Interoception

Individuals, who have difficulty recognizing and verbalizing emotions, also experience problems with identifying and differentiating body conditions and functions such as heartbeat, breathing, body temperature, fatigue, hunger, thirst, satiety, muscle tension or pain [5]. Research demonstrates that the mechanism responsible for our emotional awareness significantly overlaps with the neural systems supporting our interoceptive awareness (IA) [6–11]. Craig [6, 7] suggested an broad approach to interoception as a system for perceiving somatic sensations such as heart rate, respiratory effort, fatigue, hunger, thirst, satiety, but also temperature, muscle tension, pain or itching (most frequently considered as exteroceptive information), as well as the representation of internal condition in the context of current activities [8]. Interoception refers to the ability to accurately perceive internal bodily processes, which comprise receiving, processing, and integrating body-relevant signals, together with external stimuli. Individual differences in interoception can be divided into three distinct dimensions: interoceptive accuracy (performance on objective tests of interoceptive accuracy), interoceptive sensibility (self-reported beliefs concerning one’s own interoception) and interoceptive awareness (a metacognitive measure indexed by the correspondence between interoceptive accuracy and interoceptive sensibility) [10, 11]. The notion of interoceptive accuracy describes our capacity for identifying internal body sensations, whereas the notion of interoceptive sensibility applies to our capacity for focusing on internal sensations and to take them into consideration, also from a cognitive point of view. In the light of present studies, interoception is associated with experiencing emotions, processing emotional stimuli, and activation of brain structures responsible for monitoring signals which come from the body, indicating the physiological and emotional condition [12]. There is increasingly more empirical evidence showing interoception as the basis of motivation, emotions, social cognition, and human self-awareness [5].

Alexithymia and emotional dysregulation

Alexithymia, as found by many studies, is linked to non-secure attachment, especially emotional neglect in early childhood [13]. The exchange and social relationships in early life are essential for the emotional development of a child and later an adult. Schore [14] claims that especially important is the impact of attachment communication on the development of the right hemisphere involved in emotional processing, dealing with stress, self-regulation and shaping bodily-based implicit self. In the case of non-secure attachment, it is not only the disturbed psychological and emotional development, as has been pointed out so far, but also the inappropriate neurobiological development [14]. Experiences in a period critical for the development of a child’s brain are encoded in rapidly developing right hemisphere (its frontal area in particular), affecting the ability to process negative emotions [15] or establishing a satisfactory relation between outside world and the self [16]. It is imperative to relate the child and caregiver to mutual responsiveness that takes the form of emotional tuning of the parent and child. Extremely important in this process are co called signified emotional responses, which mean that a parent adjusts to the child’s emotional condition, expressing the same emotion but supplemented by signals which indicate that it is the reflection of the child’s condition, and not the expression of the parent’s pure emotions. The repetition of such situations enables the child to develop their own sense of Self, in particular, the awareness of own emotions. Those “signified” parent’s emotional responses are fundamental to the development of the child’s ability to accurately differentiate the physiological correlates of emotions, name emotions and regulate emotions. Experiencing a parent as unavailable and insensitive to the signals coming from the child for many years results in feeling chronic negative emotions, such as fear, anger or sadness. It is alexithymia that constitutes a persistent personality factor fostering deficits in the cognitive analysis of emotional arousal.

The main characteristics of alexithymia include (1) difficulty identifying feelings and distinguishing between feelings and bodily sensations of emotional arousal, (2) difficulty describing feelings to other people, (3) reduced capacity to fantasize and to imagine, (4) stimulus-bound, externally oriented cognitive style [17, 18], and, more recently, (5) low perspective-taking, as well as difficulty understanding and describing the emotions of others [19]. Emotion dysregulation includes difficulties in identifying and describing feelings, difficulties in distinguishing feelings from the bodily sensations of emotional arousal, impaired symbolization, as evidenced by the scarceness of fantasies and other imaginative activity, and a tendency to focus on external events rather than inner experiences (specific thought). According to Gratz and Roemer [20] emotional dysregulation is a multi-faceted construct involving: a lack of awareness, understanding, and acceptance of emotions; a lack of access to adaptive strategies for modulating the duration and/or intensity of aversive emotional experiences; an inability to control behaviors when experiencing emotional distress; and an unwillingness to experience emotional distress. It has also been conjectured that failure to experience complex emotional states is associated with exaggerated or dysregulated autonomic activation [21].

People who have difficulty processing their negative and positive emotions are more vulnerable to developing psychopathological symptoms [22]. One of the mechanisms that may be responsible for the above is the asymmetry typical of people with high levels of alexithymia in experiencing negative over positive emotions. Negative emotions include anxiety, fear, contempt, disgust, anger, irritability, guilt or depression [22]. It is worth adding that individual differences in relation to negative vs. positive asymmetry are stable over time and trans-situational [22]. As a consequence, this entails problems with the regulation and self-regulation of emotions. As was noted above, an essential assumption underlying alexithymia theory is the fact that alexithymic individuals lack mental representations of emotions due to a deficit in the cognitive processing of these [23, 24]. The alexithymic individuals have limited capacities to use cognitive mechanisms to understand and regulate emotions lead them to focus on, amplify and misinterpret the bodily sensations accompanying emotional arousal. Porcelli and Taylor [25] have suggested that a failure to regulate and modulate stress-related emotions at the cognitive level may result in exaggerated physiological and behavioral responses to stressful situations and an increased vulnerability to disease [26].

Several studies indicate that one of the neuronal correlates of alexithymia is reduced neuronal activity in the emotional attention system, which includes the amygdala, fusiform gyrus and occipital cortex. Since the amygdala is involved in triggering emotional reactions and initiating ANS changes [25] the reduced activity of the amygdala in response to emotional stimuli will lead to a limited physiological response and disturbed somatosensory remapping. Persons who have difficulty identifying feelings may also have less access to information coming from the body, on which they could base spontaneous emotional reactions [26]. Kano et al. [27, 28] showed that persons with high levels of alexithymia present higher levels of anxiety and higher levels of adrenaline during visceral stimulation than people without alexithymia. The authors hypothesized that alexithymic individuals are more sensitive to unpleasant sensations from the body, and their higher autonomic reactivity is manifested in the increased activity of the right insula.

Interoception, alexithymia and dysregulation emotion

In accordance with the adopted approach, factors, which foster somatization, include impairment interoception and alexithymia, understood as a disturbance in cognitive analysis and reinterpretation of stimuli both from the body and from the environment, as well as emotion dysregulation favoring the condition of continuous, chronic agitation of organism. An individual, who is unable to handle the excess of uninterpretable somatic conditions, high level of affective arousal, may cope using maladaptive defense mechanisms. Alexithymia may compound maladaptive behaviors. Such role of alexithymia has long been emphasized by Porcelli and Taylor [25] and by Lane [29]. A recent meta-analysis by De Gucht and Heiser [30] has demonstrated a small to moderate association between alexithymia and different self-report measures of somatization (e.g., health complaint scales; reflect = 0.23). The existing studies examining alexithymia in patients with somatoform disorders have yielded generally consistent evidence of increased levels of alexithymia in somatoform disorders.

Brewer et al. [31] investigated the association between alexithymia and self-reported non-affective interoceptive ability, as well as the extent to which people perceive a similarity between affective and non-affective states, in both control individuals and individuals reporting a diagnosis of a psychiatric condition. The findings showed that alexithymia was related to poor non-affective interoception and increased perceived similarity between affective and non-affective states, in both normal and clinical populations. Those with alexithymia not only have difficulty recognizing their own emotions (affective interoception) but also confuse these states with non-affective interoceptive states, such as hunger, tiredness, and arousal.

Numerous studies [32–35] have supported the coexistence of impairment interoception and alexithymia in the context of somatosensory amplification, i.e. exaggerated sensibility and excessive concentration on somatic sensations, and their misinterpretation [32] Messina et al. [33] indicate that the reception of body signals in alexithymia may be related to somatosensory amplification (SA). SA has been characterized as: 1) excessive attention and hyper-vigilance to somatic symptoms; 2) exaggerated sensitiveness to physical sensations; 3) misinterpretation of physical sensations interpreted as a sign of disease. Somatosensory amplification and somatization are generally associated with difficulty identifying and describing feelings (but less so with externally oriented thinking style) [33].

Barsky [34] defines this phenomenon as a tendency to feel the body tense, and its condition distressing, as well as an individual’s tendency to focus on unpleasant somatic sensations, assign them a more pathological meaning than it actually is, and interpret them as the evidence of disease conditions. Such mechanism may operate on a vicious circle basis, thereby reinforcing deficits typical for alexithymia, i.e. difficulty in identifying and naming the sensations, leading additionally to the condition of chronic ANS arousal, impairment interoception. Dragoş and Tănăsescu [35] emphasize that the phenomenon of somatosensory amplification occurring in alexithymic individuals is strongly related to the mechanism of somatization, which, in their opinion, may be perceived as a cognitive disorder resulting from excessive perception of body sensations and their cognitive interpretation as a sign of disorder. The individual perceives many situations as threatening, which leads to chronic ANS arousal, hormonal stimulation, and it may finally result in further health problems. Typical for this type of somatic disorders is high variability of symptoms that a suffering individual complains about. Ailments may last for years and originate from different systems: digestive, cardiovascular, genitourinary, as well as they frequently affect skin, muscles and joints. They may include such symptoms as accelerated heartbeat, excessive sweating, dry mouth, flushing, gastrointestinal disorders, difficulty breathing, and chest discomfort. Typical for many persons is also persistent psychogenic pain, i.e. pain which may persist for numerous months, but cannot be explained by any disease process within the body.

Alexithymia, interoception and autism spectrum disorders

Autism Spectrum Disorders (ASD) is a neurodevelopmental disorder characterized by difficulties with social communication and interaction, and restricted or repetitive patterns of behavior or interests [1]. Following the publication of the DSM-5 [1], a view of and approach to autism was developed positing it on a spectrum, no longer seen as a categorical condition. The term ‘spectrum’ is used for the reason of the heterogeneity in the presentation and severity of ASD symptoms, as well as in the skills and level of functioning of individuals with ASD [36]. It is now clear that genetic factors play a predominant role in its etiology [37]. Persons with autism spectrum present difficulties in social communication, which, according to many researchers, is related to deficits in emotion processing. This particularly refers to recognizing emotions in others or a decreased level of empathy [38]). Hill, et al., [39] have also supported that individuals with autism spectrum disorders have significantly greater difficulties in identifying and naming emotions than persons from general population.

A study by Leonardi et al., [40] found that parents of children with ASD show higher level of alexithymia, as measured with Toronto Structured Interview for Alexithymia, than children of neurotypical parents. Alexithymia, disrupting the appropriate recognition and understanding of emotions, including those expressed by facial expression, results in the misuse of emotions as important sources informing about the mental state and relationships with other people, and thus contributes to an increase in the number of stressful and stress-inducing situations. A significant amount of data indicates a relationship between alexithymia and interoception [31] also in relation to persons with autism [41]. At the anatomical level, alexithymia and interoception are associated with impairment functioning of the same brain areas: insular cortex and cingulate cortex–the processing of emotions and the processing of interoceptive signals take place within the same neural system [31].

Researchers suggest that the impairment of interoception processes in ASD is caused by abnormalities in the way current experience updates predictions for the future [42]. Garfinkel et al. [11] demonstrated that individuals with ASD have reduced interoceptive accuracy (quantified using heartbeat detection tests) and exaggerated interoceptive sensibility (subjective sensibility to internal sensations on self-report questionnaires), reflecting an impaired ability to objectively detect bodily signals alongside an over-inflated subjective perception of bodily sensations. The divergence of these two interoceptive axes can be computed as a trait prediction error. This error correlates with deficits in emotion sensibility and occurrence of anxiety symptoms. They believe that these results indicate an origin of emotion deficits and affective symptoms in ASD. Atypical forms of interoceptive awareness have been noted in people who suffer from both alexithymia and ASD [43]. It has been advanced that alexithymia could be correlated with the atypical interoception which is noted in people suffering from ASD [36, 41, 44]; this might be reflected in their difficulties understanding their bodily states, as well as theirs and others’ emotions [36, 45].

Dissociation, alexithymia-regulation of emotions and somatization

Muskens et al. [46] conducted a meta-analysis to verify the prevalence of somatic disorders in people with attention deficit hyperactivity disorder (ADHD) and ASD. The main finding of this systematic review is that medical disorders in children with ASD and ADHD appear to be widespread, e.g., can manifest themselves across different medical areas, such as immunology, neurology, and gastroenterology. They suggest that these children require multidisciplinary medical services, including psychiatric help [46]. On the other hand, it has been proposed that certain features of ASD symptomatology may predispose this population to an increased risk of cumulative stressful life events and trauma exposure, and subsequent development of posttraumatic stress disorder (PTSD) [47–50]. Following exposure to trauma, PTSD may and does develop in certain individuals with ASD [50], with PTSD diagnosis found to be associated with suicidal thoughts and attempts within this population [51, 52]. Taylor and Gotham [50] suggest that contextual factors such as trauma might be important for the development of mood symptomatology in individuals with ASD. Mood and anxiety disorders are the most widespread psychiatric comorbidities in adolescents and adults with ASD [50].

Dissociation in the setting of chronic trauma is considered to be a coping strategy, at least initially. In the setting of childhood trauma, dissociation is thought to be a self-protective survival technique in which a child (or adult) slips into a dissociative state in order to escape fully experiencing trauma that is unbearable [53]. However, developmental mood and anxiety disorders, PTSD or physical symptoms strengthen psychological consequences of experienced traumas; in fact, they demonstrate symptoms that are distressing and confusing and that stand in the way of a fulfilling life. According to Nijenhuis [54], it is necessary to stress that the “psychological dissociation” and “somatoform dissociation” labels should not be taken to signify that only psychological dissociation is a mental phenomenon. Both labels relate to the ways in which dissociative symptoms may show themselves, not to their presumed cause. Somatoform dissociation designates dissociative symptoms that phenomenologically involve the body, and psychological dissociative symptoms are those that phenomenologically involve psychological variables [2]. The “somatoform” descriptor demonstrates that the physical symptoms are akin to, but cannot be explained by, a medical symptom or the direct effects of a substance. Thus “somatoform dissociation” denotes phenomena that are manifestations of a lack of integration of somatoform functions, reactions, and experiences. Motor inhibitions and anesthesia/analgesia are somatoform dissociative symptoms that are akin to animal defensive reactions to major threat and injury [2, 53].

Hypothesis and study rationale

It was hypothesized that the higher interoceptive sensibility in individuals with ASD is accompanied by a higher level of alexithymia on the emotions’ identification and verbalization dimensions, as well as a higher dysregulation of emotions, especially in relation to deficits in realizing emotions and deficits in the clarity as to experienced emotions. However, to date, no studies have specifically assessed the relationships between interoceptive sensibility and somatoform disorders with the mediating role of alexithymia, and emotion dysregulation in adults with ASD (Fig 1).

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Fig 1. A graphical model presenting the nature of dependencies between interoceptive sensibility (autonomic reactivity), alexithymia, and difficulties in emotion regulation in explaining an inclination to somatoform disorders.

https://doi.org/10.1371/journal.pone.0255460.g001

To verify the above relationships, individuals with ASD have been selected due to the fact that disorders related to experiencing, understanding, and cognitive analysis of emotions in this group coincide with those observed in alexithymia. Mattila et al. [55] stated that alexithymia rates in the general population have been reported to be 9–17% for men and 5–10% for women whereas estimates are as high as 70% in some clinical groups [56]. Studies show that alexithymia has been found in nearly 50% of persons with ASD [57]. Gaig et al., [58] showed that alexithymia occurring both in the group with ASD and without this personality trait, is associated with the disturbance of appropriate differentiation of physiological arousal and thereby with distortions in the cognitive processing of experienced emotion and feelings. Therefore, it is alexithymia that is associated with the described disorders, not autism.

To the best of our knowledge, this is the first study aiming at: 1) testing whether somatoform disorders in the ASD patients might depend on interoceptive sensibility; 2) assessing the impact of alexithymia and dysregulation in the prediction of somatoform disorders using a battery of correlation studies, t-tests, moderation and mediation analyses. The serial multiple mediation model consistent with the theoretical findings and research results discussed above assumes an effect of alexithymia and dysregulation of emotions upon the relationship between interoceptive sensibility and somatoform disorders.

Participants

This study was conducted in accordance with the recommendations of the SWPS University of Social Sciences and Humanities Ethics Committee with written informed consent from all those who took part. All procedures during the study involving human participants were performed in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its further amendments or comparable ethical standards. The project was approved by Institutional Review Board (IRB) of the SWPS University of Social Sciences and Humanities, Protocol No. 4/2019.

Persons under the care of the Foundation helping people with ASD located in Warsaw and other individuals not connected with the Foundation were asked to participate in the study, who constituted the control group. The study was carried out from April to August 2019. 205 people took part in the research including 157 women (76.6% of the total number of participants) and 48 men (23.4% of the total number of participants). The participants aged from 18 to 63 (M = 34.91; SD = 8.44). The clinical group included persons diagnosed with autism spectrum disorders, specifically Asperger’s syndrome. The diagnosis has been additionally supported by the Autism-Spectrum Quotient. To be eligible for the clinical group, an individual must have been diagnosed with Asperger’s syndrome and must have had at least 32 points in the AQ questionnaire. Ultimately, the clinical group comprised 79 persons, 72% women and 28% men, aged 20 to 45 (M = 35.12 SD = 6.32). The control group comprised individuals without any diagnosis of autism spectrum disorders and scoring less than 32 points in AQ questionnaire. The control group comprised 126 persons, 79% women and 21% men, aged 18 to 63 (M = 34.77 SD = 9.54).

Measures

Procedure

The study was carried out with each person individually. A question regarding the possibility of conducting a questionnaire survey was sent by email to the Foundations which help adults with ASD. Having obtained the consent, the researcher visited the Foundation’s office, introduced themselves, and invited persons who were willing to participate in the study. At first, each participant received the form of informed consent to participate in the study. Then questionnaires to be filled in were provided to participants in envelopes. Questionnaires were completed in random order. After completing, the questionnaires were returned to the researcher. In order to complete the control group, an announcement was published on SWPS University website with the invitation to participate. The willing persons contacted via a given email address. After making an appointment at the University Campus, as in the case of the clinical group, the respondents were given an informed consent form to participate in the study, and after that they were given an envelope containing the questionnaire. Upon completion, each participant was thanked for taking part in the study.

Data analysis

A statistical analysis to test the posited hypotheses was undertaken using IBM SPSS Statistics, version 26. Key descriptive statistics were undertaken using the software, making it possible to study the distributions of successive measured variables. Parametric tests were performed on all variables as the skewness values did not exceed the conventional absolute value of 1. In the first place, a series of correlation analyses was performed to assess the relationship between somatoform disorders and all other variables. Further, a series of t-tests was performed to determine differences between the clinical and control groups in terms of alexithymia, emotion dysregulation, and interoceptive sensibility dimensions. The next step was to carry out a moderation analysis, where a (clinical/control) group was the moderator, using the A. F. Hayes PROCESS macro (model 1) [65] to determine to what extent the fact of being diagnosed with ASD affects the relationship between interoceptive sensibility (autonomic reactivity) and somatoform disorders. Subsequently, the mediating role of all dimensions of alexithymia and emotion dysregulation was verified separately using the A. F. Hayes PROCESS macro (model 4). Finally, a method was applied that combined the relationship of interoceptive sensibility (autonomic reactivity) and somatoform disorders with the mediating role of alexithymia and emotion dysregulation. Due to the high level of correlation between mediators, the serial multiple mediation model A. F. Hayes PROCESS macro (model 6) was performed since this method assumes a strong relation between mediators [65]. In addition, it allows to control the impact of a single mediator, as well as to determine the simultaneous impact of both mediating variables on the relation between an independent and dependent variable.

Limitations

Our study has some limitations that we would like to highlight. It based exclusively on self-report measures. In addition, it is cross-sectional and correlative. For this reason, it is difficult to clearly outline unequivocal directions or relationships between the investigated factors. We adopted, in line with the attachment theory, a direction of relationship from interoceptive sensibility through alexithymia to somatic disorders. However, we examined adults and those who, due to somatic problems of unspecified etiology, may show increased alexithymia and interoceptive sensibility. The nature of relationship between emotion understanding and experiencing and becoming sensitive to specific body signals requires longitudinal studies to be carried out in the future. The excessive interoceptive sensibility, combined with alexithymia, may favor the development of somatic dysfunctions. Such is the case with the examined group of individuals with ASD.