Follow your gut: A review on the gut-brain
axis and emotion regulation
Master Brain and Cognitive Sciences
Literature thesis
Kanthida van Welzen (10797424)
Supervisor: Laura Steenbergen
Examiner: Suzanne Oosterwijk
Abstract
Influential theories have indicated that the perception of physiological sensations within the body constitute emotional feelings. Interoception is the vital process of afferent signalling from the internal systems of the body to the brain. Recent findings have conceptualised interoception and its related neuroanatomy and these developments have confirmed that the interoceptive system is relevant for emotion. Thereby, being aware of interoceptive signals also contributes to appropriate emotion regulation. The growing understanding of interoception and its role in emotion and emotion regulation has been mainly examined by assessing cardiac interoception, overlooking the relevance of other interoceptive sensations, such as the gastrointestinal system. The gastrointestinal system or also called the gut has received increasing attention and demonstrate the complex interactions involved in regulating gut homeostasis. Via the gut-brain axis, the gut and the brain can communicate through many pathways. Therefore, this review will consider whether the gut is crucial for emotion and emotion regulation.
Keywords: Interoception, gut-brain axis, emotion, emotion regulation
Introduction
Some of us might relate to the following scenario whereas others do not:
While you are working, you notice that you are getting annoyed quickly by things surrounding you, like the buzzing of the light above you, the computer crashing, the incoming emails, etc. Then
someone comes in the room with a question, but as you have already been agitated by your surroundings, you just snarl them away. Sooner or later, you realise that you are hungry. Once you have eaten, you are satiated and you also notice that you are not moody anymore.
This is a classic case of being ‘hangry’ (hungry and angry), defined by the Urban Dictionary as: “when a person gets to the point of being angry, snappy, short-tempered, or emotional due to lack of food and being extremely hungry”. This example clearly shows how the gut, by indicating that you are hungry, can influence your emotion and behaviour and once you have taken care of your gut by eating food, the hunger is gone and the emotion has been regulated. Moreover, this example indicates that sensations from the body are important to correctly identify and to be aware of emotions, which in turn is the start of appropriate emotion regulation (Berking & Whitley, 2014; Gratz & Roemer, 2004).
One might not be aware of the importance of bodily sensations in emotion, but theories have suggested this for a long time. A well-known theory by James (1884) proposed that the perceived situation induces changes in the body and via afferent feedback to the brain induce a specific emotion. Damasio's (1999) somatic marker hypothesis also indicates the role of body perception by proposing that somatic markers (representations of the body associated with certain emotions) arise from emotional feelings being associated with certain bodily responses (body loops) to certain situations. These body loops can thereby influence behaviour, such as decision-making. A more recent account is the theory of constructed emotion (Feldman Barrett, 2017). It states that the brain runs an internal model of the world with sensations both from the external (outside of the body) and internal (inside the body) milieu. The internal model makes predictions by running past experiences as implemented concepts. When the prediction is similar to the newly incoming information, the prediction becomes a perception or an experience e.g., feeling of an emotion. These theories indicate that the perception of sensations from the body, also called interoception, is a basis of for emotion.
More importantly, interoception and the emotions that it constitutes are crucial for regulating life. In the end, the brain’s core task is to ensure that it has the resources to fulfil the body’s needs (Sterling, 2012). Interoception provides feedback about one’s bodily state to the brain, including information for homeostatic reflexes and allostatic control (Critchley & Garfinkel, 2017). It encompasses information from all tissues of the body such as the viscera, but also the nociceptive system, thermoregulatory system, endocrine and immune systems (Craig, 2002, 2003). For practical reasons, the most commonly studied interoceptive system is the heart and the cardiovascular system (Critchley, Wiens, Rotshtein, Öhman, & Dolan, 2004; Schulz, 2016) and its effect on emotion and emotion regulation (Dunn et al., 2010; Pollatos, Schandry, Auer, & Kaufmann, 2007). Little light has been shed on the gastrointestinal system, although in our language sayings as ‘hangry’, ‘gut feeling’ and ‘butterflies in your stomach’ are a first indication that gut signals guide us in our emotions and
behaviour. Moreover, the gut has received increasing attention and thereby our understanding of it over the last few decades (reviewed in Mayer, 2011). It has been discovered that the gastrointestinal system has its own nervous system called the enteric nervous system and it is often referred to as the ‘second brain’ because of its size, complexity and similarity to the brain. Furthermore, the gut and the brain have many ways to communicate with each other and this has been referred to as the gut-brain axis. Via this axis, the gut can influence the brain and subsequently behaviour as it is clear in the case of behavioural disorders such as anxiety and depression (Cryan & Dinan, 2012). Preliminary evidence shows that treatments involving one of the connections between the brain and the gut have beneficial effects on mood and anxiety (Breit, Kupferberg, Rogler, & Hasler, 2018). This indicates that by influencing the gut-brain axis, emotion dysregulation can be altered in affective disorders. Thus, it is noteworthy to review the potential role of the gut-brain axis in emotion regulation.
As discussed above, the importance of the gut-brain axis in brain and behaviour is just starting to unravel. The gut-brain axis consists of many potential pathways to communicate with the brain and so affect emotion regulation. In this review I will examine studies to comprehend the gut-brain axis and its influence on emotion regulation. First, I will give a broad view about interoception and its role in emotion and emotion regulation. Then I will explain the pathways through which the gut-brain axis could influence emotion and emotion regulation and I will highlight studies investigating how the gut-brain axis modulates emotion regulation. Lastly, I will summarize these findings to understand whether the gut-brain axis is crucial in emotion regulation.
Overview of interoception and its related neuroanatomy
The theory of emotion (James, 1884), the somatic marker hypothesis (Damasio, 1999) and theory of constructed emotion (Feldman Barrett, 2017) indicate the importance of perceived sensations from the body in emotion processing. To better comprehend how the gut can possibly influence emotion and emotion regulation, an overview of interoception and related neuroanatomy will be presented.
Interoception is a vital process that sends information from the body to the brain and because of its necessity in homeostasis, it has been extensively researched (Craig, 2002, 2003; Critchley & Garfinkel, 2017; Critchley & Harrison, 2013). Via the homeostatic afferent system, information from all internal systems - including the gut – ascend via afferent fibres of the sympathetic nervous system (spinal lamina 1 neurons) and the parasympathetic nervous system (vagus nerve and glossopharyngeal nerve) to the nucleus of the solitary tract (NTS) in the brain (Berntson, Sarter, & Cacioppo, 2003; Craig, 2003; Critchley & Harrison, 2013). The NTS can engage the noradrenergic pathways via the locus coeruleus but also pass on the information to other brain regions (e.g., parabrachial nucleus, periaqueductal grey (PAG), and thalamus) where the information from all homeostatic afferents is integrated for the maintenance of the physiological condition of the body. From there, information
reaches the anterior cingulate cortex (ACC) and the insula, with the latter one being suggested as the interoceptive cortex (Kurth, Zilles, Fox, Laird, & Eickhoff, 2010). The insula integrates gradually more information in a posterior-to-anterior progression starting in the posterior (dorsal) insula with a cortical representation of all the distinct interoceptive sensations (e.g., heart rate, respiration, and gastrointestinal sensations) (Craig, 2002, 2003, 2009). Continuing to the mid-insula, these homeostatic re-representations are combined with activation associated with emotionally salient environmental stimuli coming from higher-order sensory regions. In the anterior insula, the re-representations from the mid-insula are integrated with information about hedonic conditions from the orbitofrontal cortex and information concerning motivational and social conditions from the ACC. The final re-representation in the anterior insula constitutes the basis for the subjective perception of one’s physical condition, leading to consciousness and self-awareness of one’s body (Craig, 2009; Critchley & Harrison, 2013; A. Damasio, 2003). Although the insula is seen as the interoceptive cortex and the central region for interoceptive awareness, the somatosensory cortex is critical too (Khalsa, Rudrauf, Feinstein, & Tranel, 2009). These cortical regions involved in interoception are called visceromotor regions and alterations in this system do not only affect awareness in interoception but also in emotion and emotion regulation as will be discussed in the upcoming paragraph.
Although the comprehensive knowledge on the homeostatic afferent system through which we have interoception, methods to assess interoceptive ability have been inconsistent. Since recently, a clear differentiation has been made in interoception between the objective, subjective and metacognitive aspects (Garfinkel, Seth, Barrett, Suzuki, & Critchley, 2015). Firstly, interoceptive accuracy is objectively measured with paradigms that quantify differences between individuals. These are tasks that involve individuals to track or detect an internal bodily sensation accurately. Tasks that involve the heartbeat dominate because heartbeats are distinct and thereby easily discriminated and measured. For example, in the heartbeat tracking task an individual is asked to count the number of times they can perceive their heart beat in a specific time period or to tap along with their heartbeat. Another measure is the heartbeat discrimination task and it allows the individual to listen to tones and report whether they occur coincidently with their heartbeat or not. Secondly, how internal sensations are experienced by an individual is the subjective part of interoception, also referred to as interoceptive sensibility. This implies a subjective assessment of the belief the individual has in their interoceptive ability and the degree of engagement by interoceptive signals. There are two approaches to quantify interoceptive sensibility: 1) self-reported questionnaires and 2) a subjective score – often their confidence rating – during the performance of an interoceptive task. The last interoceptive aspect, metacognitive awareness, represents the relationship between the subjective and objective interoceptive ability. This can be assessed by averaging individual’s confidence ratings on an interoceptive task combined with the individual’s mean task accuracy. More sophisticated analytic
approaches such as the receiver operating characteristic (ROC) curves can also be applied to examine how confidence and accuracy are related in an individual.
After clearly differentiating the interoceptive aspects and their assessment methods, Garfinkel et al. (2015) determined to which extent the interoceptive aspects relate to each other by taking two measures for each aspect. Only relationships were observed in people with high interoceptive accuracy. In these individuals, interoceptive accuracy was the underlying central construct for interoceptive sensibility and interoceptive awareness. Interoceptive sensibility and interoceptive awareness were independent from each other. However, this approach has been evaluated because interoceptive accuracy sometimes correlated with interoceptive sensibility when measured with confidence ratings, whereas with self-reported questionnaires typically do not. Murphy, Catmur, & Bird (2019) therefore suggest to modify this existing three-dimensional model to a 2 × 2 factorial model of interoception with the first factor distinguishing whether accuracy or attention is measured and the second factor whether an objective performance or a self-reported belief is assessed. Although this critique, the three-dimensional model of interoception has been mainly used in studies examining the relationship between interoception and emotion (regulation). Furthermore, interoception has been mainly studied by heartbeat tasks, so these discrepancies between interoceptive aspects and the associated alterations in brain regions might be overcome by focusing on the gut instead of the heart.
Interoception as a basis for emotion and emotion regulation
The relationship between the body and the brain has been considered progressively in neuroscience. Therefore, the relevance of interoception has been taken more into account in studies examining emotion. First indications that sensations from the body were involved in emotions came from studies in which people were asked to draw on bodily sensation maps where they felt activity changing when an emotion was induced by emotional stimuli (Jung, Ryu, Lee, Wallraven, & Chae, 2017; Nummenmaa, Glerean, Hari, & Hietanen, 2014). Every emotion had a distinguishable pattern of activation on the bodily sensation maps, varying from only changes along the gastrointestinal tract when feeling disgust to changes over the entire body for happiness. Moreover, when interoceptive accuracy – as measured by the heartbeat tracking task – was greater, individuals also showed a greater degree of bodily sensation in the pattern specific for that emotion and these changes were more specific (Jung et al., 2017). Event-related potentials (ERPs) could be measured to examine this relationship between interoceptive accuracy and emotion on an electrophysiological level, because greater P300 and subsequent slow wave amplitudes were found following emotionally arousing stimuli compared to neutral (e.g., Keil et al., 2002). When dividing participants based on their cardiac accuracy performance in a heartbeat detection task, good cardiac accuracy perceivers had significantly greater P300 and slow
wave amplitudes than poor cardiac accuracy perceivers in response to emotionally salient pictures (Herbert, Pollatos, & Schandry, 2007). Furthermore, they experienced the emotions more intensely. Source reconstruction revealed that both EEG components – P300 followed by the slow wave – were associated with activity coming from the insula, somatosensory cortex, prefrontal cortex and ACC (Pollatos, Gramann, & Schandry, 2007). These visceromotor regions are of importance for interoception, but were also found to activate during emotion-induction tasks in neuroimaging studies (Damasio et al., 2000; Terasawa, Fukushima, & Umeda, 2013). These regions are part of the salience network (Seeley et al., 2007) and it has been known as one of the seven large-scale distributed networks in the brain from which mental states emerge (Yeo et al., 2011). Oosterwijk et al. (2012) examined whether network activity patterns changed across three mental states, namely emotions, body feelings, and thoughts. The salience network was common in all three states but showed more activity during mental states of emotion and body feelings than thoughts. Therefore, these studies support the theories of bodily sensations underlying emotion by demonstrating that visceromotor regions associated with interoception were activated when emotion was induced.
Further studies showed the more specific role of the interoceptive cortex, the insula, during an emotional state. For example, experience of disgust was accompanied with tachygastric responses (rapid dysregulated gastric responses) in the gut and less parasympathetically influence on the heart (Harrison, Gray, Gianaros, & Critchley, 2010). These visceral changes predicted anterior insular activity, demonstrating that bodily feelings are critical for subjective experience of emotions. In another fMRI study, the anterior insula was activated during both emotion-inducing videoclips and during a heartbeat monitoring task (Zaki, Davis, & Ochsner, 2012). It suggested that the anterior insula has a functional overlap in emotional and bodily experiences. This was confirmed by a meta-analysis by Kurth et al. (2010). Indeed, activation of the anterior insula was found in studies examining interoception but also in studies examining emotion and therefore they concluded that the anterior insula acts as a multimodal integration region. How the anterior insula integrates information from different modalities was especially shown in a study that used dynamic causal modelling to examine the neural mechanisms (Nguyen, Breakspear, Hu, & Guo, 2016). During free listening to an emotionally salient audio film, participants’ cardiac activity synchronised with the emotional moments in the film. The cardiac activity was correlated with posterior insular activity, whilst the anterior insula integrated these interoceptive representations with exteroceptive sensory information from the superior temporal gyrus (involved in auditory processing). When the cardiac activity increased, the influence of the superior temporal gyrus was also upregulated, indicating that interoception can also affect emotion processing by enhancing relevant exteroceptive information.
The abovementioned studies made use of heartbeat tasks and since each subregion in the insula has a representation of all distinct sensations, this could imply that sensations from the gut can
likewise sensations from the heart, influence emotion processing. Because appropriate identification of emotion is necessary for emotion regulation (Berking & Whitley, 2014; Gratz & Roemer, 2004), the gut could have an effect via the homeostatic afferent system. Moreover, it is as expected that the insula is involved in emotion considering the posterior-to-anterior progression in the insula, because interoceptive information is integrated in the insula with emotional, motivational, and social conditions coming from other visceromotor regions (Craig, 2009). These regions have evolved to continuously observe and regulate one’s physical condition of the body. Recent theories therefore suggest that the visceromotor regions responsible for homeostasis support emotional feelings by integration of interoceptive and exteroceptive information as a basis (Craig, 2003, 2009; Critchley & Harrison, 2013; Damasio, 2003; Feldman Barrett, 2017; Park & Tallon-Baudry, 2014; Seth & Friston, 2016; Strigo & Craig, 2016). In other words, emotions might function to help maintain homeostasis. This implies that an appropriate emotion regulation would also be beneficial for one’s physical condition of the body.
The influence of interoception on emotion regulation has mainly been examined by means of questionnaires. However, one study measured ERPs to investigate whether greater interoceptive accuracy is associated with a more appropriate regulation of negative affect, the so-called reappraisal strategy (Füstös, Gramann, Herbert, & Pollatos, 2012). As shown before, negative affect led to more arousal accompanied with greater amplitudes in P300 and the subsequent slow wave (Herbert et al., 2007). Once the appraisal strategy was applied, arousal and the corresponding ERP components decreased. Moreover, greater interoceptive accuracy as measured with the heartbeat tracking task, facilitated the downregulation of affect and thereby the modulation in ERP components. These components correspond to activity in the insula and ACC, part of the interoceptive system, confirming that higher interoceptive accuracy relates to appropriate emotion regulation. Besides reappraisal, suppression is another emotion regulation strategy. Whether interoceptive accuracy was associated with the habitual use of either reappraisal or suppression was examined by individuals undergoing a heartbeat tracking task and completing the Emotion Regulation Questionnaire (Kever, Pollatos, Vermeulen, & Grynberg, 2015). Individuals with higher interoceptive accuracy showed greater use of both emotion regulation strategies compared to those with lower interoceptive accuracy. These results were not as expected, because reappraisal is often seen as adaptive whereas suppression as a maladaptive strategy. Kever et al. (2015) argued that suppression might be adaptive in certain social situations and that greater interoceptive accuracy might facilitate emotion regulation because better perception of bodily changes might ease modulation regardless of strategy. This also corresponds to the interaction found between self-regulation and interoception. Self-regulation implies the trait to override or alter our responses, including emotion regulation but also decision making for instance. Self-regulation was examined with the Hannover Self-Regulation Inventory and interoceptive accuracy
with a heartbeat tracking task. Greater interoceptive accuracy was associated with better self-regulation capacities (Weiss, Sack, Henningsen, & Pollatos, 2014). Furthermore, they also examined self-regulation in somatoform patients, people with more than three unexplained symptoms that have been present for more than two years. These patients exhibited reduced interoceptive accuracy and reduced self-regulation capacities. These studies demonstrate that greater interoceptive accuracy accompanies appropriate emotion regulation.
Interoceptive sensibility has also been investigated aside from interoceptive accuracy. First study by Zamariola, Frost, Oost, Corneille, & Luminet (2019) hypothesized that individuals with better interoceptive accuracy and sensibility would implement more adaptive strategies than maladaptive strategies. By means of qualitative and quantitative measures (heartbeat tracking task and interviews, respectively), people with low interoceptive abilities were less able to cope with negative experiences and verbalizing them. Continuing their research with a bigger sample population, they examined the influence of interoceptive accuracy (measured with a heartbeat tracking task) and interoceptive sensibility (assessed by the Body Awareness Questionnaire) on coping with negative affect (Zamariola, Luminet, Mierop, & Corneille, 2019). The results were inconsistent with their first study showing that there was no interaction between emotion induction and any measure of interoception. There was marginal evidence that a higher interoceptive sensibility was accompanied with more negative affect. They argued that the heartbeat tracking task might not be an appropriate measure for interoceptive accuracy as all individuals performed poorly. This seems to be confirmed by the following study in which the relationship between interoceptive accuracy, interoceptive sensibility and emotion identification and regulation was also explored (Schuette, Zucker, & Smoski, 2020). The same heartbeat tracking task was used as in Zamariola, Frost, et al. (2019) and Zamariola, Luminet, et al. (2019) to measure interoceptive accuracy. Questionnaires were completed for interoceptive sensibility (Multidimensional Assessment of Interoceptive Awareness), emotion identification and regulation (Profile of emotional competence), and coping strategies (brief COPE). Interoceptive accuracy was not related to any outcome measures in this case either. However, interoceptive sensibility had a positive relationship with emotion identification and emotion regulation. This implied that emotion identification mediates the relationship between interoceptive sensibility and emotion regulation.
In this section, studies examining the relationship between interoception and emotion were first discussed. Theories about how information from the body can constitute an emotion to neuroimaging studies showing the role of visceromotor regions in emotion induction clearly indicate that interoceptive information is critical for emotion processing. Interoceptive accuracy seemed to enhance activity in visceromotor regions when emotions were induced. Although emotion processing is crucial for emotion regulation, it is ambiguous how interoceptive accuracy relates to the use of emotion regulation strategies. However, interoceptive sensibility was positively related to emotion
regulation, suggesting that the subjective part of interoception might be more involved in emotion regulation than the objective part. As previously mentioned, interoceptive accuracy and interoceptive sensibility were sometimes related depending on how interoceptive sensibility was measured and therefore a 2 × 2 factorial model was proposed (Murphy et al., 2019). Considering that most studies make use of heartbeat tasks, cardiac interoception might not be the appropriate interoceptive channel to study emotion and emotion processing. Individuals perform poorly on heartbeat tasks and in daily life we are not much aware of our heartbeat. Therefore, the gut might have a bigger potential since we perceive more (consciously) signals from the gut, like hunger, bloating and fullness.
The potential pathways of the gut to intervene with emotion processing
Like other internal systems, the gut sends interoceptive signals to the brain. Unlike other systems, the gut or also called the gastrointestinal tract is a massive system consisting of the tract from the mouth to the anus and involves all organs that are necessary for digestion. Such a complicated system involves numerous events in order to have successful digestion and absorption (Rao & Gershon, 2016). The brain can influence the gut’s function and similarly, the gut can also send information to the brain. This bidirectional communication is called the gut-brain-axis and within this axis exist many systems through which the brain and gut can interact with each other. For this review, the relevant systems will be discussed to understand the influence of the gut on emotion processing.The gut has a tremendous number of functions to execute digestion and so, the gut has its own nervous system to regulate and coordinate digestion, the so-called enteric nervous system (ENS). It is referred to as the second brain because it can control gastrointestinal behaviour without any input from the brain. Furthermore, it contains over more than 100 million neurons that communicate with practically every neurotransmitter that has been found in the brain too (Furness, Callaghan, Rivera, & Cho, 2014). As the ENS resembles the brain in terms of structure and neurochemistry, dysfunction in the brain might lead to dysfunction in the ENS and vice versa (Rao & Gershon, 2016). This could be the case for affective, neurological and neurodegenerative disorders (Breit et al., 2018; Cryan & Dinan, 2012; Cryan et al., 2019).
The number of neurons in the ENS might be astonishing but pales in comparison to the amount of microbiota present in the gut. (Cryan & Dinan, 2012). There are three main types of microbiota: Bacteroides, Prevotella, and Ruminococcus and they are involved in the metabolism and digestive absorption of nutrients. Some nutrients cannot be metabolised by the gut itself and therefore we depend on the microbiota (Liang, Wu, & Jin, 2018). Together, we live in a symbiose and in order to survive, microbiota can interact with other systems in the gut-brain axis and so influence the brain (Carabotti, Scirocco, Maselli, & Severi, 2015). The other way around, the brain can influence the gut microbiota either. Therefore, dysfunction of microbiota cannot only affect the digestive system, but
also affects other systems in the gut-brain axis and so even the brain and behaviour, which could be a factor in pathophysiology of disorders (Cryan et al., 2019).
Another crucial pathway is the autonomic nervous system which consists of the sympathetic and parasympathetic nervous system. The brain influences the gut through sympathetic innervation from the spinal ganglia by inhibiting gastrointestinal function whereas parasympathetic innervation stimulates the gut stimulated (Mayer, 2011). The main input and output via the parasympathetic nervous system is via the vagus nerve, of which 90% of the fibres are afferent, suggesting that the brain receives more information than it transmits to the gut (Rao and Gershon, 2016). Besides the parasympathetic vagus nerve, the gut can also communicate with the brain via the sympathetic spinal primary afferent neurons (Mayer, 2011; Cryan et al., 2019).
The abovementioned systems communicate mainly through electrochemical neurotransmission, which is rather quick and direct. Given that emotional states last only for a few seconds to minutes and we transition easily through emotional states throughout the day (Ekman & Davidson, 1994), these fast pathways are likely to affect emotion and emotion regulation. Other systems in the gut-brain axis depend mainly on the blood circulation and would therefore be too slow to intervene with emotion regulation. For the completeness of this overview, the remaining systems in the complicated gut-brain axis will be briefly mentioned. One of these systems is the immune system, which main role is to protect the visceral tissue from microbiota and other harmful pathogens. Furthermore, the immune system can also identify changes in the gastrointestinal environment in order to sustain the homeostatic balance. The enteroendocrine system is also important for the maintenance of homeostasis and it establishes this by secreting signalling molecules. The hypothalamic-pituitary-adrenal axis is the main neuroendocrine system and its primary function is the response to stress and to prime the body for the ‘fight or flight’ response. Other means of communication between the gut and the brain are with neurotransmitters, branched chain amino acids, bile moieties, short chain fatty acids, and peptidoglycans (see for a review Cryan et al, 2019).
Emotion-induced changes from the brain to the gut are likely mediated by subsets of postganglionic sympathetic and parasympathetic neurons (Almy, Kern, & Tulin, 1949; Welgan, Meshkinpour, & Beeler, 1988). They induce an emotion-specific pattern of changes in the gut in a similar way as distinct facial expressions and body postures are seen for each emotion. Eventually, these emotion-specific changes will affect the interoceptive feedback to the brain, consequently prolonging the duration of an emotional state. If the alterations are prolonged for a very long time, they will change the gut and so the gut-to-brain signalling chronically, which could lead to altered emotional states such as anxiety disorders or depression. This suggests that it is of importance to examine the role of the gut in emotion and to examine whether interoceptive information of the gut could possibly affect emotion regulation.
The role of the gut-brain axis in emotion
Although the gut continuously sends interoceptive signal to the brain, only a small fraction is perceived consciously (Mayer, 2011). Despite this small part, gastric interoceptive accuracy is likely to be as good as or better than cardiac interoceptive accuracy. It has been shown that better heartbeat perception is accompanied with better gastric perception (Herbert, Muth, Pollatos, & Herbert, 2012). In this experiment, gastric perception was measured by the amount of ingested water an individual could drink to feel satiated. Satiation is one of the interoceptive sensations that can be consciously perceived. Other gut sensations are fullness, hunger, discomfort, pain, and nausea (Mayer, 2011). Although not an interoceptive sensation, sounds are also relevant for awareness of the gut. As demonstrated in an experiment where participants learnt with biofeedback training to control their gastric motility, individuals who used both feeling of abdominal tightening and listening to abdominal sounds accomplished to fulfil this task more than individuals that used only one of the sensations (Whitehead & Drescher, 1980). Even though only a few gut sensations are consciously perceived, they indicate to the brain that action is necessary for homeostasis and this usually requires a conscious behavioural response (Mayer, 2011). In other words, gut sensations may induce the emotional state for homeostasis of the gut; by being aware of one’s emotional state, a behavioural response is required to regulate the emotional state but also the gut state.
In order to examine the interoceptive signals of the gut on emotion (regulation), a variety of methods have been developed to measure gut interoception. First of all, gastric myoelectrical activity can be measured with electrogastrography (EGG). Activity increases after eating, sham feeding or when expected to eat pleasant food. Dysrhythmia can also occur (bradygastria and tachgastria) and this is associated with the feeling of nausea and vomiting. As EGG is an objective measure, it has been suggested that it could be used as biofeedback to make people more conscious of their internal state and thus improve their emotion regulation (Mladenović, 2018). Another measure of gut interoception is gastric balloon inflation and deflation (Stephan, Pardo, & Faris, 2003). This requires the placement of a balloon in the stomach and it can be used to examine short-term satiety. Individuals reported that with inflation the feeling of hunger decreased and the feelings of sleepiness, fullness, nausea, and gastric discomfort increased. This task combined with fMRI demonstrated that different visceromotor regions activate, such as the insula and the ACC, confirming indeed that the gut has a representation in the interoceptive brain. Since placement of a gastric balloon takes an extensive procedure and feels uncomfortable, it is not ecologically valid and therefore the water load test has been opted as a replacement. The task entails to either drink the same amount of non-caloric water or caloric drink in a few sessions of a fixed amount of time. After each session, the subjective fullness is rated (Boeckxstaens et al, 2001). A different way to test this is the two-step water load test in which the first
step is to drink non-caloric water until the feeling of satiation and the second step is to drink until maximum fullness (van Dyck et al., 2016). An individual index of gastric interoception can be calculated because it is not confounded by stomach capacity. The last method that will be described here is the interoceptive attention task. Individuals are asked to focus on either the stomach, bladder or heart. Previous research has indicated that focus on a perceptual modality strengthens the activity in the modality-specific brain regions (Jancke et al, 1999; Johansen-Berg et al, 2000; Somers et al, 1999).
With these possible methods to examine the relationship between the gut and emotion, the studies are nonetheless diverse because the focus can be on any of the systems involved in the gut-brain-axis. One of the first studies investigated the relationship between the gut and emotion by presenting negative emotional stimuli while receiving phasic oesophageal stimulation (Phillips et al., 2003). Increased activity was found in the ACC and insula for negative over neutral emotional context. This activity was enhanced in combination with oesophageal stimulation accompanied with increased subjective ratings in anxiety and discomfort. This study indicated that a sensation from the gut in a negative context could increase attentional and emotional processing as shown with the increased activity in the ACC and insula, corresponding to a more intense feeling of that emotional state.
The microbiota’s role was also examined in emotion. Tillisch et al. (2017) investigated whether the microbiota composition was associated with differences in brain structure and function when undergoing an emotion induction task. Individuals were clustered based on their microbiota composition into two groups (Bacteroides and Prevotella). The group with a greater abundance of Prevotella was associated with a heightened negative affect together with functional and structural differences in the hippocampus. The hippocampus – involved in emotion regulation – had a lower volume and less BOLD response during viewing of negative images. Another way of showing the effects of microbiota is by taking probiotics: microbiota that are claimed to have health benefits. Participants consumed the probiotics in the form of a fermented milk for 4 weeks to examine whether it would alter brain connectivity in response to emotional stimuli and during rest (Tillisch et al., 2013). The probiotics had widespread effects on the brain showing reduced activity in interoceptive and somatosensory cortices, frontal, prefrontal, and temporal cortices, parahippocampal gyrus, and the PAG. The PAG was found to be the center in a resting-state network connected to interoceptive, affective, and prefrontal regions. These results suggested that these changes are either induced by metabolic changes related to the probiotics or via altered afferent signalling to the NTS. The NTS transmits information to the PAG and connected brain regions or as previously mentioned, the homeostatic afferent system, responsible for interoception.
Shortly mentioned before, microbiota can break down nutrients that are indigestible by the host. These metabolites are called short-chain fatty acids and one of the pathways in the gut-brain axis. Whether these short-chain fatty acids had an effect on emotion was examined at both
behavioural and neural level by a subliminal intragastric infusion of the fatty acids during negative emotion induction while undergoing fMRI (Van Oudenhove et al., 2011). An interaction was found between fatty acid infusion and negative emotion induction at the level of brain and behaviour. Fatty acid infusion reduced the ratings of hunger, fullness and mood and activity in pre-hypothesized brain regions such as the medulla/pons, midbrain, hypothalamus, striatum, hippocampus, and ACC. No significant effects were found in the amygdala and insula and it was reasoned that these regions were not activated because subliminal infusion does not reach consciousness. Zhao et al. (2019) tried to replicate similar findings with positive emotion induction instead of negative emotion induction and only at the behavioural level. However, they did not find any influence of the fatty acid infusion on emotion induction, what makes one doubt the effect of short-chain fatty acids on emotion.
Lastly, serotonin is one of the neurotransmitters that serves both a function in the brain and the gut. Decreasing the availability of its precursor tryptophan with a method called acute tryptophan depletion (ATD) enhanced changes in activity in the homeostatic afferent network (insula and ACC) and emotional arousal network (pons and amygdala) that resulted from balloon inflation in the rectum (Labus et al., 2011). During balloon inflation, ATD engaged the emotional arousal network more than a placebo. This suggests that during an aversive interoceptive stimulus, ATD reduced feedback inhibition of the amygdala.
Overall, these neuroimaging studies demonstrate that the gut-brain axis is involved in emotion by altering activity in the homeostatic afferent network, from lower levels such as the PAG to higher levels like the ACC and the insula. The gut-brain axis can mediate these effects via the enteric nervous system, autonomic nervous system and microbiota as already suggested. The results regarding the short-chain fatty acids effect on emotion might be inconsistent because short-chain fatty acids depend on the blood circulation and this might be too slow to mediate emotion. Overall, manipulating a system in the gut-brain axis leads to alterations in the homeostatic afferent network, it shows indirectly that gut interoception influences emotion processing.
Gut interoception and emotion regulation in disorders
In the previous section I discussed how different systems in the gut-brain axis could affect emotion. Here I will continue by reviewing literature that has investigated the influence of the gut-brain axis on emotion regulation, which has primarily been examined in disorders.
Interoceptive deficits have been investigated in major depressive disorder to observe whether this is associated with abnormal insula function (Avery et al., 2014). With the use of the interoceptive attention task during fMRI, reduced dorsal mid-insula activity was found during attentional focus on interoceptive signals broadly (the stomach, the bladder, and the heart). Moreover, the more reduced the activity was in the mid-insula, the more severe depression and somatic symptoms were. This
suggested that people with major depressive disorder have a distorted perception of their bodily sensations, having a higher sensitivity to signals that might not be relevant or harmful for one’s homeostatic state. Similar findings have been found in anorexia nervosa patients, where activity in the dorsal mid-insula was also decreased during stomach interoception (Kerr et al., 2016). Besides, less average activity was found in the precuneus – involved in mental self-representations – for anorexia nervosa patients compared to controls. Both results suggest that an aberrant interoception and self-representations are contributors to the pathophysiology in anorexia nervosa. Instead of decreased mid-insula activity during interoception as found in major depressive disorder and anorexia nervosa, increased connectivity was found between the anterior insula and supramarginal gyrus with higher interoceptive awareness for patients with irritable bowel syndrome (Longarzo et al., 2017). These connections probably occurred as a consequence of increased attention towards sensations from the gut in these patients. A second finding was a negative correlation between interoceptive awareness and connectivity between the precuneus and the supramarginal gyrus, indicating that strong concerns about one’s health might reduce the ability to perceive bodily sensations for efficient regulation of one’s emotions. Zvolensky et al. (2018) evaluated whether interoceptive sensibility of adults with a history of gastrointestinal symptoms and disorders was related to their emotion regulation. It was indeed found that individuals with gastrointestinal symptoms had higher interoceptive sensibility and this was related to emotional dysregulation, leading to anxiety and depressive symptoms. Emotion dysregulation was also found in obese people (Willem et al., 2019). They had less adaptive emotion regulation, less emotional awareness and less interoceptive awareness than normal-weighted people. Obese people were less attentive to their bodily states and had a greater difficulty noticing it than normal-weighted people. These results suggest that an appropriate interoception is necessary for emotional states and thereby emotion regulation.
Considering that the vagus nerve is the main parasympathetically pathway in the gut-brain axis and consists for 90% of afferent connections, it is an attractive target to treat affective and gastrointestinal disorders. Interoceptive deficits have been found in major depressive disorder and posttraumatic stress disorder (Avery et al., 2014; Reinhardt et al., 2020) and therefore vagus nerve stimulation has been suggested as a treatment (Breit et al., 2018). The stimulation of vagal afferent fibers in the gut connect to the NTS and can thereby alter activity in many subcortical and cortical regions that are part of the homeostatic afferent system and regulate emotion and mood. Furthermore, vagus nerve stimulation influences monoaminergic brain systems in the brain stem. These important mechanisms reduce depressive symptoms and PTSD symptoms. In line, preliminary evidence in mice show that probiotics can have a beneficial effect on emotion regulation and anxiety (Breit et al., 2018; Cryan et al., 2019). Moreover, microbiota have been related to a growing list of other affective disorders, such as bipolar disorder and attention deficit hyperactivity disorder (Cryan
et al, 2019). These findings mainly rely on studies in mice and rats and as it is difficult to study emotion regulation in these animals, it is out of the scope of this review. All things considered, it is suggested that the gut-brain axis is able to influence emotion regulation via the vagus nerve and the homeostatic afferent system.
Discussion
In this review, I first gave an overview of interoception and its relationships to emotion and emotion regulation. Interoception is a crucial vital process for homeostasis; to control the body’s physiological condition. The homeostatic afferent system has been described in great detail, with the insula seen as the main interoceptive cortex, showing a representational map of all distinct internal bodily sensations. Together with the anterior cingulate cortex and the orbitofrontal cortex, these visceromotor regions are important to become aware of bodily feelings and constitute emotional feelings too. Early theories by James (1884) and Damasio (1999) to more recent theories like Feldman Barrett’s (2017) and neuroimaging studies have confirmed that interoceptive signals arise emotional states.
As interoception is in involved in emotion processing to regulate homeostasis, one might consider that emotion regulation is not only relevant to regulate one’s emotional state but also one’s physiological condition of the body (Damasio, 2003; Feldman Barrett, 2017). When evaluating findings about interoception and emotion regulation, there are discrepancies between the objective and subjective part of interoception. Some earlier studies did find that a better interoceptive accuracy (objective) was related to better emotion regulation (Füstös et al., 2012; Kever et al., 2015; Weiss et al., 2014), but later studies did not replicate this (Schuette et al., 2020; Zamariola, Frost, et al., 2019; Zamariola, Luminet, et al., 2019). However, interoceptive sensibility, the subjective part of interoception, seemed to have a positive relationship with emotion regulation (Schuette et al., 2020; Zamariola, Luminet, et al., 2019). It has been critiqued before that interoceptive sensibility and interoceptive accuracy seem to be related depending on the measure of interoceptive sensibility (Murphy et al., 2019). Furthermore, interoceptive accuracy in these studies was examined by heartbeat tasks and individual performances were rather poorly, which could be explained by the unawareness of one’s own heartbeat (Zamariola, Luminet, et al., 2019). Because of inconsistencies between the relationships of different aspects of interoception when measured with heartbeat tasks, another interoceptive sensation such as sensations from the gut could be a potential way to investigate the role of interoception in emotion and emotion regulation.
Sensations from the gut such as hunger and fullness arise from the gut-brain axis. The gut needs a load of regulation to be able to control such a complex system and therefore the gut-brain axis consists of many pathways through which the gut and the brain can interact (Rao & Gershon, 2016).
The enteric nervous system, the autonomic nervous system and the microbiota could alter the homeostatic afferent system and, in some cases, the emotional arousal network during emotion induction (Labus et al., 2011; Phillips et al., 2003; Tillisch et al., 2013, 2017). Only the role of short-chain fatty acids seems questionable, but fatty-acid mediated effects on emotion might be too slow as emotions arise and go in seconds to minutes. Microbiota on the other hand, can directly affect the enteric and autonomic nervous systems, which have fast neurotransmission (Cryan et al., 2019).
The vagus nerve appears to be the crucial pathway in the relationship between gut interoception and emotion regulation. Studies concerning disorders showed that aberrant interoception was accompanied with alterations in activity in the homeostatic afferent network (Avery et al., 2014; Kerr et al., 2016; Longarzo et al., 2017; Willem et al., 2019; Zvolensky et al., 2018). Furthermore, this is characterized by emotion dysregulation. Preliminary evidence with vagus nerve stimulation and microbiota that possibly influence the vagus nerve, have shown to mitigate mood and anxiety symptoms in affective disorders such as depression and posttraumatic stress disorder (Breit et al., 2018; Cryan et al., 2019).
Nevertheless, the research in the role of interoception of the gut on emotion regulation could be extended, as it has been mainly investigated in affective and gastrointestinal disorders. Furthermore, studies about gut interoception did not examine interoception in accordance to the three-dimensional model suggested by Garfinkel et al. (2015). Interoceptive accuracy as assessed by heartbeat tasks might not be similar to gastric distension. Although both measurements are objective, counting the number of times one’s heart beat is not comparable to the judgment of how full one feels. Moreover, the interoceptive attention task seemed to be favoured when assessing gut interoception and it does not fit to any aspect in the three-dimensional model of interoception, although it would in the 2 x 2 factorial model by Murphy et al. (2019). It would therefore be compelling to measure different interoceptive sensations and examine how they correlate to emotion regulation. Recently, it has been proposed to examine whether it is possible to improve emotion regulation by practicing differing forms of interoception (Davey, Bell, Halberstadt, & Collings, 2020). Individuals will follow an 8-week intervention in which 20 mins per day, 6 days a week they will be asked to focus on either sensations of the chest area or the lower abdomen.
To conclude, the gut-brain axis is not solely to mediate gastrointestinal homeostasis, but also to connect to emotional and cognitive brain areas and even regulate emotion. The gut-brain axis is crucial from the first step in emotion regulation, to correctly identify an emotion, to the last step, the appropriate emotional response. The gut-brain axis is a perfect example of a complex system involving different pathways between the body and the brain to show how interconnected the body and the brain actually are. Thus, the most suitable emotional response could be to follow your gut feeling.
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