The man who feels two hearts: the different pathways of interoception

Abstract

Recent advances in neuroscience have provided new insights into the understanding of heart-brain interaction and communication. Cardiac information to the brain relies on two pathways, terminating in the insular cortex (IC) and anterior cingulate cortex (ACC), along with the somatosensory cortex (S1-S2). Interoception relying on these neuroanatomical pathways has been shown to modulate social cognition. We report the case study of C.S., a patient with an 'external heart' (an extracorporeal left-univentricular cardiac assist device, LVAD). The patient was assessed with neural/behavioral measures of cardiac interoception complemented by neuropsychological and social cognition measures. The patient's performance on the interoception task (heartbeat detection) seemed to be guided by signals from the artificial LVAD, which provides a somatosensory beat rather than by his endogenous heart. Cortical activity (HEP, heartbeat-evoked potential) was found decreased in comparison with normal volunteers, particularly during interoceptive states. The patient accurately performed several cognitive tasks, except for interoception-related social cognition domains (empathy, theory of mind and decision making). This evidence suggests an imbalance in the patient's cardiac interoceptive pathways that enhances sensation driven by the artificial pump over that from the cardiac vagal-IC/ACC pathway. A patient with two hearts, one endogenous and one artificial, presents a unique opportunity to explore models of interoception and heart-brain interaction.

Keywords: HEP; heart-brain; insula; interoception; social cognition.

Fig. 1

Schematic and picture of the LVAD implantation procedure. (A) Schematic view of the LVAD with the pump lying over the patient’s abdominal skin and canulae connecting it to the apex and aortic artery. (B) Implantation procedure; canulae can be seen exiting from the thoracic cavity to the abdominal skin and connecting to the pump (images provided by Berlin Heart).

Fig. 2

Behavioral performance on HBD tasks. Polar histograms of relative synchronization between the patient’s responses and his actual endogenous heartbeats (in red bars) and artificial pump-beats (blue bars). (A) motor control condition; (B) interoception pre-condition; (C) auditory feedback condition; (D) interoception post-condition. A large proportion of blue area (artificial pump-beats) can be seen in the interoception conditions (B and D), whereas a greater proportion of red area (endogenous heartbeats) can be seen in the motor control and auditory feedback conditions (A and C).

Fig. 3

HEP comparison. (A) HEP per condition in the patient and control sample during the three states (MW, mind wandering; Ext, exteroception; Int, interoception). Note the lack of modulation in the interoception condition between 130 and 300 ms in the patient. (B) Significance curve of permutations comparing the interoceptive condition between controls and the patient. (C) Raster plots of HEP single trials during the interoceptive condition in the patient and control sample. The box indicates the HEP time window.