Summary Are external socio-emotional signals perceived differently by the brain depending on the internal states of our body? In this study we evaluate whether the perception of the emotional states of others depends on internal interoceptive states, combining multimodal measures (behavioral experiments, electrophysiology, brain anatomy and brain network connectivity) in healthy controls and patients with neurodegenerative diseases (Alzheimer’s disease , Parkinson’s and frontotemporal dementia). Our study suggests that if people focus on their own internal bodily states (cardiac interoception), the perception of emotions improves, accompanied by modulations at the behavioral, electrophysiological, neuroanatomical and brain connectivity levels. Furthermore, frontotemporal dementia, a condition characterized by socioemotional deficits, presents convergent and multimodal neurocognitive markers of interoceptive disruption during emotional processing (selective behavioral deficits, modulations of abnormal evoked potentials of the heart, insular-cingulate atrophy and alterations of the salience network ), compared to patients with Alzheimer’s, Parkinson’s disease and controls. These results support a predictive coding model of emotions based on interoceptive states, also proposing an inadequate allostatic load in frontotemporal dementia. |
| Everything is according to the body with which you look |
The external world around us is not perceived reflexively or passively. We learn to perceive reality based on our own fabric of meaning that provides each of us with partially similar and partially different perspectives. Ramón de Campoamor’s poem beautifully states “ that in the treacherous world / there is no truth or lie: / everything is according to the color / of the glass with which one looks ”, capturing the inner gaze with which we perceive and act in the world.
Cognitive neuroscience has devoted itself greatly to understanding how our brain perceives the outside world (especially in the case of our visual system), often forgetting that the brain is itself a crystal that establishes how we perceive. However, current approaches to situated and embodied cognition remind us again that our body and its circumstances are more than just a powerful filter through which we observe reality.
In particular, the importance of the organism’s internal signals from the study of interoception - processes through which the brain censures, integrates and sends information about bodily states - has gained enormous relevance. Imhotep in Egypt several millennia ago warned that cardiac blood flow influenced the brain, and some Greek philosophers proposed that the heart and intestines were the engines of the mind.
But it was William James, American philosopher and psychologist, who much later suggested that the perception of emotions has a bodily basis. For him, the origin of emotions came from the viscera. Later, Sherrington introduced the term interoception . Despite this, it took a long time for the body to take a leading role in contemporary cognitive neurosciences.
| The emotions of others under the glass of our body |
Interoceptive processes can be evaluated in a very simple way, for example through tasks in which participants follow their heartbeat . Based on this task, a new clinical-therapeutic agenda has emerged in multiple psychiatric and neurological diseases, including depression, anxiety, anorexia, depression, stroke, hypertension, dementia and so-called functional disorders. More recently, it has been suggested that interoceptive processes could impact social cognition (empathy, social decision making) and emotions.
Interoceptive predictive coding theory proposes that interoceptive states are used in future predictions (or Bayesian inference) based on previous bodily experiences, which colors the perception of external social phenomena . However, to date, it has not been possible to consistently demonstrate that changing interoceptive states also changes the perception of the external social world and its brain correlates.
| How our body impacts the perception of emotions and how this is affected by neurodegenerative diseases |
Cognitive neuroscience and behavioral neurology have begun to highlight interoceptive states as central modulators of emotions (and particularly negative ones, such as disgust, anger, or rage). However, the field lacks experimental designs that manipulate emotion perception through interoception and its brain correlates.
In this study we designed an experimental task that involves conditions of cardiac interoceptive focusing (attending to one’s own heartbeat) and exteroceptive control (attending to an eternal sound) followed by the presentation of facial emotions in which participants must recognize the type of emotion. .
We recruited 114 participants, including healthy controls, and patients with behavioral variant frontotemporal dementia (bvFTD), Parkinson’s disease (PD), and Alzheimer’s disease (AD). During the task, we measured modulations of cortical brain activity (with EEG, assessing the heart evoked potential, or HEP) and their association with patterns of anatomy and functional connectivity.
At the performance level, only bvFTD patients experienced deficits in tracking their interoceptive body states compared to controls. In the latter, cardiac interoceptive targeting generated better recognition of negative emotions (compared to the control task), but this effect was nullified in patients with bvFTD. Cardiac cortical activity (HEP) increased during the recognition of negative emotions, but only in the cardiac interoceptive focusing condition, both in controls and AD.
In all groups, recognition of negative emotions during the cardiac interoceptive focusing task was associated with increased volume of the insula and anterior cingulate cortex , two crucial regions of interoceptive and allostatic regulation. Furthermore, negative emotion recognition was associated with the connectivity of the salience network (an interoceptive-allostatic network) in the cardiac interoceptive focusing task, and with the executive network in the external stimulus control condition.
Salience network activity was impaired in relation to interoceptive emotional recognition in bvFTD. Our results together suggest that interoceptive states shape emotion recognition and its brain correlates, while revealing a specific pathophysiological marker of bvFTD. These findings provide a promising theoretical and clinical agenda for understanding interoception, emotion, allostasis, and neurodegeneration.
| Return the body to the perception of reality |
The investigation of the interaction between internal bodily signals and emotions has a long controversy in cognitive neuroscience, psychiatric, neurology and related disciplines. This study, in conjunction with other results, has theoretical and clinical implications. The construction of subjective bodily states permeates multiple processes of external perception.
Given that processing the emotions of others (and other external objects) would seem to depend on one’s own visceral perception, many clinical practices could be improved by better understanding interoception. This becomes an essential component of allostasis , the anticipation based on physiological needs and internal states, of external signals and context. This opens new avenues for a clinical agenda at the intersection of cognitive neuroscience, psychiatry, and cognitive neurology .
Apparently, the brain uses the body’s internal states to anticipate the needs of the context and define the most adaptive responses.
In the case of heartbeats and other visceral signals, this suggests that the perception of external socioemotional information is an active process based on one’s own previous experiences along with contextual expectations. In other words, the perception of external reality is a co-construction of an internal narrative .
Although this conclusion may sound purely philosophical, and may even be incorrectly interpreted as Berkeley solipsism , I believe it opens up new possibilities. Multi-disciplinary clinics for physical and mental illness require new approaches that clarify the functioning of these subjective and corporeal processes that occur in patients.
A clear example of this is functional disorders (which usually involve cardiovascular, gastrointestinal or chronic pain conditions), in which doctors’ misunderstanding of patients’ interoceptive or subjective states often leads to over-medication, negligence or underestimation of suffering .
Health professionals are often trapped in theoretical and methodological gaps to evaluate subjective illness, and much more to evaluate how said illness impacts the particular perception of the external world. This emptiness seems to come from misunderstanding the body at the service of the brain in a scheme of homeostasis . In contrast to this, for allostasis , it is the brain that is actively at the service of the body.
It seems that the study of external realities often denies our internal universe. Carl Sagan reminded us that we are "stardust." Even earlier, in 1929, astronomer Harlow Shapley said in The New York Times that “our own bodies are composed of the same chemical elements found in the most distant nebulae.” The neuroscience of interoception would replicate today, in a paradoxical and circular device, that the crystal in our body today returns that peculiar shine to the stars.
