Elsevier

Neuropsychologia

Volume 160, 17 September 2021, 107965
Neuropsychologia

Galvanic Vestibular Stimulation influences risk-taking behaviour

https://doi.org/10.1016/j.neuropsychologia.2021.107965Get rights and content

Highlights

  • Vestibular signals play an important role in behavioural control strategy.

  • Galvanic Vestibular Stimulation (GVS) modulates risk-taking behaviour.

  • Left anodal GVS reduces risky choices compared to right anodal GVS.

  • GVS may induce changes in cortical excitability in behavioural control networks.

Abstract

Risk-taking behaviour is an essential aspect of our interactions with the environment. Here we investigated whether vestibular inputs influence behavioural measurement of risk-taking propensity. We have combined bipolar Galvanic Vestibular Stimulation (GVS) with a well-known and established risk-taking behaviour task, namely the Balloon Analogue Risk Task (BART). A sham stimulation was used to control for non-specific effects. Left-anodal and right-cathodal GVS (L-GVS), which preferentially activates the vestibular projections in the right hemisphere, decreased the willingness to take risk during the BART compared with right-anodal and left-cathodal GVS (R-GVS), which activates the left hemisphere. This proved a specific vestibular effect which depends on GVS polarity. Conversely, no generic vestibular effect, defined as the adjusted average of L-GVS and R-GVS conditions compared to sham, emerged, excluding non-specific vestibular effects. Our results confirmed recent findings of a vestibular contribution to decision-making and strategy control behaviour. We suggest that the vestibular-mediated balancing of risk seeking behaviour is an important element of the brain's capacity to adapt to the environment.

Introduction

Risk is ubiquitous in human life. We make decisions in a continuously changing environment balancing expectations, internal states and possible consequences. Whenever these decisions involve potential harm or even danger, while providing the opportunity to gain rewards as a result, we talk about risk-taking behaviour (Leigh, 1999). Although some amount of hazardous behaviour is desirable and essential for survival and environmental adaptation, excessive risk-taking tendencies have been described in association with several clinical conditions, including compulsive gambling and drug abuse (Mishra et al., 2010; Schneider et al., 2012).

Vestibular information has been traditionally considered a specific sensory input for basic orienting behaviours, such as oculomotor adjustments, postural control, balance and gaze stabilisation (Angelaki and Cullen, 2008). The vestibular system in the inner ear comprises three orthogonal semicircular canals (anterior, posterior and horizontal) that sense rotational acceleration of the head in three-dimensional space, and two otolith organs (utricle and saccule) that jointly sense translational acceleration, including the orientation of the head relative to gravity. Human neuroimaging studies have identified several cortical areas involved in vestibular processing in the brain, including the Temporo-Parietal Junction (TPJ), posterior insula, superior temporal gyrus, Inferior Parietal Lobule (IPL), Anterior Cingulate Cortex (ACC), fronto-parietal operculum, both primary and secondary somatosensory cortices and the prefrontal cortex (Lopez et al., 2012a, 2012b; Zu Eulenburg et al., 2012). This widespread vestibular cortical network is primarily located in the non-dominant right hemisphere in right-handed subjects (Dieterich et al., 2003; Duque-Parra, 2004). Notably, this unique neuroanatomical architecture suggests a vestibular contribution to cognition that goes far beyond the traditional, automatic, low-level reflex motor circuits for balance, gaze stabilisation and orientation (Ferrè and Haggard, 2020). Accordingly, artificial vestibular stimulation has been shown to modulate an impressive range of cognitive functions, including spatial attention, decision-making, body-representation, memory, motor and spatial imagery and emotion perception (Ferrè et al., 2013a, 2013b; Ferrè and Haggard, 2020; Hilliard et al., 2019; Lenggenhager et al., 2008; Lopez et al., 2012a, 2012b; Miller, 2016; Pasquier et al., 2019; Preuss et al., 2017; Schmidt et al., 2013a, 2013b; Wilkinson et al., 2008).

Recent studies have demonstrated that vestibular signals play an important role in behavioural control strategy, influencing the balance between novel and routine responses in implicit decision-making tasks (Ferrè et al., 2013a, 2013b). Bipolar Galvanic Vestibular Stimulation (GVS) was used to non-invasively stimulate the vestibular organs (Fitzpatrick and Day, 2004). An anode and cathode were placed on the left and right mastoid, or vice versa. Perilymphatic cathodal currents are known to depolarize the trigger site and lead to excitation, whereas anodal currents hyperpolarize it resulting in inhibition (Gensberger et al., 2016; Goldberg et al., 1984; Minor and Goldberg, 1991). Galvanic currents equally affect the afferents innervating all five vestibular endorgans resulting in a change in the vestibular nerve afferent discharge. GVS results in a diffuse activation of the cortical and subcortical vestibular projections (Fitzpatrick and Day, 2004). Neuroimaging evidence has shown that left-anodal and right-cathodal GVS caused a unilateral activation of the right hemisphere vestibular projections, while the inverse polarity activated both left and right hemispheres (Fink et al., 2003). We have observed polarity-specific effects in a decision-making task: left-anodal and right-cathodal GVS, which primarily activates the right hemisphere vestibular projections, increased novel responses compared to right-anodal and left-cathodal GVS (Ferrè et al., 2013a, 2013b).

However, it remains unclear whether vestibular information might also modulate the willingness of taking risks. Here we have combined bipolar GVS with a well-known and established risk-taking behaviour task, namely the Balloon Analogue Risk Task (BART) (Lejuez et al., 2002, 2003). The BART has been widely used to implicitly measure the behavioural measurement of risk-taking propensity in adolescents (Lejuez et al., 2003), drug abusers (Campbell et al., 2013; Canavan et al., 2014), brain-injured patients (Balagueró et al., 2016) and psychopathic inmates (Swogger et al., 2010). Neuroimaging studies described activations of ACC, medial-frontal cortex and dorsolateral-frontal cortex, and insula when participants were asked to perform the BART (Li et al., 2020; Schonberg et al., 2012). We have therefore hypothesized that GVS might induce a polarity-specific modulation of risk-taking behaviour during the BART.

Section snippets

Participants and ethics

Twenty healthy right-handed participants volunteered in the study (19 women; age range 18–22 years; mean = 19 years; SD = 1.28 years). The sample size was estimated a priori based on similar experimental procedures (Ferrè et al., 2013a, 2013b). The sample size was set in advance of testing and was also used as data-collection stopping rule. Participants with a history of neurological, psychiatric, vestibular or auditory disorders were excluded. Informed consent was obtained prior to

Results

The proportion of exploded balloons in each GVS condition was numerically similar (L-GVS = 0.24, SD = 0.12; R-GVS = 0.28, SD = 0.15; SHAM = 0.29, SD = 0.16) ruling out a potential impact of the exploded balloons on subsequent choices made by participants.

First, we investigated whether any activation of the vestibular system might influence risk-taking behaviour independently of GVS polarity and hemispheric effects, perhaps because of non-vestibular effects such as changes in general arousal.

Discussion and conclusion

Successfully dealing with risks is a fundamental aspect of human adaption to the surrounding environment. Here we show that vestibular input, in general, did not modulate the cognitive processes involved in risk-taking propensity. However, specific polarities of vestibular input, associated with activation of vestibular projections in each hemisphere separately, had differential effects on risk-taking behaviour. In particular, L-GVS induced a significant reduction in risk tendencies compared to

Ethics approval and consent

The experimental protocol was approved by Royal Holloway University of London research ethics committee. Consent to participate and for publication were asked to participant according to ethical standards of the Declaration of Helsinki.

Funding

This work was supported by a European Low Gravity Association Research (ELGRA) Prize to E.R.F.

Data availability

Data are available as supplementary information.

Declaration of competing interest

The authors declared that they had no conflicts of interest with respect to their authorship or the publication of this article.

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