Abstract
Mental processes and their neural substrates are intimately linked to the homeostatic control of internal bodily state. There are a set of distinct interoceptive pathways that directly and indirectly influence brain functions. The anatomical organization of these pathways and the psychological/behavioral expressions of their influence appear along discrete, evolutionarily conserved dimensions that are tractable to a mechanistic understanding. Here, we review the role of these pathways as sources of biases to perception, cognition, emotion, and behavior and arguably the dynamic basis to the concept of self.
Main Text
Introduction
The internal state of the body motivates our desire to walk in the shade on a warm summer’s day and inhibits the desire to eat or socialize when feeling off-color. Communication from the viscera to brain is continuous and pervasive, yet we rarely give it a second thought. Visceral fluctuations and reactions accessible to introspective appraisal represent only the visible tip of the iceberg. The majority of visceral signals that shape behavior, cognition, and, arguably, emotion go unnoticed. Techniques such as human neuroimaging permit valuable insights into the brain basis of perceptions, thoughts, feelings, and actions, yet these mental functions are for the most part considered in isolation from the physiological state of the body. Nevertheless, experimental information from studies of autonomic psychophysiology, feeding and metabolism, osmoregulation, and psychoneuroimmunology is converging. Identification of the neural circuitry representing internal state paves the way for more comprehensive understanding of how visceral signals shape human cognition and behavior.
The brain is dependent on the physiological state of the body in two ways. First, the brain requires appropriate conditions (physiological context) for efficient biological functioning. Second, the brain receives and responds to continuous dynamic feedback of afferent visceral signals (informational context) that shape its operational functioning. The latter is classical interoception, i.e., the encoding and representation of internal bodily signals reporting the body’s physiological state (Craig, 2002). Interoceptive information is conveyed centrally by cranial and spinal nerves and by direct sampling of chemicals carried in the blood within specialized brain structures. This information is comprehensive, encompassing distinct classes of signal with distinct temporal response characteristics (including hormonal, immunological, metabolic, thermal, nociceptive, and visceromotor). These parameters are encoded across a set of brain regions in a way that permits dynamic interaction and integration with descending (top down) expressions of perceptual expectation and volitional control of action.
The concept of homeostasis as a collection of reflexes has biased research on viscera-brain interactions to focus on proximate factors determining stability of physiological state within set ranges. Interoceptive pathways do signal deviation of individual physiological parameters toward the limits of these ranges, but it is behavior that determines the environmental challenges and rate of internal change, e.g., build up of metabolic byproducts. Homeostatic control is well described in terms of local reflexes in individual or groups of organs. Patterned homeostatic autonomic responses are coordinated within brainstem and hypothalamus (Saper, 2002). Efficient internal regulation also requires integration across systems and ultimately at the whole organism level. Internal visceral states drive complex motivational behaviors both implicitly and through cognitive and affective responses, e.g., arousal, sickness behavior, memory, and mood. There is a primacy of interoceptive control to functional health; the fundamental experience and awareness of self is proposed to follow dynamic central representations of physiological state, driven by afferent visceral signaling (e.g., Damasio, 2010). However, empirical neuroscientific data about the extent to which internal bodily state influences behavior have been slow to emerge. Here, we draw together anatomical and experimental information about the representation and influence of visceral state on brain processes to illustrate principles through which human behavior and experience is colored by internal bodily signals.
Interoception and Emotion
Aristotle’s attribution of sensation and emotion to the heart contrasted sharply with the Hippocratic recognition of the brain as the source of mental operations and experiences (Gross, 1995). The fundamental association between bodily changes and emotions remains apparent in the universal use of physiological words to describe emotional states. Darwin highlighted the consistency of physiological expression of emotions even across species (Darwin, 1872). Shortly thereafter, James and Lange both argued for an obligatory origin of emotional feelings in bodily physiological changes (Lange, 1885; James, 1894). Lange’s conceptualization of specific bodily changes as signatures of individual emotions was in line with Darwin’s notion of “basic emotions”; James was more “constructionist,” viewing emotions as made up of elements (e.g., bodily arousal) shared by other processes (Gendron and Barrett, 2009). Cannon (1927), meanwhile, argued that physiological changes accompanying emotions were not necessarily specific to emotions. Yet, the idea that emotions are dependent on physiological changes, in conjunction with cognitive evaluation/appraisal of the context, has proved relatively robust (Cantril and Hunt, 1932; Schachter and Singer, 1962). Emotions are now commonly viewed as a class of psychological states that encompass behavioral, experiential, and visceral changes (Gendron and Barrett, 2009).
In parallel with these developments in psychology, knowledge has progressed regarding the representation and control of visceral state above the level of the brainstem. Electrical stimulation in animals and man has demonstrated the coupling of visceral responses to neocortical regions (e.g., Kaada, 1951; Penfield and Faulk, 1955). There is increasing interest in the neural substrates of emotion, triggered in part by evidence-driven arguments for basic emotional states (Ekman et al., 1983; Panksepp, 1998) and emergence of consciousness science. Thus, internal bodily changes are shown to act as covert unconscious influences on “conscious” processes, notably motivational decision making (Bechara et al., 1997). Such effects are linked to the integrity of orbitofrontal, somatosensory, and insular cortices and their putative roles in supporting emotional processes grounded in bodily states. Increasingly detailed understanding of the anatomical projections of interoceptive neural pathways into cortical regions complements functional neuroimaging evidence in humans (Allen et al., 1991, King et al., 1999). The notion that viscerosensory insula cortex supports more general emotional experiences is further highlighted by functional neuroanatomists (Craig, 2002; Saper, 2002). Concepts of emotion continue to be refined, yet distinct theoretical stances typically acknowledge the contribution of physiological changes (Gendron and Barrett, 2009). Experimental research into the mechanisms through which visceral afferent information is represented within the brain will continue to enrich our understanding of emotion, cognition and behavior.
Conclusions
Internal bodily state exerts pervasive influences on brain function and mental activity. There is a primacy to these representations. Interoceptive signals inform central control processes necessary to maintain life, a role that naturally emerges prior to maturation of the exteroceptive senses and which is usually uninterrupted thereafter. Adaptive behavior is motivated by the need to ensure immediate and prospective integrity of internal physiology, from which emerges motivational states and emotions of increasing complexity. The integration of rich humoral and neural viscerosensory information is supported by a relatively small set of interacting brain areas linked to low-level homeostatic reflexes, but these are able to draw on both instinctive and volitional behavioral repertoires when functionally challenged. It is likely that predictive coding underlies the operational architecture of viscerosensory control, including consciously accessible feeling states, influencing motivational behaviors and directing cognitive processes including memory. Interoceptive representations are also engaged, perhaps symbolically, in the exchange of social emotions. Perturbation of viscerosensory representation is anticipated to impact multiple levels of functioning, yet clinically there appears to be redundancy and a robustness that mitigates major decompensation. Affective, dissociative, and psychotic phenomena suggest uncoupling of a usually integrated physiological and cognitive representation of self. A comprehensive understanding of the integration of internal bodily signals in health is ultimately required for effective management of physical and psychological symptoms in illness. Such a goal can only be achieved through coordinated experimental approaches and perhaps a move away from treating physiological changes as irrelevant confounds in neuropsychological experiments. Together, these observations make “us realize more deeply than ever how much of our mental life is knit up in our corporeal frame” (James, 1890).
Acknowledgments
N.A.H. is funded by the Wellcome Trust. N.A.H. and H.D.C. are faculty within the Sackler Centre for Consciousness Science, University of Sussex, supported by the Dr. Mortimer and Theresa Sackler Foundation. Help with the manuscript and figures from Dr. S. Garfinkel and with earlier drafts from Dr. M. Gray is gratefully acknowledged.