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Laboratory of Neuromotor Physiology, IRCCS Santa Lucia Foundation, 00179, Rome, Italy
Centre of Space BioMedicine, University of Rome Tor Vergata, 00173, Rome, Italy
Department of Medical and Surgical Sciences, University Magna Graecia, Catanzaro, Italy
d
Department of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, USA
e
Department of Systems Medicine, Neuroscience Section, University of Rome Tor Vergata, 00133 Rome, Italy
f
Institute of Bioimaging and Molecular Physiology, National Research Council 88100, Catanzaro, Italy
b
c
a r t i c l e
i n f o
Article history:
Received 20 March 2014
Received in revised form 31 July 2014
Accepted 5 September 2014
Keywords:
Anxiety
Neuroticism
Introversion
Sound-evoked vestibular stimulation
fMRI
Chronic subjective dizziness
a b s t r a c t
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 identied 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 rst 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 reect risk factors for anxiety-related morbidity in patients with vestibular
disorders, including previously observed associations of neuroticism and introversion with CSD.
2014 Elsevier Inc. All rights reserved.
Introduction
Anxiety inuences 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 denition 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 condence, and higher autonomic
arousal [39]. Individuals with high trait anxiety stiffened their stance
under modest stress that did not alter postural control of those with
Corresponding author at: Santa Lucia Foundation, Via Ardeatina 306, 00179 Rome
Italy.
E-mail address: i.indovina@hsantalucia.it (I. Indovina).
http://dx.doi.org/10.1016/j.jpsychores.2014.09.005
0022-3999/ 2014 Elsevier Inc. All rights reserved.
392
393
Table 1
Correlation between sound-evoked brain vestibular responses and personality traits
Positive
Negative
P
0.045
3.60
56
58
42
B. Extraversion
Amygdala R (ReS)
0.008
3.38
24
24
C. Openness
IFg (Triang) L (ReS)
0.014
3.97
52
34
12
A. Neuroticism
Cerebellar nuclei L (ReS)
Cerebellar nuclei R (ReS)
Pontine nuclei L (ReS)
Pontine nuclei R (ReS)
Visual cortex L (V2) (LeS)
SMg L (PFm) (LeS)
0.002
0.005
0.009
0.030
0.009
3.85
3.53
3.81
3.38
4.17
8
2
2
2
18
52
54
22
24
102
24
24
26
24
4
Correlation between sound-evoked brain vestibular responses (STB100dB vs. STB 65 dB excluding white noise vs. rest related activity) and personality traits at P b 0.05, small volume
correction. Activations in the visual area (V2) and SMg refer to the Left ear Stimulation (LeS) while activations in the cerebellum, amygdala and IFg (Triang) refer to the Right ear
Stimulation (ReS).
Z = Z-score, L = left hemisphere, R = right hemisphere. x,y,z = MNI coordinates in millimeters. SMg = supra marginal gyrus, IFg (triang) = inferior frontal gyrus pars triangularis.
Fig. 1. Main effects of vestibular and acoustic stimulation. Statistical parametric maps (shown at P b 0.001 uncorrected for visualization purposes) for the STB100dB N rest comparison (A),
STB65dB N rest (B), modulated white noise 100 dB N rest (C), and STB100dB N STB65dB exclusively masked for white noise (D). Maps are separately reported for right and left ear
stimulation in normalized sterotactic space, overlaid on a high-resolution anatomical MR image (CH2, Montreal Neurological Institute), with the right side shown on the right. Sagittal,
coronal and axial slices are centered on the rst peak relative to each contrast reported on Supplementary Table S1.
394
Image acquisition
Image pre-processing
Fig. 2. Effect of individual differences in neuroticism on brain activations during unilateral sound-evoked vestibular stimulation. Neuroticism scores were positively associated with the
activity in the cerebellar fastigial nuclei (A), and superior pons (B) during right saccular stimulation, and with parastriate visual cortex (V2) response during left saccular stimulation
(C). In contrast, neuroticism levels were negatively linked with the response in the supra-marginal gyrus (SMg) during left ear stimulation (D). The plots of the data are from the local
maxima in each region. The coordinates (X,Y,Z) are in the Montreal Neurological Institute space. Color bars represent T-statistics. Black lines represent the regression lines. Red lines
are the 95% condence interval. BOLD, blood oxygenation level dependent.
395
Fig. 3. Effect of individual differences in introversion on brain activations during right ear
vestibular stimulation. Introversion scores were positively associated with the activity in
the right amygdala during right saccular stimulation. The plot of the data is from the
local maxima in the amygdala. The coordinates (X,Y,Z) are in the Montreal Neurological
Institute space. The color bars represents T-statistics. Black line represents the regression
line. Red lines are the 95% condence interval. BOLD, blood oxygenation level dependent.
396
Fig. 4. Effect of individual differences in neuroticism on brain functional connectivity during sound-evoked vestibular stimulation. During right saccular stimulation, neuroticism scores
were positively associated with the functional connectivity between the left cerebellar fastigial nucleus seed region and the right amygdala (A), and with the functional connectivity
between the superior pons seed and the right amygdala (B). During left saccular stimulation, neuroticism levels were positively linked with the functional connectivity between the
left para-striate visual cortex (V2) seed and the left inferior frontal gyrus (IFg) pars triangularis (C) and with the connectivity between the left supra-marginal gyrus (SMg) seed
and the left IFg pars triangularis (D). The plots of the data are from the local maxima in each region. The coordinates (X,Y,Z) are in the Montreal Neurological Institute space. Color bars
represent T-statistics. Black lines represent the regression lines. Red lines are the 95% condence interval. BOLD, blood oxygenation level dependent.
397
Table 2
Regional coupling during sound-evoked response as a function of personality
A. Coupling correlates with neuroticism.
Target:
Seed:
IFg (Triang) L
P
Cerebellar nuclei
L (ReS)
Pontine nuclei L
(ReS)
Visual cortex L
0.002 4.61 52 18
(V2) (LeS)
SMg L (LeS)
0.034 3.84 34 32
Amygdala R
z
0.006 3.54
18 2 16
0.044 2.83
18 2 16
22
18
IFg (Orb) R
P
0.003 4.51
IFg (Orb) L
y
36 24 22 0.034 3.86 20
14 20
Correlation of coupling (between SEED and target areas) and personality traits at P 0.05,
small volume correction. SEED areas are from Table 1, TARGET areas are those areas that
showed a signicant dependence of coupling on personality traits in the PPI analysis.
Z = Z-score, L = left hemisphere, R = right hemisphere. x,y,z = MNI coordinates
in millimeters. SMg = supra marginal gyrus, IFg (Orb) = inferior frontal gyrus pars
orbitalis.
and Conscientiousness (52.0, 33.568.1). Mean T-scores were within general population
norms (4555), except for minimally elevated openness. Individual T-scores covered the
full range from low (b45) to high (N55) for all ve traits.
Discussion
Effect of personality traits on vestibular and anxiety system activation
Neuroticism scores correlated (Table 1A): 1) positively with bilateral cerebellar
fastigial nuclei and pontine activity during right ear stimulation (Fig. 2A, B); 2) positively
with left V2 cortical activity during left ear stimulation (Fig. 2C); and 3) negatively with
the left SMg activity during left ear stimulation (Fig. 2D). Extraversion-introversion scores
did not correlate with stimulated activity in predominately vestibular regions. Openness
scores correlated negatively with left IFg activity during right ear stimulation (Table 1C).
Agreeableness and consciousness scores did not signicantly modulate activity in any
ROI during right or left vestibular stimulation (all analyses refer to STB100dB N STB65dB
contrast, exclusively masked for the white-noise 100dB N rest contrast) (P b 0.05, FWE,
svc).
Extraversion scores correlated negatively (i.e., introversion correlated positively)
with right amygdala activation during right ear stimulation (Fig. 3 and Table 1B).
Other traits did not correlate with stimulated activity in predominately anxiety
regions.
The results, summarized in Fig. 6, support the latest models integrating vestibular and anxiety function in health and disease [2], and are
consistent with ndings regarding neuroticism and introversion as
risk factors for CSD [48]. They offer the rst evidence of possible neural
mechanisms linking personality traits to functional alterations in central
vestibular pathways and support the suppositions that: (1) central
vestibular systems may be more reactive to vestibular stimuli than
normal (in neurotic individuals), (2) anxiety systems may be more
reactive to vestibular stimuli than normal (in introverted individuals),
and (3) increased connectivity between subcortical vestibular and
anxiety systems may facilitate amplied vestibularanxiety reactions
to vestibular stimuli (in neurotic individuals).
Consistently with past studies [31], the posterior insula showed
robust activation to vestibular stimuli across all participants, but surprisingly, its response did not correlate with any personality trait. This
null result is in contrast to previous ndings showing that the insula
response during cognitive and emotional tasks may be modulated by
individual differences in anxiety-related traits [25,78,79]. It may be
that the sound-evoked vestibular stimulation was insufcient per se
to trigger altered insula responses in healthy individuals with variable
levels of neuroticism, while these effects may become evident in clinical
populations (e.g., CSD patients). Further studies are warranted to
explore these issues.
398
Fig. 6. Summary of regional effects and functional connectivity results. Neuroticism was positively correlated with activity in cerebellar fastigial and superior pontine nuclei and with functional connectivity between these nuclei and the right amygdala during vestibular stimulation. These ndings reect potentiated processing of vestibular inputs in neurotic people that
may predispose them to enhanced viscero-motor and emotional responses to space-motion stimuli. Introversion was linked with increased amygdala response to vestibular stimuli
and reduced functional connectivity between the right amygdala and IFg pars orbitalis bilaterally. These results may be neural correlates of enhanced acquisition or decreased extinction
of fear conditioned responses to vestibular stimuli that are thought to play a role in development of specic phobias of falling and chronic subjective dizziness. Neuroticism levels were
positively associated with increased activity in the parastriate visual cortex (V2) and reduced response in the supra-marginal gyrus (SMg) during vestibular stimulation. Neuroticism
also modulated the connectivity between the IFg pars triangularis and both the V2 and SMg. The combination of SMg hypoactivity and V2 hyperactivity may reect a visual bias in the
reciprocally inhibitory connectivity of vestibular and visual cortices modulated by the IFg pars triangularis, a key region in attentional modulation. The lines connecting different brain
areas represent the positive (continuous lines) or negative (dotted lines) correlation of the inter-regional connectivity with the personality factor indicated within the black arrow.
399
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