Resting heart rate variability predicts safety learning and fear extinction in an interoceptive fear conditioning paradigm.

Meike Pappens,Stefan Sütterlin,Omer Van den Bergh,Ilse Van Diest,Julian F. Thayer,Mathias Schroijen,Elyn Smets,Manabu Sakakibara

doi:10.1371/journal.pone.0105054

Meike Pappens, Stefan Sütterlin + Show 6 more

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https://doi.org/10.1371/journal.pone.0105054

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Abstract

This study aimed to investigate whether interindividual differences in autonomic inhibitory control predict safety learning and fear extinction in an interoceptive fear conditioning paradigm. Data from a previously reported study (N = 40) were extended (N = 17) and re-analyzed to test whether healthy participants' resting heart rate variability (HRV) - a proxy of cardiac vagal tone - predicts learning performance. The conditioned stimulus (CS) was a slight sensation of breathlessness induced by a flow resistor, the unconditioned stimulus (US) was an aversive short-lasting suffocation experience induced by a complete occlusion of the breathing circuitry. During acquisition, the paired group received 6 paired CS-US presentations; the control group received 6 explicitly unpaired CS-US presentations. In the extinction phase, both groups were exposed to 6 CS-only presentations. Measures included startle blink EMG, skin conductance responses (SCR) and US-expectancy ratings. Resting HRV significantly predicted the startle blink EMG learning curves both during acquisition and extinction. In the unpaired group, higher levels of HRV at rest predicted safety learning to the CS during acquisition. In the paired group, higher levels of HRV were associated with better extinction. Our findings suggest that the strength or integrity of prefrontal inhibitory mechanisms involved in safety- and extinction learning can be indexed by HRV at rest.

Highlights

Fear conditioning research has yielded a wide array of laboratory models, tools and sophisticated experimental designs that are helpful to unravel the specific mechanisms that contribute to fear learning, and, potentially, to the pathogenesis of anxiety disorders [1,2,3]
Follow-up analyses within each level of group showed that only in the unpaired group, RMSSD was a significant predictor of how CSISI differences changed across acquisition blocks (Probe6 Block6RMSSD for the unpaired: F(2, 52) = 6.90, p,.01, g2 = .21, e = .98; for the paired: F(2, 52) = 0.23, p = .80, g2 = .009, e = .89)
In the unpaired condition (Figure 1, Table 1), only participants with high RMSSD showed a decreasing linear trend in startle responding during the conditioned stimulus (CS) (unpaired low RMSSD: t(53) = 1.11, p = .46; unpaired high RMSSD: t(53) = 3.40, p,.001), suggesting more successful safety learning in the high compared to the low RMSSD unpaired group

Summary

Introduction

Fear conditioning research has yielded a wide array of laboratory models, tools and sophisticated experimental designs that are helpful to unravel the specific mechanisms that contribute to fear learning, and, potentially, to the pathogenesis of anxiety disorders [1,2,3]. It has been shown that anxiety patients are characterized by enhanced conditionability and fear generalization, by flattened extinction curves, by worse retention of extinction and by a reduced inhibition of fear responding to safety cues [3,4]. Common to all these characteristics seems an impaired capacity to inhibit fear responding compared to healthy subjects. The activation of medial subcortical areas underlying sympathetic-driven fear responding is regulated by top-down inhibitory input from the prefrontal cortex (PFC) [5,6]. Prefrontal areas are involved in learning to discriminate between periods of safety and danger [8,9]

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