Personality traits modulate subcortical and cortical vestibular and anxiety responses to sound-evoked otolithic receptor stimulation

Highlights

• First fMRI study of personality traits and brain responses to vestibular stimuli

• Neuroticism correlated with increased subcortical vestibular system responses.

• Introversion correlated with increased amygdala responses.

• Neuroticism correlated with increased vestibular–anxiety system connectivity.

• Findings support published neuroanatomical models of vestibular–anxiety interactions.

Abstract

Objective

Strong links between anxiety, space-motion perception, and vestibular symptoms have been recognized for decades. These connections may extend to anxiety-related personality traits. Psychophysical studies showed that high trait anxiety affected postural control and visual scanning strategies under stress. Neuroticism and introversion were identified as risk factors for chronic subjective dizziness (CSD), a common psychosomatic syndrome. This study examined possible relationships between personality traits and activity in brain vestibular networks for the first time using functional magnetic resonance imaging (fMRI).

Methods

Twenty-six right-handed healthy individuals underwent fMRI during sound-evoked vestibular stimulation. Regional brain activity and functional connectivity measures were correlated with personality traits of the Five Factor Model (neuroticism, extraversion-introversion, openness, agreeableness, consciousness).

Results

Neuroticism correlated positively with activity in the pons, vestibulo-cerebellum, and para-striate cortex, and negatively with activity in the supra-marginal gyrus. Neuroticism also correlated positively with connectivity between pons and amygdala, vestibulo-cerebellum and amygdala, inferior frontal gyrus and supra-marginal gyrus, and inferior frontal gyrus and para-striate cortex. Introversion correlated positively with amygdala activity and negatively with connectivity between amygdala and inferior frontal gyrus.

Conclusions

Neuroticism and introversion correlated with activity and connectivity in cortical and subcortical vestibular, visual, and anxiety systems during vestibular stimulation. These personality-related changes in brain activity may represent neural correlates of threat sensitivity in posture and gaze control mechanisms in normal individuals. They also may reflect risk factors for anxiety-related morbidity in patients with vestibular disorders, including previously observed associations of neuroticism and introversion with CSD.

Introduction

Anxiety influences postural control and locomotion in health and disease, though neural mechanisms responsible for these effects are incompletely understood. In the 1870s, publication of the original definition of agoraphobia (i.e., spatial disorientation and fear in busy town squares) sparked debates about interactions among anxiety, spatial orientation, and gait [1]. A century later, these interactions were investigated in clinical and laboratory studies [1], [2]. Healthy people, when positioned at height, were found to have a stiffer stance and experience greater state anxiety, lower balance confidence, and higher autonomic arousal [3], [4], [5], [6], [7], [8], [9]. Individuals with high trait anxiety stiffened their stance under modest stress that did not alter postural control of those with low trait anxiety [10]. Conversely, vestibular disorders were identified as potent triggers of secondary anxiety disorders [11], [12], [13], [14], [15], [16], [17], [18] and elevated state anxiety was associated with lower functional status [19] and poorer treatment outcomes [19], [20].

Animal studies provided evidence about important neural connections between subcortical anxiety and vestibular systems [21], [22], [23], [24], [25], [26]. Information about head motion is conveyed from vestibular labyrinths to vestibular nuclei, and then to pathways that control oculomotor and spinal reflexes, modulated by loops through the cerebellum. This information reaches systems that mediate affective responses via pathways from vestibular nuclei through the pontine nuclei to the amygdala [2], [21], [22], [23]. In the cortex, vestibular, visual, proprioceptive, and somatosensory information about space and motion reach associative regions via the thalamus. In monkeys, the core vestibular cortex is called the parieto-insular vestibular cortex. The human homologue of this region includes sylvian and peri-sylvian areas at the interface between the posterior- and retro-insula, posterior superior temporal gyrus (STg) and parietal operculum. Neuroimaging studies showed that human vestibular cortical network includes the inferior parietal lobule [supra-marginal gyrus (SMg), temporo-parietal junction and ventral intra-parietal area], parts of the prefrontal cortex [e.g., the inferior frontal gyrus (IFg)], and the anterior cingulate cortex and hippocampus [27], [28], [29], [30], [31], [32], [33]. Vestibular and visual cortices interact in a reciprocally inhibitory manner. Vestibular stimuli activate vestibular cortex and suppress visual cortical function, whereas visual motion stimuli do the opposite [34], [35]. Thus, the human vestibular cortex is a multimodal processor that integrates vestibular, visual, proprioceptive, somatosensory, and motor information [36], [37], [38]. It also overlaps regions that process anxiety and affective responses, particularly in the posterior parietal, insular, hippocampal and prefrontal areas [25], [39], [40], [41]. This may provide the cortical substrate for anxiety to influence vestibular information processing and for vestibular data to affect emotional states.

Researchers have developed increasingly sophisticated models of vestibular–anxiety interactions at subcortical and cortical levels to explain vestibular symptoms in patients with primary anxiety disorders, and secondary anxiety disorders in patients with vestibular illnesses [2], [21], [23]. These models may extend to other conditions with vestibular-anxiety interactions, such as height phobia and phobic postural vertigo [42], [43] or chronic subjective dizziness (CSD) [2], [44], [45]. The latter two are similar conditions that manifest with chronic non-vertiginous dizziness or unsteadiness exacerbated by upright posture, head motion, and exposure to complex or moving visual stimuli, usually triggered by acute vestibular or balance disorders. They occupy a place in clinical neurotology akin to irritable bowel syndrome in gastroenterology (i.e., independent psychosomatic conditions that occur with or without medical or psychiatric comorbidity). A pre-existing anxiety diathesis may increase the risk of developing CSD [18], [46], add chronic psychiatric comorbidity [18], [46], and reduce treatment response [47]. Personality traits of neuroticism and introversion were more closely associated with CSD than with comorbid neurotologic disorders producing similar levels of vestibular and psychological symptoms [48]. In contrast, resilience, life satisfaction, and strong sense of coherence predicted lower rates of persistent dizziness after acute vestibular illnesses [49]. Thus, personality traits associated with anxiety, specifically neuroticism and introversion may be important factors for anxiety-mediated vestibular conditions.

This untested hypothesis rests on the supposition that neurotic, introverted people compared to non-neurotic, extraverted individuals have: (1) central vestibular systems that are more reactive to vestibular stimuli, (2) anxiety systems that are more reactive to vestibular stimuli, or (3) central vestibular systems that react more strongly to inputs from anxiety systems during vestibular stimulation. To investigate these possible mechanisms, we examined correlations between personality traits of the Five Factor Model (neuroticism, extraversion–introversion, agreeableness, openness, and conscientiousness) measured by the Revised NEO Personality Inventory (NEO-PI-R) [50] and brain activity and connectivity within vestibular and anxiety networks using functional magnetic resonance imaging (fMRI) in healthy volunteers stimulated with short tone bursts (STB) at 100 dB SPL. The STB procedure is known to activate primary afferents in sacculi of the labyrinths and evoke robust responses in vestibular cortical areas [51], [52], [53]. By using healthy and drug-free volunteers imaged while in a comfortably relaxed state, we focused on inherent relationships among personality traits and brain activity during vestibular stimulation in subjects who were free of potential confounds of high state anxiety, vestibular or anxiety disorders, and medications.

We predicted that higher neuroticism and lower extraversion scores (i.e., introversion) would correlate with increased reactivity to STB stimuli in subcortical and cortical vestibular and anxiety regions and greater vestibular–anxiety system connectivity, thereby identifying potential neural substrates for clinical vestibular conditions ranging from comorbid anxiety in vestibular illnesses to CSD and phobias of heights [2].