Elsevier

Neuropsychologia

Volume 143, June 2020, 107465
Neuropsychologia

Transcutaneous vagus nerve stimulation modulates attentional resource deployment towards social cues

https://doi.org/10.1016/j.neuropsychologia.2020.107465Get rights and content

Highlights

  • tVNS modulates attention to salient social cues.

  • In a RSVP, tVNS enhanced conditional T2 accuracy for stimuli with a direct gaze.

  • The effect is independent of the emotion expressed and the temporal lag.

  • This supports the role of the vagus in processing relevant features of facial expression.

  • tVNS is a promising tool to enhance social functioning in healthy humans.

Abstract

Transcutaneous vagus nerve stimulation (tVNS) has been shown to promote inferences of emotional states based on eye-related information provided by facial expressions of emotions. Eye gaze direction can influence the allocation of attentional sources when processing facial emotional stimuli. Here we sought for further evidence indicating whether tVNS effects would be specific to emotional expressions or to gaze - both socially relevant stimuli - and whether they reflect the enhancement of attention. In two separate sessions receiving either active or sham tVNS, forty-three healthy young volunteers completed a Rapid Serial Visual Presentation task in which participants identified the gender of a target face (T1) with direct (salient social cue) or averted gaze (subtler social cue) with different emotional expressions or a neutral expression, and then judged the orientation of a landscape (T2) that appeared at different temporal lags after T1. Active tVNS, compared to sham stimulation, enhanced conditional T2 accuracy for both neutral and emotional faces and independently of the temporal lag, but only when gaze was directed at the participant. This suggests that tVNS modulates attention to a direct gaze (salient social cue) irrespective of the expressed emotion. We interpret that the effects of tVNS seem to reflect enhanced perception of gaze direction, which in turn attracts attention, making the observer more sensitive and increasing the impact of the socially relevant facial cue. We conclude that tVNS is a promising technique for enhancing social information processing in healthy humans.

Introduction

Other's emotions are important social cues, which provide us with ample information on how to respond in social situations. Without the ability to recognize and react to other's emotions, successful social interactions would not be possible (Frijda and Mesquita, 2004; Frith, 2009). An evolutionary perspective on emotion recognition has suggested that the vagus nerve is the key phylogenetic element underlying social engagement with the environment (Porges, 2007, 2003, 2001). The vagus nerve is the tenth cranial nerve and controls, among other functions, how humans are nodding their head and how they allocate their gaze towards other people, in fact modulating facial expressions, listening, and vocalizing (Porges, 2001; Stifter et al., 1989; Thayer and Lane, 2000; Yang and Immordino-Yang, 2017); all functions known to regulate social engagement. Following Porges' polyvagal theory, mammals (in contrast to other species) mature a ventral, myelinated, branch of the vagus. Whereas energy conservation is related to the primitive, dorsal vagal branch, the activation of the later developed ventral vagal branch has been connected to the ability to adapt and regulate complex behaviors such as attention, emotion, and communication (Porges, 2007, 2003, 2001). A number of studies confirm that activity of the vagus is associated with social cognitive abilities like empathy, recognizing and regulating emotions (Thayer and Lane, 2000), as well as prosocial traits (Kogan et al., 2014), cooperation (Beffara et al., 2016), and other forms of altruistic prosocial behaviors (Bornemann et al., 2016).

The vagus nerve is composed of around 75% afferent and 25% efferent fibers, which defines the vagus as an important conductor of sensitive and somatic signals (Berthoud and Neuhuber, 2000). One way to study the causal role of the afferent vagus in cognitive and emotional functions is transcutaneous vagus nerve stimulation (tVNS), a novel and noninvasive brain stimulation technique which imaging studies have shown to activate the afferent vagus (Badran et al., 2018; Frangos et al., 2015; Yakunina et al., 2017) and the insula (Dietrich et al., 2008; Kraus et al., 2007), a crucial neural structure for emotion recognition (Adolphs, 2002). For safety reasons – to not interfere with cardiac innervation – tVNS is provided to the left afferent branch of the vagus towards the brain (Van Leusden et al., 2015). The left and right vagus nerve innervate the heart differently (Ardell and Randall, 1986) and due to the low intensity of tVNS, stimulating the afferent vagus is not a necessary requirement for efferent parasympathetic effects.

Several behavioral studies have demonstrated the causal role of the vagus nerve in emotion recognition by applying tVNS to the afferent branch of the vagus (Colzato et al., 2017; Sellaro et al., 2018). Although the evidence for tVNS-effects on the processing of socially relevant stimuli is still emerging, there is consistent support for the role of the vagus in emotion recognition and social functioning (Geisler et al., 2013; Kemp et al., 2012; Kok and Fredrickson, 2010; Quintana et al., 2012). Therefore, the use of tVNS allows us to provide further evidence on the causal role of the vagus in the mechanisms of social perception.

Colzato et al. (2017) showed that tVNS promoted the ability of inferring people's emotional state based on images of the eye region - at least if the emotional state was well-discriminable. In other words, tVNS-induced increase of afferent activity of the ventral vagal complex enhanced the ability to recognize salient social cues. People's fight/flight response strategies are a sympathetic response likely to depend on salient and recognizable social cues, and the homeostatic adjustment between sympathetic and parasympathetic responses relies heavily on the vagus nerve (Damasio et al., 1991). Taken together, the findings converge and support the role of the vagus nerve in regulating social engagement via emotion recognition (Porges, 2007, 2003, 2001).

However, while the findings of Colzato et al. (2017) do suggest an interesting connection between vagal activity and the processing of socially relevant stimuli, the particular design that was used still leaves open different interpretations regarding the nature of this connection. For one, the stimulus set was only comprised of faces expressing specific emotions, so it remains unclear whether tVNS might also enhance the processing of faces not expressing an emotion. For another, the stimulus faces had varying gaze directions, straight towards the participant or averted to either the right or the left. Because in the results from Colzato et al. (2017) gaze was not systematically manipulated, this does not allow to disentangle the impact of the expressed emotion on the one hand, and the social relevance depicted by the gaze on the other. Gaze direction is a critical component of facial processing and emotion recognition (Hamilton, 2016; Kleinke, 1986) and it has been shown that the direction of the gaze influences the allocation of attentional sources when processing facial expressions (Palermo and Rhodes, 2007; Ricciardelli et al., 2012). Finally, it remains unclear whether the tVNS-induced enhancement was attentional in nature. Although not directly manipulated, given that the task required perceptual identification, increased vagal activation might have improved performance by speeding up the perceptual interpretation of the stimuli. However, there is ample evidence that affective stimuli also attract visual attention (Schwabe et al., 2011; Vuilleumier and Schwartz, 2001), which means that performance might also have benefited from vagus-induced increases of attentional resources on processing the affective stimuli.

The main goal of the current study was twofold: first, to disentangle the impact of gaze and emotional expression, and so to test whether tVNS impacts the processing of faces expressing particular emotions, or the processing of faces of particular social relevance to the observer (as manipulated by comparing direct and averted gaze) or both, we varied these two factors orthogonally. And second, we tried to assess the degree to which facial stimuli make use of attentional resources by measuring their after-effects on the processing of a subsequent non-facial stimulus. To achieve our goal, we employed a Rapid Serial Visual Presentation (RSVP) paradigm, a well-established tool to assess the allocation of attention over time, allowing us to investigate how tVNS impacts attentional deployments. If two visual targets appear close in time in a RSVP task, the first target (T1) is typically easy to report, but report of the second target (T2) is dramatically impaired. The shorter the temporal distance between T1 and T2 (the so-called lag), the greater the impairment - a phenomenon known as Attentional Blink (AB; Raymond et al., 1992).

Most theories explain the AB by assuming that processing and consolidating T1 uses so many attentional resources that too little is left for processing and consolidating T2 if it appears too early (Chun and Potter, 1995; Jolicœur and Dell’Acqua, 1998; Vogel et al., 1998). Indeed, manipulating the amount of attentional resources needed to process T1 has been shown to systematically impact the size of the AB (Jackson and Raymond, 2006; Müsch et al., 2012), and individuals that tend to allocate more attentional resources to the processing of T1 exhibit a stronger AB (Colzato et al., 2008a, 2007; Dale and Arnell, 2010; Martens et al., 2006; Martens and Valchev, 2009; Shapiro et al., 2006). Of particular importance for our purposes, the affective salience of the stimuli has been demonstrated to systematically affect the size of the AB (de Jong et al., 2009; Milders et al., 2011; Schwabe et al., 2011) and the AB is shown to be sensitive to the emotional content/meaning (Schwabe and Wolf, 2010; Schwabe et al., 2011) and to gaze direction of T1 (Ricciardelli et al., 2016, 2012). More specifically, when emotional expressions are manipulated at both T1 and T2, a neutral T1 indeed attenuates the AB for emotional T2s but an aversive T1 prolongs the AB (Schwabe and Wolf, 2010; Schwabe et al., 2011). However, it must be noted that the emotional stimuli presented in T1 were words in the studies of Schwabe and Wolf (2010) and Schwabe et al. (2011) - with emotional vs. neutral meaning - while the stimuli used in Ricciardelli et al. (2016, 2012) were pictures of faces. Although the level of processing is across studies is different – more semantic for words (Schwabe et al., 2011; Schwabe and Wolf, 2010) and more visual/perceptual for pictures (Ricciardelli et al., 2016, 2012) - what both groups of results have in common is the emotional meaning of the stimuli and its social relevance. The finding that an emotional T1 eliminates the blink-reducing effect of an emotional T2 suggests that emotionality of T1 is a critical factor in the emotional modulation of the AB (Schwabe and Wolf, 2010). Ricciardelli et al. (2016, 2012) reported that even neutral T2s were found to escape the AB (i.e., showed equal, unimpaired accuracy at all lags), if T1 was an angry face with a gaze that was directed at the participant, but not if the gaze was averted. The authors attributed this effect pattern to the biological significance of T1: due to the arguably stronger bottom-up salience of angry faces with direct gaze, less top-down attention was necessary to process the T1, which left more capacity to process T2 even at short lags.

At the physiological level, evidence suggests that norepinephrine (NE) and cortisol have a regulatory role in modulating attention to emotional stimuli (De Martino et al., 2008; Schwabe and Wolf, 2010) and both markers of noradrenergic function have been shown to be affected by tVNS (Ventura-Bort et al., 2018; Warren et al., 2019). Accordingly, tVNS-induced changes in the allocation of attentional resources devoted to processing T1 would be expected to affect the size of the AB (i.e., should impair T2 processing more for short than for longer temporal distances between T1 and T2), while possible changes of T1 perception should affect T2 processing independently of the temporal distance.

In the current study, we used an emotional RSVP paradigm in which participants were explicitly asked to first discriminate the gender of the target face (T1) with direct (salient social cue) or averted gaze (subtler social cue) when its expression was angry, fearful or neutral, and then to judge the orientation of a landscape (T2) (Ricciardelli et al., 2012, 2016) that was rotated either clockwise or anticlockwise. Gaze direction and emotional expressions were task-irrelevant to control for the spontaneous allocation of attention in processing the facial expression. Formally, our study consisted of the crossing of four independent variables: the emotion that the facial stimuli used as T1 were displaying (angry vs. fearful vs. neutral), the gaze direction of these faces (averted vs. direct), the temporal distance (lag) between T1 and T2 (2 vs. 4 vs. 7), and tVNS stimulation (active vs. sham). We used the same experimental paradigm as in the third experiment described in Ricciardelli et al. (2016), adding tVNS as the main factor of interest for the current study. Because it was not part of our main hypothesis, we had no specific predictions regarding the findings observed in Ricciardelli et al. (2016) and, therefore, we expected to find similar results.

To address our predicted effect of tVNS, statistical tests were guided by the three questions underlying the present study: First, we were interested to see whether tVNS-induced changes in performance, as compared to the sham condition, would differ for angry or fearful versus neutral faces, which would indicate that the effect is specific to emotional stimuli. Second, we were interested in the role of social relevance, which would suggest that tVNS effects would be restricted to stimuli showing direct gaze. And, third, we were interested to see whether tVNS would target attention to social stimuli that are particularly relevant for the observer (i.e., direct gaze), which should lead to an interaction involving lag, or whether, if effects are independent of lag, tVNS could be modulating mechanism of perception.

Section snippets

Participants

An a-priori sample size calculation was performed using G*Power 3.1.7 (Faul et al., 2007) to estimate the approximate number of participants required, considering 0.01 as criterion for statistical significance (the traditional alpha = 0.05 slightly corrected for multiple testing) and a desired power of 0.90 in a within-subjects design with 2 groups and measurements. Based on prior results (Colzato et al., 2017) evidencing the effect of tVNS on emotion recognition, medium effect sizes (r ≈ 0.20)

Personality questionnaires

Participants’ scores on the personality questionnaires were comparable to previous reports (Sellaro et al., 2018), with the average measures of empathy [IRITotal score (M = 73.12, SD = 12.13), IRIPerspective taking (M = 20.30, SD = 4.02), IRIFantasy scale (M = 18.81, SD = 5.80), IRIEmpathic concern (M = 21.12, SD = 4.70), IRIPersonal distress (M = 12.88, SD = 3.62), EQ (M = 49.26, SD = 10.71)], autistic traits [AQ (M = 17.26, SD = 6.83)] and alexithymia [BVAQTotal score (M = 89.58, SD = 18.44),

Discussion

The aim of this study was to provide more insight with respect to three issues that were left open by the study of Colzato et al. (2017). First, we asked whether tVNS-induced changes in performance are specific to emotional faces (faces showing emotional expressions) or whether they also occur for neutral faces. While we found general performance to be better with fearful faces, which might be due to a general increase of arousal induced by these faces, facial expression did not interact with

Funding

This work was supported by research grants from the Netherlands Organization for Scientific Research (NWO) awarded to Lorenza S. Colzato (Vidi grant: #452-12-001) and to Laura Steenbergen (Veni grant: #016.Veni.198.030).

CRediT authorship contribution statement

Maria J. Maraver: Data curation, Formal analysis, Investigation, Methodology, Project administration, Supervision, Validation, Writing - original draft, Writing - review & editing. Laura Steenbergen: Conceptualization, Data curation, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Writing - original draft, Writing - review & editing. Romina Hossein: Data curation, Investigation, Methodology, Project administration, Supervision, Writing - review & editing.

Acknowledgments

The authors are grateful to Luisa Lugli and Antonello Pellicano, who very kindly provided them with the stimuli and the first draft of the E-Prime experiment script.

References (81)

  • E. Frangos et al.

    Non-invasive access to the vagus nerve central projections via electrical stimulation of the external ear: FMRI evidence in humans

    Brain Stimul

    (2015)
  • F.C.M. Geisler et al.

    Cardiac vagal tone is associated with social engagement and self-regulation

    Biol. Psychol.

    (2013)
  • H.I.L. Jacobs et al.

    Transcutaneous vagus nerve stimulation boosts associative memory in older individuals

    Neurobiol. Aging

    (2015)
  • P. Jolicœur et al.

    The demonstration of short-term consolidation

    Cognit. Psychol.

    (1998)
  • K. Kessler et al.

    Target consolidation under high temporal processing demands as revealed by MEG

    Neuroimage

    (2005)
  • B.E. Kok et al.

    Upward spirals of the heart: autonomic flexibility, as indexed by vagal tone, reciprocally and prospectively predicts positive emotions and social connectedness

    Biol. Psychol.

    (2010)
  • R. Palermo et al.

    Are you always on my mind? A review of how face perception and attention interact

    Neuropsychologia

    (2007)
  • S.W. Porges

    The polyvagal perspective

    Biol. Psychol.

    (2007)
  • S.W. Porges

    The polyvagal theory: phylogenetic substrates of a social nervous system

    Int. J. Psychophysiol.

    (2001)
  • D.S. Quintana et al.

    Heart rate variability is associated with emotion recognition: direct evidence for a relationship between the autonomic nervous system and social cognition

    Int. J. Psychophysiol.

    (2012)
  • D. Sander et al.

    A systems approach to appraisal mechanisms in emotion

    Neural Network.

    (2005)
  • L. Schwabe et al.

    Emotional modulation of the attentional blink: the neural structures involved in capturing and holding attention

    Neuropsychologia

    (2011)
  • R. Sellaro et al.

    Transcutaneous vagus nerve stimulation (tVNS) enhances recognition of emotions in faces but not bodies

    Cortex

    (2018)
  • L. Steenbergen et al.

    Transcutaneous vagus nerve stimulation (tVNS) enhances response selection during action cascading processes

    Eur. Neuropsychopharmacol

    (2015)
  • C. Stifter et al.

    Facial expressivity and vagal tone in five- and ten-month-old infants

    Infant Behav. Dev.

    (1989)
  • J.F. Thayer et al.

    A model of neurovisceral integration in emotion regulation and dysregulation

    J. Affect. Disord.

    (2000)
  • H.C.M. Vorst et al.

    Validity and reliability of the bermond-vorst alexithymia questionnaire

    Pers. Indiv. Differ.

    (2001)
  • C.M. Warren et al.

    The neuromodulatory and hormonal effects of transcutaneous vagus nerve stimulation as evidenced by salivary alpha amylase, salivary cortisol, pupil diameter, and the P3 event-related potential

    Brain Stimul

    (2019)
  • N. Yakunina et al.

    Optimization of transcutaneous vagus nerve stimulation using functional MRI

    Neuromodulation

    (2017)
  • R.B. Adams et al.

    Perceived gaze direction and the processing of facial displays of emotion

    Psychol. Sci.

    (2003)
  • E.G. Akyürek et al.

    Adaptive control of event integration: evidence from event-related potentials

    Psychophysiology

    (2007)
  • J.L. Ardell et al.

    Selective vagal innervation of sinoatrial and atrioventricular nodes in canine heart

    Am. J. Physiol. Cell Physiol.

    (1986)
  • S. Baron-Cohen et al.

    The empathy quotient: an investigation of adults with asperger syndrome or high functioning autism, and normal sex differences

    J. Autism Dev. Disord.

    (2004)
  • S. Baron-Cohen et al.

    The Autism-Spectrum Quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians

    J. Autism Dev. Disord.

    (2001)
  • M.M. Chun et al.

    A two-stage model for multiple target detection in rapid serial visual presentation

    J. Exp. Psychol. Hum. Percept. Perform.

    (1995)
  • L.S. Colzato et al.

    Working memory and the attentional blink : blink size is predicted by individual

    Psychon. Bull. Rev.

    (2007)
  • G. Dale et al.

    Individual differences in dispositional focus of attention predict attentional blink magnitude

    Atten. Percept. Psychophys.

    (2010)
  • A.R. Damasio et al.

    Somatic markers and the guidance of behavior: theory and preliminary testing

    Frontal Lobe Function and Dysfunction

    (1991)
  • M.H. Davis

    Measuring individual differences in empathy: evidence for a multidimensional approach

    J. Pers. Soc. Psychol.

    (1983)
  • M.H. Davis

    A multidimensional approach to individual differences in empathy mark

    Cat. Sel. Doc. Psychol.

    (1980)
  • Cited by (17)

    • Evidence for a modulating effect of transcutaneous auricular vagus nerve stimulation (taVNS) on salivary alpha-amylase as indirect noradrenergic marker: A pooled mega-analysis

      2022, Brain Stimulation
      Citation Excerpt :

      Initial brain imaging studies confirmed enhanced functional LC activation during taVNS compared to active sham stimulation in healthy participants [52–57]. Other studies, but not all, showed a modulatory effect of taVNS on various cognitive and affective processes potentially associated with noradrenergic signaling, with respect to fear extinction (see for positive effects [58–60]; but see for no effects [61,62]), memory (see for positive effects [63–65]; but see for no effects [37,66]), cognitive control (see for positive effects [67–71]; but see for no effects [72]) and attention (see for positive effects [73,74]; but see for no effects [75]). Despite the promising indications for taVNS-related behavioral improvements, there is current uncertainty regarding the relation between NA markers and taVNS-mediated vagal activation due to a number of non-replicable or merely subtle findings (cf. [7,51]).

    • Gut Feelings: Vagal Stimulation Reduces Emotional Biases

      2022, Neuroscience
      Citation Excerpt :

      By applying a within-subject sham-controlled design, we therefore investigate the effect of tVNS on the processing of negative and positive information in healthy volunteers. The required sample size was estimated using a power analysis (parameters: power = 0.8, Cohen’s d = 0.5, alpha = 0.05), assuming a moderate effect size based on previous tVNS protocols (Maraver et al., 2020). While the estimated sample size was 34, to provide a buffer the study sought to recruit approximately 40 participants for a within-subject design with two groups (active and sham).

    View all citing articles on Scopus
    View full text