Interoceptive awareness moderates neural activity during decision-making
Introduction
Embodied cognition is a growing research issue in psychophysiological science that emphasizes the role of bodily states in cognitive processes. The general theory is that mental processes do not only influence bodily states but that bodily states also influence thoughts, feelings and motivational behavior. In particular, emotion theories have accounted for bodily signals as an important factor in emotion processing (cf. Bechara and Naqvi, 2004, Damasio, 1994, James, 1884). James (1884) was one of the first who postulated that feedback from the body is closely related to emotional experience. His theory holds that the experience of an emotion is the perception of bodily responses that result from some stimulus. Damasio (1994) revived the field with the formulation of the somatic marker hypothesis, which emphasizes that cognitive processes such as decision-making are guided by central feedback of bodily arousal responses. According to this theory, automatically generated bodily arousal responses, the so-called somatic markers, are induced by external or internal events and mark these events with an “emotional” signal. These somatic markers are conveyed to the brain and are integrated in emotional and cognitive processes. According to Damasio and coworkers (e.g., Bechara, Tranel, & Damasio, 2000), somatic markers are represented and regulated in the emotion circuitry of the brain including the medial prefrontal cortex, the amygdala, the insula, the somatosensory cortex, and brainstem nuclei. Particularly in situations of uncertainty and complexity, somatic marker signals are thought to enable a faster and experience driven integration of decision-making by forcing attention towards “the negative outcome to which a given action may lead, and function as an automated alarm signal that says: Beware of danger ahead if you choose the option that leads to this outcome” (Damasio, 1994, p. 123).
Empirical support for somatic signals affecting decision-making comes from studies using the Iowa Gambling Task (IGT, Bechara, Damasio, Damasio, & Anderson, 1994). This task simulates real-life decision-making by presenting ambiguous consequences. Participants are presented with four card decks. Two decks yield high gains but also high losses. If decks of this type are played continuously, the result is a net loss, and thus the selection of these decks is disadvantageous in the long term. The other two decks yield small gains and small losses. If they are selected continuously the result is a net profit. Thus, the selection of these decks is advantageous in the long term. Recent studies demonstrate that healthy individuals usually learn within a short time period to adopt an advantageous strategy in this task. Additionally, they develop anticipatory skin conductance responses preceding disadvantageous choices (Bechara, Damasio, Tranel, & Damasio, 1997). However, patients with lesions of the ventromedial prefrontal cortex, which is associated with an impairment of somatic signal processing, do not show a generation of somatic markers in the form of increased skin conductance responses preceding disadvantageous decisions. Accordingly, they demonstrate impaired decision-making by carrying on selecting disadvantageous options (Bechara et al., 1997). Impairments in decision-making also hold true for patients with autonomic peripheral neuropathy, who show deficient visceral regulation and feedback (North & O’Carroll, 2001). In contrast, individuals with particular accurate sensitivity to bodily signals demonstrate superior decision-making performance in the IGT compared to individuals with non-accurate bodily perception (Werner, Jung, Duschek, & Schandry, 2009). In an evolved version of the IGT interoceptive awareness was associated with both good and poor guidance in decision-making depending on whether bodily signals indicate adaptive or maladaptive choices (Dunn et al., 2010). Accordingly, we assume that individuals with accurate body perception display more efficient central nervous processing of bodily signals, which may bias the decision-making process. The present study aimed to substantiate this assumption by investigating the relationship between bodily awareness and neural activation during performance of the IGT.
The ability to consciously detect subtle changes in bodily states including temperature, pain, visceral or muscular sensations is referred to as “interoceptive awareness”. The neural system that underlies interoceptive awareness is a homeostatic pathway that conveys information about the internal state of the body through the lamina I spinothalamocortical pathway to the insula and orbitofrontal cortex (Craig, 2002). Converging evidence from functional imaging studies substantiates the central role of the anterior insula as mapping internal body states and representing emotions (Craig, 2009, Critchley, 2005).
Studies quantifying interoceptive awareness have primarily focused on afferent information from the viscera, in particular from the heart (“heartbeat perception”, e.g., Critchley et al., 2004, Pollatos et al., 2005, Schandry, 1981, Werner et al., 2009c, Wiens et al., 2000). A variety of methods for the quantification of heartbeat perception has been developed (e.g., McFarland, 1975, Schandry, 1981). The most widely used procedure is the mental tracking task proposed by Schandry (1981). In this paradigm, participants count their heartbeats silently during different time intervals lasting less than a minute each.
The processing of sensory information from the heart varies to a substantial degree among individuals depending on age, gender, percentage of body fat and physical fitness (Cameron, 2001, Khalsa et al., 2009, Vaitl, 1996). Furthermore, differences in cardio-dynamic parameters such as stroke volume and blood pressure also contribute to differences in heartbeat perception (O’Brien et al., 1998, Schandry et al., 1993). A close association between heartbeat perception and the activation of specific brain structures has been demonstrated including enhanced neural activity in the insula, the somatomotor and cingulate cortex (Critchley et al., 2004, Pollatos et al., 2007a). Furthermore, participants’ heartbeat perception accuracy correlates with activity in the right anterior insular cortex (Critchley et al., 2004). Consistent with the aforementioned emotion theories there is evidence that the ability to perceive bodily signals influences subjective emotional experience (e.g., Barrett et al., 2004, Pollatos et al., 2007a, Schandry, 1981, Wiens et al., 2000). Individuals with high interoceptive awareness frequently reported emotions with higher intensity. Recent research also suggests an association between interoceptive awareness and cognitive functioning with superior decision-making (Werner, Jung et al., 2009) and memory performance (Pollatos and Schandry, 2008, Werner et al., 2010).
To understand how bodily signals affect cognitive and affective processing it is important to relate interoceptive awareness to neural processing during behavior. Thus, the purpose of our study was to investigate the relationship between interoceptive awareness and neural activity during the performance of the IGT. Previous studies on the IGT have shown that decision-making during the IGT is associated with activity in several brain regions consistent with the neural circuitry hypothesized to underlie the somatic marker hypothesis. Specifically, this neural circuitry involves the prefrontal cortex, the insula and the cingulate cortex (e.g., Lawrence et al., 2009, Li et al., 2010, Windmann et al., 2006). Assuming that bodily signals affect decision-making, the anticipation of a long-term consequence is according to the somatic marker hypothesis of particular interest. The few previous studies unraveling the dimensions of decision-making have demonstrated increased selection related activity in the medial prefrontal cortex (Fukui et al., 2005, Lin et al., 2008), the insula and the basal ganglia (Lin et al., 2008).
In the present study, functional magnet resonance imaging (fMRI) was used to investigate the relation between interoceptive awareness and selection related neural activity during IGT performance. Since the insula plays an important role both in the processing of somatic signals (Critchley et al., 2004, Pollatos et al., 2007a) and in decision-making (Lawrence et al., 2009, Li et al., 2010, Lin et al., 2008), we suggested that interoceptive awareness is associated with stronger processing of somatic markers. In particular, we hypothesized that selection related activity in the insula would be related to interoceptive awareness and that neural activity in this region would correlate with decision-making performance.
Section snippets
Participants
Twenty-nine participants aged between 19 and 32 years, all with university-entrance level qualifications, took part in the study. Health status was assessed with a questionnaire covering diseases of the cardiovascular and respiratory systems and psychiatric disorders. Participants were only included if they did not report any of these disorders and did not report using medication affecting the cardiac and central nervous system. All participants gave written informed consent and received
Decision-making performance
Behavioral performance during the IGT is displayed in Fig. 1 as learning curves. A repeated measurement ANOVA revealed a significant main effect of card deck, F(1,28) = 6.93, p = 0.014, η2 = 0.20, indicating that overall participants chose significantly fewer of the disadvantageous decks (M = 42.00, SD = 16.18) and more of the advantageous decks (M = 57.86, SD = 16.23). A significant interaction effect card deck × block, F(4, 112) = 6.45, p < 0.001, η2 = 0.19, proved that participants learned to avoid the selection
Discussion
This study investigated the relation between interoceptive awareness and selection related neural activity during the IGT. In accordance with our hypotheses, we found indications of a relationship between interoceptive awareness and right anterior insula activity preceding disadvantageous decisions. The intensity in right insula activity increased with more accurate interoceptive awareness. This finding is in line with previous fMRI studies demonstrating the role of the insula in representing
Conflict of interest
None of the authors declare any actual or potential conflict of interest.
Acknowledgements
We are grateful to Ute Coates and Tanja Mannhart for their assistance in fMRI scanning.
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2021, Neuroscience and Biobehavioral ReviewsCitation Excerpt :Decision urgency (the increasing desire to make a decision as time passes) has also been associated with insula activation (van Maanen et al., 2016). The degree of insula activation during decision-making may also be a function of interoceptive accuracy; one study found that right insula activation was associated with Iowa Gambling Task performance only in individuals who performed well on the heartbeat counting task, and not in those with poor cardiac perception (Werner et al., 2013). It is worth noting, of course, that co-activation of large, differentiated neural structures during interoception and representation of learning parameters does not necessarily indicate that the same neurons, or even populations of neurons, are involved in both processes.