ABSTRACT
We propose a computational framework for high-dimensional brain-body states as transient embodiments of nested internal and external dynamics governed by interoception. Unifying recent theoretical work, we suggest ways to reduce arbitrary state complexity to an observable number of features in order to accurately predict and intervene in pathological trajectories.
Subject(s)
Brain , Interoception , Humans , Brain/physiology , Interoception/physiologyABSTRACT
BACKGROUND AND HYPOTHESIS: There is mounting evidence that cardiac interoception, the perception of one's heartbeat, is central to affective experiences. It has been proposed that symptoms of psychosis could arise from interoceptive dysfunction. Here we hypothesized that people with psychotic disorders would have a specific impairment in cardiac interoception, over and above broader perceptual deficits. STUDY DESIGN: 43 adults with a history of psychosis (31 schizophrenia, 12 schizoaffective disorder) and 41 matched control participants completed a heart rate discrimination task. Participants responded to whether they perceived a sequence of auditory tones to be faster or slower than their heart rate. By trialing a range of auditory tone rates, we estimated a threshold for each participant, the difference between perceived heart rate and actual heart rate. To test whether differences were specific to interoception, participants completed an exteroceptive control condition, testing their discrimination of the rate of 2 sets of audible sounds instead of heart rate. STUDY RESULTS: Participants with a history of psychosis had greater absolute differences between perceived and actual heart rate, indicating over- or under-estimation of heart rate compared to healthy controls. This difference was specific to the interoceptive condition, and not explained by group differences in exteroceptive perception. CONCLUSIONS: Psychotic disorders are associated with misestimation of heart rate. Further research may elucidate whether interoceptive abnormalities contribute to specific symptoms such as somatic delusions or affective features, and whether interoception could be a treatment target in psychotic disorders.
ABSTRACT
Interoception-the perception of internal bodily signals-has emerged as an area of interest due to its implications in emotion and the prevalence of dysfunctional interoceptive processes across psychopathological conditions. Despite the importance of interoception in cognitive neuroscience and psychiatry, its experimental manipulation remains technically challenging. This is due to the invasive nature of existing methods, the limitation of self-report and unimodal measures of interoception, and the absence of standardized approaches across disparate fields. This article integrates diverse research efforts from psychology, physiology, psychiatry, and engineering to address this oversight. Following a general introduction to the neurophysiology of interoception as hierarchical predictive processing, we review the existing paradigms for manipulating interoception (e.g., interoceptive modulation), their underlying mechanisms (e.g., interoceptive conditioning), and clinical applications (e.g., interoceptive exposure). We suggest a classification for interoceptive technologies and discuss their potential for diagnosing and treating mental health disorders. Despite promising results, considerable work is still needed to develop standardized, validated measures of interoceptive function across domains and before these technologies can translate safely and effectively to clinical settings.
Subject(s)
Cognitive Neuroscience , Interoception , Mental Disorders , Humans , Emotions/physiology , Mental Disorders/diagnosis , Mental Disorders/therapy , Self Report , Interoception/physiology , Heart Rate , Awareness/physiologyABSTRACT
Breathing plays a crucial role in shaping perceptual and cognitive processes by regulating the strength and synchronisation of neural oscillations. Numerous studies have demonstrated that respiratory rhythms govern a wide range of behavioural effects across cognitive, affective, and perceptual domains. Additionally, respiratory-modulated brain oscillations have been observed in various mammalian models and across diverse frequency spectra. However, a comprehensive framework to elucidate these disparate phenomena remains elusive. In this review, we synthesise existing findings to propose a neural gradient of respiratory-modulated brain oscillations and examine recent computational models of neural oscillations to map this gradient onto a hierarchical cascade of precision-weighted prediction errors. By deciphering the computational mechanisms underlying respiratory control of these processes, we can potentially uncover new pathways for understanding the link between respiratory-brain coupling and psychiatric disorders.
Subject(s)
Brain Waves , Mental Disorders , Animals , Humans , Brain Waves/physiology , Brain , Respiration , MammalsABSTRACT
Interoception is the sensation, perception, and integration of signals from within the body. It has been associated with a broad range of physiological and psychological processes. Further, interoceptive variables are related to specific regions and networks in the human brain. However, it is not clear whether or how these networks relate empirically to different domains of physiological and psychological health at the population level. We analysed a data set of 19,020 individuals (10,055 females, 8965 males; mean age: 63 years, age range: 45-81 years), who have participated in the UK Biobank Study, a very large-scale prospective epidemiological health study. Using canonical correlation analysis (CCA), allowing for the examination of associations between two sets of variables, we related the functional connectome of brain regions implicated in interoception to a selection of nonimaging health and lifestyle related phenotypes, exploring their relationship within modes of population co-variation. In one integrated and data driven analysis, we obtained four statistically significant modes. Modes could be categorised into domains of arousal and affect and cardiovascular health, respiratory health, body mass, and subjective health (all p < .0001) and were meaningfully associated with distinct neural circuits. Circuits represent specific neural "fingerprints" of functional domains and set the scope for future studies on the neurobiology of interoceptive involvement in different lifestyle and health-related phenotypes. Therefore, our research contributes to the conceptualisation of interoception and may lead to a better understanding of co-morbid conditions in the light of shared interoceptive structures.
Subject(s)
Connectome , Interoception , Male , Female , Humans , Middle Aged , Aged , Aged, 80 and over , Prospective Studies , Brain/physiology , Sensation/physiology , Heart , Interoception/physiology , Awareness , Heart RateABSTRACT
Respiratory rhythms sustain biological life, governing the homeostatic exchange of oxygen and carbon dioxide. Until recently, however, the influence of breathing on the brain has largely been overlooked. Yet new evidence demonstrates that the act of breathing exerts a substantive, rhythmic influence on perception, emotion, and cognition, largely through the direct modulation of neural oscillations. Here, we synthesize these findings to motivate a new predictive coding model of respiratory brain coupling, in which breathing rhythmically modulates both local and global neural gain, to optimize cognitive and affective processing. Our model further explains how respiratory rhythms interact with the topology of the functional connectome, and we highlight key implications for the computational psychiatry of disordered respiratory and interoceptive inference. (PsycInfo Database Record (c) 2023 APA, all rights reserved).
Subject(s)
Brain , Interoception , Respiration , Brain/physiology , Interoception/physiology , Humans , Affect , Cognition , Models, Biological , Neurons/physiology , ConnectomeABSTRACT
A growing body of evidence highlights the intricate linkage of exteroceptive perception to the rhythmic activity of the visceral body. In parallel, interoceptive inference theories of affective perception and self-consciousness are on the rise in cognitive science. However, thus far no formal theory has emerged to integrate these twin domains; instead, most extant work is conceptual in nature. Here, we introduce a formal model of cardiac active inference, which explains how ascending cardiac signals entrain exteroceptive sensory perception and uncertainty. Through simulated psychophysics, we reproduce the defensive startle reflex and commonly reported effects linking the cardiac cycle to affective behaviour. We further show that simulated 'interoceptive lesions' blunt affective expectations, induce psychosomatic hallucinations, and exacerbate biases in perceptual uncertainty. Through synthetic heart-rate variability analyses, we illustrate how the balance of arousal-priors and visceral prediction errors produces idiosyncratic patterns of physiological reactivity. Our model thus offers a roadmap for computationally phenotyping disordered brain-body interaction.
Subject(s)
Interoception , Brain , Emotions/physiology , Heart Rate/physiology , Interoception/physiologyABSTRACT
Bruineberg and colleagues report a striking confusion, in which the formal Bayesian notion of a "Markov blanket" has been frequently misunderstood and misapplied to phenomena of mind and life. I argue that misappropriation of formal concepts is pervasive in the "predictive processing" literature, and echo Richard Feynman in suggesting how we might resist the allure of cargo cult computationalism.
ABSTRACT
The ability to sense, monitor, and control respiration - e.g., respiratory interoception (henceforth, respiroception) is a core homeostatic ability. Beyond the regulation of gas exchange, enhanced awareness of respiratory sensations is directly related to psychiatric symptoms such as panic and anxiety. Indeed, chronic breathlessness (dyspnea) is associated with a fourfold increase in the risk of developing depression and anxiety, and the regulation of the breath is a key aspect of many mindfulness-based approaches to the treatment of mental illness. Physiologically speaking, the ability to accurately monitor respiratory sensations is important for optimizing cardiorespiratory function during athletic exertion, and can be a key indicator of illness. Given the important role of respiroception in mental and physical health, it is unsurprising that there is increased interest in the quantification of respiratory psychophysiology across different perceptual and metacognitive levels of the psychological hierarchy. Compared to other more popular modalities of interoception, such as in the cardiac domain, there are relatively few methods available for measuring aspects of respiroception. Existing inspiratory loading tasks are difficult to administer and frequently require expensive medical equipment, or offer poor granularity in their quantification of respiratory-related perceptual ability. To facilitate the study of respiroception, we here present a new, fully automated and computer-controlled apparatus and psychophysiological method, which can flexibly and easily measure respiratory-related interoceptive sensitivity, bias and metacognition, in as little as 30 min of testing, using easy to make 3D printable parts.
Subject(s)
Interoception , Metacognition , Anxiety , Awareness , Dyspnea , Heart Rate/physiology , Humans , Interoception/physiology , Metacognition/physiology , Respiratory RateABSTRACT
Over the past six years, a rapidly growing number of studies have shown that respiration exerts a significant influence on sensory, affective, and cognitive processes. At the same time, an increasing amount of experimental evidence indicates that this influence occurs via modulation of neural oscillations and their synchronization between brain areas. In this article, we review the relevant findings and discuss whether they might inform our understanding of a variety of disorders that have been associated with abnormal patterns of respiration. We review literature on the role of respiration in chronic obstructive pulmonary disease (COPD), anxiety (panic attacks), and autism spectrum disorder (ASD), and we conclude that the new insights into respiratory modulation of neuronal activity may help understand the relationship between respiratory abnormalities and cognitive and affective deficits.
Subject(s)
Autism Spectrum Disorder , Panic Disorder , Brain , Cognition , Emotions , Humans , Panic Disorder/psychologyABSTRACT
Interoception - the physiological sense of our inner bodies - has risen to the forefront of psychological and psychiatric research. Much of this research utilizes tasks that attempt to measure the ability to accurately detect cardiac signals. Unfortunately, these approaches are confounded by well-known issues limiting their validity and interpretation. At the core of this controversy is the role of subjective beliefs about the heart rate in confounding measures of interoceptive accuracy. Here, we recast these beliefs as an important part of the causal machinery of interoception, and offer a novel psychophysical "heart rate discrimination" method to estimate their accuracy and precision. By applying this task in 223 healthy participants, we demonstrate that cardiac interoceptive beliefs are more biased, less precise, and are associated with poorer metacognitive insight relative to an exteroceptive control condition. Our task, provided as an open-source python package, offers a robust approach to quantifying cardiac beliefs.
Subject(s)
Interoception , Metacognition , Awareness/physiology , Healthy Volunteers , Heart , Heart Rate/physiology , Humans , Interoception/physiologyABSTRACT
The study of the brain's processing of sensory inputs from within the body ('interoception') has been gaining rapid popularity in neuroscience, where interoceptive disturbances are thought to exist across a wide range of chronic physiological and psychological conditions. Here we present a task and analysis procedure to quantify specific dimensions of breathing-related interoception, including interoceptive sensitivity, decision bias, metacognitive bias, and metacognitive performance. Two major developments address some of the challenges presented by low trial numbers in interoceptive experiments: (i) a novel adaptive algorithm to maintain task performance at 70-75% accuracy; (ii) an extended hierarchical metacognitive model to estimate regression parameters linking metacognitive performance to relevant (e.g. clinical) variables. We demonstrate the utility of the task and analysis developments, using both simulated data and three empirical datasets. This methodology represents an important step towards accurately quantifying interoceptive dimensions from a simple experimental procedure that is compatible with clinical settings.
Subject(s)
Interoception , Metacognition , Heart Rate , Humans , Respiration , Task Performance and AnalysisABSTRACT
As source of sensory information, the body provides a sense of agency and self/non-self-discrimination. The integration of bodily states and sensory inputs with prior beliefs has been linked to the generation of bodily self-consciousness. The ability to detect surprising tactile stimuli is essential for the survival of an organism and for the formation of mental body representations. Despite the relevance for a variety of psychiatric disorders characterized by altered body and self-perception, the neurobiology of these processes is poorly understood. We therefore investigated the effect of psilocybin (Psi), known to induce alterations in self-experience, on tactile mismatch responses by combining pharmacological manipulations with simultaneous electroencephalography-functional magnetic resonance imaging (EEG-fMRI) recording. Psi reduced activity in response to tactile surprising stimuli in frontal regions, the visual cortex, and the cerebellum. Furthermore, Psi reduced tactile mismatch negativity EEG responses at frontal electrodes, associated with alterations of body- and self-experience. This study provides first evidence that Psi alters the integration of tactile sensory inputs through aberrant prediction error processing and highlights the importance of the 5-HT2A system in tactile deviancy processing as well as in the integration of bodily and self-related stimuli. These findings may have important implications for the treatment of psychiatric disorders characterized by aberrant bodily self-awareness.
Subject(s)
Magnetic Resonance Imaging , Psilocybin , Body Image , Electroencephalography , Humans , Psilocybin/pharmacology , TouchABSTRACT
The positive-negative axis of emotional valence has long been recognized as fundamental to adaptive behavior, but its origin and underlying function have largely eluded formal theorizing and computational modeling. Using deep active inference, a hierarchical inference scheme that rests on inverting a model of how sensory data are generated, we develop a principled Bayesian model of emotional valence. This formulation asserts that agents infer their valence state based on the expected precision of their action model-an internal estimate of overall model fitness ("subjective fitness"). This index of subjective fitness can be estimated within any environment and exploits the domain generality of second-order beliefs (beliefs about beliefs). We show how maintaining internal valence representations allows the ensuing affective agent to optimize confidence in action selection preemptively. Valence representations can in turn be optimized by leveraging the (Bayes-optimal) updating term for subjective fitness, which we label affective charge (AC). AC tracks changes in fitness estimates and lends a sign to otherwise unsigned divergences between predictions and outcomes. We simulate the resulting affective inference by subjecting an in silico affective agent to a T-maze paradigm requiring context learning, followed by context reversal. This formulation of affective inference offers a principled account of the link between affect, (mental) action, and implicit metacognition. It characterizes how a deep biological system can infer its affective state and reduce uncertainty about such inferences through internal action (i.e., top-down modulation of priors that underwrite confidence). Thus, we demonstrate the potential of active inference to provide a formal and computationally tractable account of affect. Our demonstration of the face validity and potential utility of this formulation represents the first step within a larger research program. Next, this model can be leveraged to test the hypothesized role of valence by fitting the model to behavioral and neuronal responses.
ABSTRACT
Emotion alters how we feel, see, and experience the world. In the domain of memory, the emotional valence and arousal of memorised stimuli can modulate both the acuity and content of episodic recall. However, no experiment has investigated whether arousal and valence also influence metacognition for memory (i.e. the process of self-monitoring memories). In a pre-registered study, we applied a novel psychophysiological design together with computational models of metacognition to assess the influence of stimulus valence and arousal on the sensitivity, bias, and efficiency of metamemory. To estimate the role of physiological arousal in mediating these effects, we recorded cardiac measures through pulse oximetry. We found that negative valence substantially decreased both memory performance and subjective confidence, in particular for low arousal words. Simultaneously, we found that emotional valence modulated both heart rate and heart-rate variability (HRV) during recognition memory. Exploratory trial-level analyses further revealed that subjective confidence was encoded in instantaneous heart-rate fluctuations and that this relationship was also modulated by emotional valence. Our results demonstrate that recognition memory and metacognition are influenced by the emotional valence of encoded items and that this correlation is in part related to cardiac activity.
Subject(s)
Metacognition , Arousal , Emotions , Humans , Mental Recall , Recognition, PsychologyABSTRACT
The Bayesian brain hypothesis, as formalized by the free-energy principle, is ascendant in cognitive science. But, how does the Bayesian brain obtain prior beliefs? Veissière and colleagues argue that sociocultural interaction is one important source. We offer a complementary model in which "interoceptive self-inference" guides the estimation of expected uncertainty both in ourselves and in our social conspecifics.
Subject(s)
Brain , Cognitive Science , Bayes Theorem , Humans , UncertaintyABSTRACT
What is the function of the insular cortex? Two recent studies (by Gehrlach et al. and Livneh et al.) offer new insight into how this enigmatic brain region integrates interoception and exteroception in the service of emotion. The findings provide much needed causal evidence for the nascent theory of interoceptive inference.
Subject(s)
Interoception , Brain , Cerebral Cortex , Emotions , Humans , NeurobiologyABSTRACT
Heat and pain illusions (synthetic heat and the thermal grill illusion) can be generated by simultaneous cold and warm stimulation on the skin at temperatures that would normally be perceived as innocuous in isolation. Historically, two key questions have dominated the literature: which specific pathway conveys the illusory perceptions of heat and pain, and where, specifically, does the illusory pain originate in the central nervous system? Two major theories - the addition and disinhibition theories - have suggested distinct pathways, as well as specific spinal or supraspinal mechanisms. However, both theories fail to fully explain experimental findings on illusory heat and pain phenomena. We suggest that the disagreement between previous theories and experimental evidence can be solved by abandoning the assumption of one-to-one relations between pathways and perceived qualities. We argue that a population coding framework, based on distributed activity across non-nociceptive and nociceptive pathways, offers a more powerful explanation of illusory heat and pain. This framework offers new hypotheses regarding the neural mechanisms underlying temperature and pain perception.
Subject(s)
Illusions/physiology , Models, Biological , Nociception/physiology , Pain/physiopathology , Thermosensing/physiology , HumansABSTRACT
Neural activity within the default mode network (DMN) is widely assumed to relate to processing during off-task states, however it remains unclear whether this association emerges from a shared role in self or social content that is common in these conditions. In the current study, we examine the possibility that the role of the DMN in ongoing thought emerges from contributions to specific features of off-task experience such as self-relevant or social content. A group of participants described their experiences while performing a laboratory task over a period of days. In a different session, neural activity was measured while participants performed Self/Other judgements (e.g., Does the word 'Honest' apply to you (Self condition) or Barack Obama (Other condition)). Despite the prominence of social and personal content in off-task reports, there was no association with neural activity during off-task trait adjective judgements. Instead, during both Self and Other judgements we found recruitment of caudal posterior cingulate cortex-a core DMN hub-was above baseline for individuals whose laboratory experiences were characterised as detailed. These data provide little support for a role of the DMN in self or other content in the off-task state and instead suggest a role in how on-going thought is represented.