Heartbeat evoked potentials mirror altered body perception in depressed patients
Highlights
► Heartbeat evoked potentials are objective markers of altered bodily awareness. ► Reduced interoception in major depression has been shown in comparison to controls. ► Interoception in depression may be linked to decreased capacity for decision-making.
Introduction
Major depression has been projected to become the second leading cause of disability worldwide by 2020 after ischemic heart disease (Bromet et al., 2011). During depressive episodes, many patients suffer from cognitive impairment, loss of awareness of their feelings, physical comorbidity and a lack of decisiveness. It has been found that people with decreased interoceptive awareness likewise show less developed information processing, less self-regulation of physical load, a reduced capacity for decision making and less intense experiencing of emotions (Bechara et al., 1996, Herbert et al., 2007b, Pollatos et al., 2007a, Pollatos et al., 2007b).
The theoretical underpinnings of these findings were first provided by William James who claimed that emotions were caused by the perception of bodily changes. He wrote, “we feel sorry because we cry […] [and] afraid because we tremble” (James, 1884). Based on this and related observations, Damasio (1994) developed the somatic marker hypothesis, which defines emotions as collections of bodily changes evoked by thoughts (Damasio, 1994, Bennett and Hacker, 2005). Furthermore, it has been argued that a person’s degree of bodily awareness helps him or her to regulate decision making and that emotional biasing signals originating in the body are integrated and stored in higher brain structures and are involved in complex decision-making processes (Damasio, 1994, Dunn et al., 2006).
Given these theories and findings, one would assume a reduction in interoceptive awareness during depression, since cognitive function and decision-making are known to be impaired. However, studies linking depression and bodily awareness are rare and contradict one another. While some authors (Mussgay et al., 1999, Van der Does et al., 1997) have reported a tendency towards decreased heartbeat perception in depressed patients, Dunn et al. (2007) found decreases in heartbeat perception only in mildly depressed participants, while more severely depressed individuals showed normal levels of heartbeat perception. Hence, more research is necessary to further understand the link between depression and interoceptive accuracy.
Assessment of heartbeat perception is one of the most common methods to quantitate interoceptive awareness and has been shown to be sufficiently reliable (Mussgay et al., 1999, Schandry, 1981, Van der Does et al., 1997). Furthermore, heartbeat perception has been related to neural systems such as the insular, cingulated and somatomotor cortices (Critchley et al., 2004). Moreover, heartbeat evoked potentials (HEPs) resulting from afferent transmission have been studied in several EEG-studies (Dirlich et al., 1998, Dirlich et al., 1997, Schandry et al., 1986). The HEPs are thought to provide an objective correlate of interoceptive processing, even though the exact brain source configuration contributing to HEP remains poorly understood.
HEPs have been shown to appear mainly close to the somatosensory cortex and the prefrontal and frontal cortices (Pollatos and Schandry, 2004). However, others have reported HEPs over various other regions, including the parietal and temporal regions (Dirlich et al., 1998, Gray et al., 2007). Despite the apparent lack of topographical consistency across studies, HEPs have been proven to be sensitive markers of the accuracy of heartbeat perception. Accordingly, significant group differences between accurate and poor heartbeat perceivers as shown through measurements of HEP amplitudes were repeatedly found, in particular at frontal and central electrode sites (Katkin et al., 1991, Pollatos and Schandry, 2004, Schandry and Weitkunat, 1990, Yuan et al., 2007). Furthermore, the HEP has been proven to be sensitive to changes in directed attention. Attention effects are stronger in good heartbeat perceivers (Yuan et al., 2007) and, surprisingly, amplitudes at some individual electrodes have been shown to be smaller during the attention state than in the distraction state (Montoya et al., 1993).
The aim of the present study was to investigate whether heartbeat perception accuracy is reduced in depressed patients. Therefore, heartbeat perception scores were assessed in patients and controls. In order to explore the significance of a more objective means of interoceptive awareness, HEP amplitudes were analyzed. Given the topographical inconsistencies of previous HEP reports, this one was done by means of a global field power (GFP) analysis, which is a measure of evoked potential strength across the scalp (Lehmann and Skrandies, 1984). The value of HEPs is that they yield information independently from the participants’ motivation to perform the task. As the majority of studies found reduced accuracy of heartbeat perception in depressed patients, we hypothesized that heartbeat perception is decreased in depressed patients and, accordingly, we expected the amplitudes of HEPs to be reduced.
Section snippets
Participants
Sixteen depressed patients (13 females, mean age 41.75 ± 12.4 years) and an age- and gender-matched control group consisting of 16 healthy volunteers (12 females, mean age 39.81 ± 17.6 years) were included in the study after applying exclusion criteria. Two participants (one patient and one control subject) were excluded because of invalid HEPs; in these participants, the GFP HEPs were larger than mean ± 2 SD and thus were considered as outliers (Montoya et al., 1993). Groups did not differ
Behavioral data
As expected, the one-tailed t-test for independent samples revealed that patients showed significantly reduced levels of heartbeat perception [controls = 0.81 ± 0.04; patients = 0.67 ± 0.05, t(30) = 2.44, p = .011, d = 0.85]. An illustration of the group comparison is provided in Fig. 3a. With respect to heartbeat and tone counting performance during EEG, the 5 × 2 × 2 ANOVA revealed a significant effect of TIME [F(2.8, 82.8) = 4.85, p = .005, η2 = 0.14], as controls and patients improved significantly over time.
Discussion
Interoceptive awareness has been shown to have an impact on cognition, self-control of physical load, self-perception and decision making (Damasio, 1994, Herbert et al., 2007b, Pollatos et al., 2007b, Pollatos et al., 2007c). In the present study, we aimed to further elucidate characteristics of interoception during depressive episodes. In terms of behavioral data, a significantly decreased heartbeat perception score was observed in depressed patients. The analyzes revealed reduced GFP HEP
Acknowledgment
We thank Anna-Karoline Israel and Jeremy Thorne for technical support. None of the authors has any conflict of interests or any financial conflict to declare.
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