Investigating the relationship between cardiac interoception and autonomic cardiac control using a predictive coding framework

Author: Andrew P Owens1, Karl J Friston2, David A Low3, Christopher J Mathias4, Hugo D Critchley5
1 Lab of Action & Body, Department of Psychology, Royal Holloway, University of London, Egham, Surrey, UK; Institute of Neurology, University College London, London WC1N 3BG, UK; National Hospital Neurology and Neurosurgery, UCL NHS Trust, London WC1N 3BG, UK. Electronic address:
2 Wellcome Trust Centre for Neuroimaging, University College London, WC1N 3BG, UK.
3 School of Sport and Exercise Sciences, Liverpool John Moores University, Liverpool L3 2AB, UK.
4 Hospital of St John & St Elizabeth, London NW8 9NH, UK.
5 Psychiatry, Brighton and Sussex Medical School, Brighton BN1 9RR, UK; Sussex Partnership NHS Foundation Trust, Brighton BN1 9RRUK, UK; Sackler Centre for Consciousness Science, University of Sussex, BN1 9RR, UK.
Conference/Journal: Auton Neurosci
Date published: 2018 Mar 1
Other: Volume ID: 210 , Pages: 65-71 , Special Notes: doi: 10.1016/j.autneu.2018.01.001. , Word Count: 276

Predictive coding models, such as the 'free-energy principle' (FEP), have recently been discussed in relation to how interoceptive (afferent visceral feedback) signals update predictions about the state of the body, thereby driving autonomic mediation of homeostasis. This study appealed to 'interoceptive inference', under the FEP, to seek new insights into autonomic (dys)function and brain-body integration by examining the relationship between cardiac interoception and autonomic cardiac control in healthy controls and patients with forms of orthostatic intolerance (OI); to (i) seek empirical support for interoceptive inference and (ii) delineate if this relationship was sensitive to increased interoceptive prediction error in OI patients during head-up tilt (HUT)/symptom provocation. Measures of interoception and heart rate variability (HRV) were recorded whilst supine and during HUT in healthy controls (N = 20), postural tachycardia syndrome (PoTS, N = 20) and vasovagal syncope (VVS, N = 20) patients. Compared to controls, interoceptive accuracy was reduced in both OI groups. Healthy controls' interoceptive sensibility positively correlated with HRV whilst supine. Conversely, both OI groups' interoceptive awareness negatively correlated with HRV during HUT. Our pilot study offers initial support for interoceptive inference and suggests OI cohorts share a central pathophysiology underlying interoceptive deficits expressed across distinct cardiovascular autonomic pathophysiology. From a predictive coding perspective, OI patients' data indicates a failure to attenuate/modulate ascending interoceptive prediction errors, reinforced by the concomitant failure to engage autonomic reflexes during HUT. Our findings offer a potential framework for conceptualising how the human nervous system maintains homeostasis and how both central and autonomic processes are ultimately implicated in dysautonomia.

Keywords: Active inference; Autonomic nervous system; Dysautonomia; Free-energy principle; Heart rate variability; Homeostasis; Interoception; Interoceptive (active) inference; Predictive coding.

PMID: 29331491 DOI: 10.1016/j.autneu.2018.01.001