Elsevier

Neuropsychologia

Volume 106, November 2017, Pages 1-6
Neuropsychologia

High vagally mediated resting-state heart rate variability is associated with superior action cascading

https://doi.org/10.1016/j.neuropsychologia.2017.08.030Get rights and content

Highlights

  • Vagally mediated HRV (vmHRV) has a key role in neurovisceral integration model.

  • We investigated the functional relation of resting state vmHRV and action cascading.

  • High resting-state HRV is associated with enhanced action cascading processes.

  • vmHRV might be a novel marker of one's ability to prioritize and cascade different actions.

Abstract

The neurovisceral integration model suggests that individual differences in heart rate variability (HRV), an index of vagal tone, may relate to prefrontal cortical activity and predict performance on cognitive control tasks. The aim of this study was to further verify this model by investigating the relationship between vagally-mediated resting-state HRV and action cascading, a crucial cognitive control function which refers to the ability to cope with multiple response options when confronted with various task goals. Resting-state HRV and performance on the stop-change paradigm, which provides a relatively well-established diagnostic measure of action cascading and response inhibition, was assessed in 88 healthy volunteers (age range 18–33). Compared to individuals with low resting-state HRV, participants with high resting-state HRV showed enhanced action cascading performance, both when a disruption (stopping) and change towards an alternative response were required simultaneously, and when requirements were cascaded (i.e. when the stopping process had already finished at the time the change was required). Our findings represent an important step towards extending our understanding of the neurovisceral integration model in cognitive control.

Introduction

The neurovisceral integration model (Thayer et al., 2009) suggests that individual differences in heart rate variability (HRV) may predict performance on cognitive control tasks. According to this model, vagally-mediated HRV plays a key role in signaling functional activity of the prefrontal cortex, a crucial area that drives cognitive control; the way we control our thoughts and goal-directed behavior (Miller, 2000). HRV is a measure of beat-to-beat temporal fluctuations in the heart rate and has been considered a proxy of parasympathetic control and vagal tone (Berntson et al., 1997). Reduced HRV is an index of poor autonomic nervous system regulation and is linked to increased risk of all-cause mortality (Thayer and Lane, 2007).

In a nutshell, the neurovisceral integration model (Thayer and Lane, 2000, Thayer et al., 2009) suggests that functioning of prefrontal-subcortical inhibitory circuits is critical for self-regulation. These circuits provide inhibitory input to the heart through the vagus nerve (see also Levy, 1971; Benarroch, 1993; Ellis and Thayer, 2010). A number of neuroimaging and pharmacological investigations have provided evidence for an association between inhibitory prefrontal-subcortical circuits and cardiac vagal tone indexed by vagally-mediated resting HRV (Ahern et al., 2001, Lane et al., 2009; for a review, see Thayer et al., 2009). Crucially, a recent meta-analysis (Thayer et al., 2012) has proposed that high resting-state HRV is associated with optimal functioning of prefrontal-subcortical inhibitory circuits that sustain flexible and adaptive responses to environmental demands (Thayer and Lane, 2000, Thayer et al., 2009).

So far, the majority of studies evaluating the neurovisceral integration model investigated the role of vagally-mediated resting HRV in emotion regulation (see Park and Thayer, 2014, for a recent review on the topic). Only few studies have explored, instead, the role of HRV in well-established cognitive control tasks. From these previous studies, the following picture arises: high HRV seems to be related to better cognitive inhibition, mental flexibility, and working memory updating (Hansen et al., 2003, Stenfors et al., 2016, Jennings et al., 2015, Luque-Casado et al., 2013, Luque-Casado et al., 2016). However, it is important to note that in the studies mentioned above, different HRV measures were recorded employing different methods (e.g. during rest, during cognitive activities, and/or during recovery), which makes it difficult to draw strong conclusions based on comparison of these studies. Given that, as proposed by Thayer et al. (2012), high resting-state HRV seems to be associated with optimal functioning of prefrontal-subcortical inhibitory circuits, and given our goal to test the neurovisceral integration model (Thayer et al., 2009), we will focus on resting-state HRV in the current study. Specifically, the aim of the present study is to gain a better understanding of the association between vagally-mediated resting-state HRV and improved cognitive control by investigating action cascading. Action cascading is a crucial cognitive control function, which refers to the ability to cope with multiple response options when confronted with various task goals. In order to assess whether high resting-state HRV is associated with an enhanced ability to prioritize and cascade different actions, we employed a stop-change (SC) task introduced by Verbruggen, Schneider, and Logan (2008). In this task, the main goal is to respond to a GO stimulus as fast as possible. Sometimes, a STOP stimulus is presented, which signals participants to stop the ongoing action. The STOP stimulus is followed by a CHANGE stimulus that informs participants to shift to another action. The time available to prepare for the execution of the change response (i.e. the delay between the STOP and CHANGE stimuli) is manipulated such that the interval between the STOP and the CHANGE stimuli (stop-change delay; SCD) can be 0 ms (i.e., SCD 0), that is, the two stimuli occur simultaneously, or it can be 300 ms (i.e., SCD 300), that is, they occur with a short delay, see Fig. 1. Responses on SC trials rely on the ability (a) to activate different task goals, and to cascade and prioritize different actions; (b) to succeed in inhibiting an ongoing response, and (c) to rapidly switch to a different response (Beste & Saft, 2015; Stock et al., 2014a; Stock et al., 2014b). Accordingly, reaction times (RTs) on SC trials can be taken to reflect the efficiency of action cascading, with lower RTs reflecting more efficient action cascading and selection.

Following previous studies, we employed the root of mean squared successive differences in heart-beat-intervals (RMSSD) measured during rest as a reliable index of resting-state vagally-mediated HRV (DeGiorgio et al., 2010, Koenig et al., 2016, Sperling et al., 2010). In sum, based on the neurovisceral integration model (Thayer et al., 2009), which proposes that high resting-state HRV is associated with optimal functioning of prefrontal-subcortical inhibitory circuits, we expected individuals associated with high resting-state RMSSD values (superior vagus-mediated HRV) to outperform individuals associated with low resting-state RMSSD (poor vagus-mediated HRV) in action cascading processes. That is, we expected them to show faster RTs on the SC trials both when an interruption (stopping) and a change toward an alternative response are required simultaneously (SCD0), and when the change to another response is required when the stopping process has already finished (SCD300).

Section snippets

Participants

Eighty-eight Leiden University undergraduate students (50 men, 38 women; mean age = 21.20 years, range 18–33; mean body mass index (BMI)= 22.17, range 18–30, mean vagally-mediated HRV = 39.75 ms, range 15–83) participated in the study. Participants were recruited via an on-line recruiting system and were offered partial course credit for participating in a study on the relationship between HRV and cognitive processes. Participants were screened individually using the Mini International

Demographic characteristics and descriptive statistics

Table 1 shows demographic information and descriptive statistics for the visual analogue scale and resting-state HRV of the two groups. No significant group differences were obtained for age, t(86) = .613, p = .542, BMI, t(86) = −.432, p = .641, and gender, χ2(1, N = 88) = .000, p = 1.00. Analyses on the self-reported level of anxiety, t(86) = .690, p = .492, nervousness, t(86) = 1.352, p = .180, insecurity, t(86) = −.667, p = .506, and stress, t(86) = −1.465, p = .147, also revealed no

Discussion

The aim of the study was to further verify the neurovisceral integration model (Thayer et al., 2009) by investigating the relationship between vagally-mediated resting-state HRV (as indexed by RMSSD) and cognitive control performance during action cascading. High resting-state HRV individuals, as compared to low resting-state HRV individuals, demonstrated better action cascading both when (a) the disruption (stopping) and a change toward an alternative response was required simultaneously [i.e.

Acknowledgments

This work was supported by a research grant from the Netherlands Organization for Scientific Research (NWO; www.nwo.nl) awarded to LSC (Vidi grant: #452-12-001).

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