Interoceptive awareness moderates neural activity during decision-making

Highlights

• We tested the relationship between cardiac interoceptive awareness and neural responses preceding decision-making.

• Cardiac interoceptive awareness was associated with activity in the right anterior insula and the left postcentral gyrus.

• Right anterior insula activity was related to decision-making performance in accurate cardiac interoceptive awareness.

• These findings support a relationship between body feedback and decision-making.

Abstract

The current study examined the relationship between conscious perception of somatic feedback (interoceptive awareness) and neural responses preceding decision-making. Previous research has suggested that decision-making is influenced by body signals from the periphery or the central representation of the periphery. Using event-related fMRI, participants whose interoceptive awareness was assessed using a heartbeat perception paradigm performed the Iowa Gambling Task. The results show a positive relationship between the degree of interoceptive awareness and selection related activity in the right anterior insula and the left postcentral gyrus. Neural activity within the right anterior insula was associated with decision-making performance only in individuals with accurate but not in those with non-accurate interoceptive awareness. These findings support the role of somatic feedback in decision-making processes. They indicate that the right anterior insula holds a representation of somatic markers and that these are more strongly processed with increased interoceptive awareness.

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.