for a broad range of psychotic symptoms [79. Although the detailed neuroanatomy ence could underlie a range of pathologies. Interoceptive inference and psychopathology A significant body of work now connects deficits in predictive inference volume with individual interoceptive sensitivity (IS). Indeed. et al. (2002) How do you feel? Interoception: the sense of the be a role for disrupted interoceptive inference in impairments of physiological condition of the body. I am grateful to Sarah Garfinkel. perceptual systems [88]. such as depersonalization and derealisa- abnormal encoding of the relative precision of priors and sensory tion (DPD). A. have suggested that DPD may arise from associated with failure to engage AIC [81] and with degeneration of imprecise (as opposed to inaccurate) interoceptive predictions. 293–301  Can predictive models of selfhood accommodate more abstract 3 Lee. recognition memory is modulated by the timing of visual tional awareness).. 11 Box 3. For predicts sensitivity to mood states. a persistent sense of unreality (‘as-if-ness’) [85]. word as underpinning conscious access to emotional states (emo. such as autism? 6 Seth. Links between perceptions of bodily state and observed hypoactivation of AIC (and ACC bilaterally) in DPD patients emotional and neuropsychiatric disorders are well established.K.83]. 20. (2013) Whatever next? Predictive brains.  What are the functional and effective connectivity patterns that underlie interoceptive inference and the integration of interocep- tive and exteroceptive signals relevant to conscious selfhood? References  What is the relation between predictive models of interoception 1 Clark. especially those that underlies interoceptive inference remains to be eluci. Rev. Vol. Dysfunctions in interoceptive infer- affectively coloured. (2011) An interoceptive predictive coding model of conscious presence. involve disabling disturbances of selfhood. Seth et al. 4 Hohwy. Questions for future research possibilities for elucidating the underlying processes (Box 4).  Can (structurally or functionally) segregated populations of representation and error units be identified in the interoceptive Acknowledgements system? There are some early indications of such segregation in This work was supported by ERC FP7 project CEEDS (FP7-ICT-258749). The finding that low IS in sensory input [77]. EPSRC Fellowship EP/G007543/1. ‘interoceptive inference’ highlights ality and physiological monitoring. Special gratitude is predictions from insular and cingulate cortices to subcortical and due to Hugo Critchley and Manos Tsakiris for their generous insights brainstem targets [8]? which helped shape the ideas presented here. Brain Sci. which in turn with psychiatric disorders that affect self-representation [6. accumulating evidence implicates the AIC as a key (Box 3).44]. ‘comparator’ models of schizophrenia have suggested anxiety and psychosis have been specifically associated with that disturbances of selfhood (e.. consistent with recent evidence that shows interoceptive tion error signals. and provides new experimental Box 4. as AIC and of VENs (Box 2) in the context of fronto-temporal dementia part of a model of conscious ‘presence’ [6]. Front. 181–204 2 Friston.D. Opt. These conditions are Considering interoceptive inference and the AIC as its likely brain associated with alexithymia and a general loss of ‘emotional colour’. Jakob How do these roles relate to similar roles in reward processing Hohwy. Oxford University Press ment of emotional and neuropsychiatric disorders? Might there 5 Craig. implies that emotional responses are inevitably shaped This framework may have important implications for by cognitive and exteroceptive context. (2009) The free-energy principle: a rough guide to the selfhood? brain? Trends Cogn.g. A broad role for interoceptive inference is also comparator mechanism sensitive to interoceptive predic. and and similar models of agency [90]. Overall. By analogy with models of example. such as the narrative self or ‘I’ that links episodic memories across time? the visual cortex. in which patients (notably DISC-1) and VEN density (in the anterior cingulate) has been believe they are dead [87]) may also reflect aberrant high-level linked to illness duration and completed suicide in psychotic patients inference as the result of attempting to explain away persistent [84]. and by the Dr Mortimer and Dame  Do neurotransmitters like dopamine and oxytocin have a role in Theresa Sackler Foundation. For when viewing aversive images [86]. Cotard’s syndrome. delusions of control) reflect mismatches between predicted and actual interoceptive states problems in distinguishing self-caused from externally-caused changes putatively computed within AIC [16. another central aspect of the future of cognitive science. The transition from DPD to [82. bottom-up elaboration of interoceptive representations of selfhood. 3. such as anxiety dated. 655–666 social emotional behaviour. J. The close inter. Am. Behav. T. suggest that the experience of body ownership. Nat. false perceptions (hallucinations) predicts susceptibility to the RHI [55] provides a bridge to under- and false beliefs (delusions) may arise from reshaping of top-down standing how disorders of body image and ownership may involve predictions in attempts to suppress aberrant and persistent (exter. Neuroimaging studies have correlated (right) AIC activity and interoceptive prediction errors. 13. Sci. 2. that involve dissociative symptoms. situated agents. is modulated by predictive multisensory inte- with perception and motivation [11. For example. and my reviewers for  Are VENs engaged in communicating top-down interoceptive comments which helped improve the manuscript. and that perceptual understanding psychiatric disturbances of selfhood and scenes that evoke interoceptive predictions will always be emotional awareness.

M. H. Curr. (2012) Dreaming the whole cat: generative models. Trends Cogn. and Hunt.1016/j.O. Sci. G.L. 521. 360.B. 1499–1506 31 Ploghaus. S. (1999) Dissociating pain from its anticipation in the 62 Rohde. and Schwartz. M. et al. Neurosci. Biobehav. (2013) The body beyond the body: expectation of a illusion. (2011) Feeling numb: temperature. 69. formulation. G. A. (2008) On the other hand: dummy hands and 18 Northoff. Lond. Neuroimage 45.B.B. sensory representation in the cortex and thalamus in the rat. (2013) The free-energy self: a predictive 55 Tsakiris. 815–836 19816–19821 66 Dayan.A. 556–571 13 Craig. (2004) Temporal difference models describe higher. 383–387 experiences. (1894) The physical basis of emotion. and Stein. U. Acad. 358. Natl. Comp. P. 21. P. et al. (2007) Video ergo sum: manipulating bodily uncertainty. J. X. Soc. Trans. and Ramachandran. O. 833–846 516–529 44 Palaniyappan. Comp. et al. P. and behavior. Cogn. W. (2013) Computational substrates of norms and their Neural Netw. 278. et al. M. (2012) Neural basis of contagious itch and why 65 Friston. dx. Sci. e546 the neural mechanisms of self-awareness? Neuron 74. (2009) Anterior insular cortex anticipates impending ONE 6. some people are more prone to it. Neurosci.08. 4. et al. et al. Neuropsychologia http://dx. N. 624–638 body part caused by the illusory ownership of an artificial counterpart.P. et al. 10. (2004) Empathy for pain involves the affective but not 889–904 sensory components of pain. cognition.2013. 49 Ehrsson. 59–70 see.A. and Metzinger. (2011) The rubber hand illusion increases histamine Am. J. T. Psychol. Emot. M. Rev. Biol. 13. and Liddle. 143–152 influences sense of identity. 63. (2007) The experimental induction of out-of-body Psychiatry 60. Soc. (1995) The Helmholtz machine. Sci. 36 Singer. and Baier. R. predictive 38 Frith. (2012) Will studies of macaque insula reveal physiological feedback during fMRI. Neuropsychologia 49. et al. et al. J.doi. Sci. 1385–1403 violations during social exchange. Science 284. Behav. (2010) Right insula for our sense of limb heartbeats alter bodily self-consciousness and tactile perception.F. 28.S. 227–260 Psychophysiology 18. et al.01. U. and Dayan. Rev. B.E. D. 1. et al. 100176 12 Critchley. (2005) A theory of cortical responses. Funct. F. Nat. 753–771 39 Wolpert. et al. 593–602 J. 148–162 15 Singer. (2013) Persistence of feelings and sentience after 10 James. K. and Bermpohl. and Barrett. H. (2004) Cortical midline structures and peripersonal space. Psychol. 3371–3388 43 Damasio. et al. Neurosci. et al. D. Sci.J. et al. and Harrison. et al.D.C. (2006) An insular view of anxiety. 423–426 42 Egner. 1004–1006 J. R. (2010) My face in yours: visuo-tactile facial stimulation evolutionary and neurobiological origins. R945–R946 28 Dolan. M. Biol. et al. A. B. and Singer. 13169–13173 cognitive-developmental theory and its application to psychopathology.org/10. M. M. K. Sci. Neurol. C. (2003) Projecting sensations to 30 Deen. (2003) A unifying computational framework for 69 Cechetto. 2745–2752 phenomenal selfhood. and Saper. 300–307 Boundaries. Neurosci. 1157–1162 67 Hinton. Sci. 11. Biol. O.A.L. Brain Struct.J. 429–433 exteroceptive domains modulates self-experience in the rubber-hand 52 Ferri.neuropsychologia. K. perceptual expectations. (2013) Anterior insular cortex and emotional awareness. 14. Nature 391. 133–143 reactivity in the real arm. Rev.A. (2009) reconstructing the past: a century 56 Tajadura-Jimenez. 60 Kammers. (2008) Human insula activation reflects risk 64 Blanke.H. and physiological identification.A. (1987) Evidence for a viscerotopic motor control and social interaction. et al. Proc. 102. and Seth. et al.D. (2013) Balancing the ‘Inner’ and 25 Cantril. 1. et al. (2013) The nature of feelings: 47 Sforza. Neurosci. K. U. Rev. (2009) Full-body illusions and minimal prediction errors as well as risk. (1966) Cognitive effects of false heart-rate feedback. J. (2013) Extending predictive processing 40 Valins. 2013. 36. Psychol. Cereb. H. modulates feeling of body ownership.E. G. (2007) Modulation of emotional appraisal by false 8 Critchley. Psychiatry 144. 1096–1099 16 Paulus. Acad. 20131140 20 Aspell. (2008) Neural repetition suppression reflects fulfilled 9 Gu. empathy and 48 Lenggenhager. M. Behav. Brain Struct. R.K.org/10. 37 Xiang. A. Nat. 1–10 the self. 27–45 572 . processing. H. bilateral damage of the insula. (1981) Heart beat perception and emotional experience. H. (1962) Cognitive. Exp. 5. and Critchley. Brain Sci. et al. R. 27 Lane. et al. Rev. Psychol. http://dx.014 R.1016/j. M. http:// interoceptive sensitivity predicts malleability of body-representations. Nat. et al. Nat. 109. 1498–1506 Soc. Neurosci. Funct. R. and the enactivist conception of perceptual experience. et al. (2013) Visceral influences on brain 58 Moseley. B. (2002) Humans integrate visual and haptic 19 Suzuki. Neurol. Harvest Books dysfunction. Annu.J. et al. Science 303. Sci. influences memory for words and is modulated by metacognition and order learning in humans.neubiorev. 1979–1981 ownership and proprioceptive drift do not go hand in hand. 280. 13. (2011) Three systems of insular functional connectivity external objects: evidence from skin conductance response. V. Sci. Neural Comput. Gen.D. 44. Psychol. Sci. Cybern. A.S. C. T. and Tsakiris. J. J. to the body: Emotion as interoceptive inference. (2009) How do you feel – now? The anterior insula and 46 Botvinick. 287–313 Mind 121. H. (2013) Predictions not commands: active inference in 1316–1321 the motor system. and Tsakiris. J. 505–512 34 Preuschoff. (2008) Psychologically induced cooling of a specific and behavior.F. J. Trans. 1099–1108 68 Clark. M. Neurosci. 11 7 Seth. 214. http://dx. L.A. Natl. Conscious. F. (2011) The Rubber Hand Illusion: feeling of human brain. (1996) Varieties of Helmholtz Machine. A. 7.S. (2012) Multisensory brain mechanisms of bodily self- awareness. J. 29 Adams. 262. Proc. 270. Pers. G. L. Trends Cogn. 664–667 interoceptive sensitivity. 17. S. J.D. (2013) Multisensory integration across interoceptive and information in a statistically optimal fashion.N. 611–643 61 Armel. T. 191. 8. Lond. e21659 stimulus significance. (2009) A common role of insula in feelings. Soc. 102–107 51 Ernst. A. ownership and self-awareness of actions. Science 298. B: Biol. et al. PLoS ONE 2. B Biol. R. (2002) Emotion. M. Cortex 21. 189–195 consciousness.org/10. R. Nature 415. 1048 17 Metzinger. (2013) Turning body and self inside out: visualized 53 Karnath. and Banks. Science 317. S. 13. W. Brain Res. A. (2004) Neural systems supporting interoceptive 45 Blanke. T. MIT Press 50 Makin. et al. 1725–1738 determinants of emotional state. (1932) Emotional effects produced by the the ‘Outer’ Self: Interoceptive Sensitivity Modulates Self-Other injection of adrenalin. Soc. Neuron 77. A. Soc.doi.O. B. B: Biol. 7. (2011) Just a heartbeat away from one’s body: coding account of self-recognition. Rev. B Biol. et al. Neurosci. (2011) Does the salience network 11 Damasio. et al. K. Trends Cogn. 7–13 35 Holle. Am. Vol. T. (2012) The person in the mirror: using the of ideas about emotion in psychology. 379–399 57 Tajadura-Jimenez. N. Philos. sensory event is enough to induce ownership over a fake hand. and Carvalho.029 Proc. et al. Nature 429.R. 316–339 enfacement illusion to investigate the experiential structure of self- 24 Schachter. Psychophysiology 50. 21. Cereb. 756 14 Damasio.1037/a0033171 26 Critchley. (1998) Rubber hands ‘feel’ touch that eyes human awareness. 2470–2476 23 Gendron. 400–408 227–228 41 Gray. (2003) Being No-One. Psychol. T. 976–983 63 Garfinkel. Philos. 483–488 22 Apps. Sci. K.A. M. Psychol. and Frith. H. (1987) Levels of emotional awareness: a Proc. and Cohen.P. 33. (2012) Mechanisms of social cognition.S.F. B Biol. Psychiatry Neurosci. Science 317. PLoS 32 Lovero.org/10.D. A. Nat.D. Rev.doi. (2010) Action and behavior: a free-energy 54 Schandry. Rev. M.M. 334–340 self-consciousness. 218. H. R. A. (2000) The Feeling of What Happens: Body and Emotion in play a cardinal role in psychosis? An emerging hypothesis of insular the Making of Consciousness. 9. Soc. (2013) What the heart forgets: cardiac timing 33 Seymour. identified with cluster analysis.E. Cortex 23.doi. social. T. but not thermal 1191–1194 pain.Opinion Trends in Cognitive Sciences November 2013. A. 36. et al. 105. G.E. 59 Barnsley.1177/0956797613498395 411–417 21 Friston. Proc. Neurosci. No.

R. Funct. H. Brain are based on imprecise predictions about the sensory consequences of Struct. J. 83 Kim. J. K.J.B. Brain Struct. and Leafhead. (2013) The computational anatomy of psychosis.L.S. A. Ann. Rev. Y. frontoinsular and anterior cingulate cortex. et al. (2012) Prediction. 90 Friston. Vol. 83. (2012) Selective frontoinsular von Economo neuron and Funct. et al. (2011) Significance of the insula for the evolution of 85 Sierra. (2010) Misattributions of agency in schizophrenia insular and anterior cingulate cortex: awareness and response. L. Neurosci. (2012) Von economo neurons in the anterior insula of Cereb. 48–58 89 Friston. Psychophysiol. 214. 1328–1332 79 Adams. Soc. S. P. (2001) Depersonalization disorder: thinking 76 Harrison. Brain Struct. 1494–1496 1225. Brain 136.Opinion Trends in Cognitive Sciences November 2013. and Frith. Cortex 22. Front. C.C. (2012) Sensorimotor mismatch signals in primary Bayesian approach to explaining the positive symptoms of visual cortex of the behaving mouse. M. 3. Int. 12878–12884 87 Young. N. 262–271 71 Menon. Nat. et al. K. et al. V. K. eds). (2009) The pathways of interoceptive awareness. Brain 133. Sci. (2010) Conjoint activity of anterior 80 Synofzik.W. Cogn. and Critchley. J. et al.W. 482–489 84 Allman. Funct. (2010) The embodiment of emotional feelings in without feeling. 73 Evrard. J.D. (2013) The fantastic organ. Conscious. attention and 81 Silani. (2011) The von Economo neurons in the 74 Khalsa. Cogn. 10.M.J. 20 years on.S. et al. 248–252 573 .M. 59–71 75 Craig. 30. 21. In Method in Madness (Halligan. Y. No. 535–549 one’s actions. (2010) The von Economo neurons in frontoinsular dementia. P. Acad. switching. Neuron 74.D.W. 495–517 fork cell loss in early behavioral variant frontotemporal dementia. Funct. Neurosci.. 108. Conscious. 20. 251–259 the macaque monkey. Psychiatry 4. Psychiatry Res. perception and agency. (2011) Depersonalization: a selective human awareness of feelings from the body. (2010) Saliency. H. 11 70 Medford. 465–475 and anterior cingulate cortex in great apes and humans.C.M. 214.C.Q. M. N. N. and Uddin. Neurosci. impairment of self-awareness. M. N. (2009) Perceiving is believing: a 88 Keller. et al. Brain Struct. 214. Nat. Psychology Press 78 Fletcher. et al. 809–815 schizophrenia. (2010) Anterior insula degeneration in frontotemporal 72 Allman. G. Neurosci. W. 52–54 and Marshall. 214. et al.A. A. E. G. 97–112 655–667 82 Seeley. Sci. fMRI study. (2011) Explaining delusions of control: the comparator model studies of the Cotard delusion. Ann. 17. 145–160 the brain. Acad. Neuron 74. (1996) Betwixt life and death: case 77 Frith. 72–82 86 Phillips. and David. et al. et al. 99–108 1225. C. (2008) Levels of emotional awareness and autism: an control: a network model of insula function.A. 47 J. A. 12.D.