Auditory Feedback Differentially Modulates Behavioral and Neural Markers of Objective and Subjective Performance When Tapping to Your Heartbeat

Abstract

Interoception, the perception of our body internal signals, plays a key role in maintaining homeostasis and guiding our behavior. Sometimes, we become aware of our body signals and use them in planning and strategic thinking. Here, we show behavioral and neural dissociations between learning to follow one's own heartbeat and metacognitive awareness of one's performance, in a heartbeat-tapping task performed before and after auditory feedback. The electroencephalography amplitude of the heartbeat-evoked potential in interoceptive learners, that is, participants whose accuracy of tapping to their heartbeat improved after auditory feedback, was higher compared with non-learners. However, an increase in gamma phase synchrony (30–45 Hz) after the heartbeat auditory feedback was present only in those participants showing agreement between objective interoceptive performance and metacognitive awareness. Source localization in a group of participants and direct cortical recordings in a single patient identified a network hub for interoceptive learning in the insular cortex. In summary, interoceptive learning may be mediated by the right insular response to the heartbeat, whereas metacognitive awareness of learning may be mediated by widespread cortical synchronization patterns.

Feeling, learning from and being aware of inner states: interoceptive dimensions in neurodegeneration and stroke

“…On the other hand, interoceptive awareness and metacognition are intimately related. Focus on internal visceral signals and constant monitoring and feedback updating of internal predictions are important for the construction of subjective feeling states, and their disruption could explain the patients' behavioural failures [11,70,71]. In this sense, previous reports show that BA10 (i) supports emotional processing of internal states [72], (ii) is related to information retrieval and prospective memory [72] and (iii) could contribute to anosognosia, a typical symptom of dementias [30].…”

“…Next, they performed the same task while receiving feedback via a stethoscope (feedback control condition). In line with previous studies [11], auditory feedback was delivered through a stethoscope, which was held by the participants themselves with the left hand, while they tapped on the keyboard with the right hand. Finally, they were asked to follow their heartbeats again without external cues, which allowed measuring interoceptive learning.…”

“…We also assessed three separate four-electrode ROIs in frontal-right, -left and -central topographies. To control As in previous cardiac interoception studies [44], ERP data were compared among conditions via Monte Carlo permutation tests [47] combined with bootstrapping from 100 ms to 400 ms (to cover typical HEP latencies [11,19]). This simple method offers a straightforward solution for multiple comparison problems and does not depend on multiple comparisons correction or Gaussian assumptions about data probability distribution [48] (see electronic supplementary material, §1.2.2).…”

“…These dimensions rely on distributed networks critically engaging the insular cortex (IC), the anterior cingulate cortex (ACC) and the somatosensory cortex (SC) [2,12], while interactions between interoceptive and high-level functions are mediated by IC projections to the ACC, the orbitofrontal cortex (OFC), the amygdala and the hippocampus (HP) [3,4,11,[13][14][15][16][17][18].…”

“…Second, regarding interoceptive learning, cortical and intracranial recordings show that post-feedback behavioural improvements are associated with activity modulations in the IC and the frontal cortex [11]. However, whole-brain neuroimaging analyses may reveal other regions related to impairments in this dimension.…”