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Received: 1 May 2016 Accepted: 6 August 2016 DOI: 10.1111/bdi.12427
C O M M E N TA RY
Vestibular neuromodulation: stimulating the neural crossroads of psychiatric illness Steven M Miller Monash Alfred Psychiatry Research Centre, Monash University Central Clinical School and The Alfred Hospital and School of Psychological Sciences, Monash University, Melbourne, Vic, Australia
KEYWORDS
anterior cingulate cortex, bipolar disorder, brain stimulation, caloric vestibular stimulation, depression, insight, insula, mania, neuroimaging, neuromodulation
Correspondence Steven M Miller, Monash Alfred Psychiatry Research Centre Level 4, 607 St Kilda Road, Melbourne, Vic, Australia. Email:
[email protected]
In a recent provocative Opinion article in Trends in Cognitive Sciences,
could lead to improved treatments for many psychiatric illnesses, and
Downar et al.1 (see also Goodkind et al.2) draw from quantitative
in turn align psychiatry with neurology as psychiatric illness pathology
meta-analyses of repositories of structural neuroimaging studies to
becomes better defined.
propose a ‟common core” of brain regions whose function is disturbed in a wide variety of psychiatric disorders. Central to this core is the (dorsal) anterior cingulate cortex (ACC) and (anterior) insular cortex (IC). These regions map closely onto a functional anterior cingulo- insular network (aCIN), or ‟salience” network, that has also been
1 | STIMULATING THE COMMON CORE/ aCIN WITH CALORIC VESTIBULAR STIMULATION
identified with meta-analyses of thousands of neuroimaging studies. The psychiatric common core/aCIN is argued to stand at a crossroads
With this line of reasoning, it needs to be commented that there al-
position in the network architecture of the brain, being active during
ready exists a simple, non-invasive brain stimulation technique that is
behavioural self-control, emotion regulation, and social cognition, and
known to reliably activate key nodes of the psychiatric common core/
acting as a switch to deploy other major functional networks mediat-
aCIN. Nearly a decade ago, it was proposed3 that caloric vestibular
ing cognition and emotion. Dysfunction in this ‟hub” role can thus
stimulation (CVS) could potentially treat a wide variety of psychiatric
predispose to multiple psychiatric illnesses such as bipolar disorder,
and neurological conditions, with examples including mania, depres-
major depressive disorder, schizophrenia, obsessive compulsive disor-
sion, persistent pain, post-lesional disorders, schizophrenia, obses-
der, anxiety disorders, post-traumatic stress disorder, attention deficit
sive compulsive disorder, autism, disorders of diminished motivation,
hyperactivity disorder, autism spectrum disorders, eating disorders
catatonia, and movement disorders, and it was suggested that the
and substance dependence disorders.
technique could be applied in still further contexts. Such a proposal
1
Downar et al. also discuss prospects for precisely targeting key
was founded on three central tenets: (i) neuroimaging studies show
nodes of the common core for therapeutic effect, potentially with
that CVS activates ACC, IC, and PN (as well as retroinsular cortex,
broad-spectrum benefits across psychiatric disorders. They review
temporo-parietal areas, and other brain regions), (ii) these brain re-
various brain stimulation methods, such as electroconvulsive therapy
gions are implicated in many psychiatric and neurological conditions,
(ECT), repetitive transcranial magnetic stimulation (rTMS), transcra-
and (iii) CVS induces a wide range of phenomenological effects in
nial direct current stimulation (tDCS), epidural cortical stimulation,
both pathological and healthy brains (Table 1). More recently, meta-
and deep brain stimulation (DBS), and point out that the non-invasive
analysis of CVS neuroimaging studies has confirmed the technique’s
techniques in particular require further development before being able
activation of dorsal (caudal) ACC, anterior IC, and PN.4
to successfully target deeply-situated and relatively focal common
The utility of CVS, which involves irrigation of a small quantity
core nodes like dorsal ACC and anterior IC, as well as relevant subcor-
of cold or warm water into the external ear canal until vertigo is
tical regions such as the putamen (PN) in the basal ganglia. It is sug-
experienced and nystagmus is observed, is well known for neu-
gested that targeting the common core/aCIN with brain stimulation
rological diagnosis. However, the several hundred-year history of
Bipolar Disorders 2016; 1–5
wileyonlinelibrary.com/journal/bdi
© 2016 John Wiley & Sons A/S. | 1 Published by John Wiley & Sons Ltd
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Commentary
2
Table 1 Reported modulations with CVS and additional modulations with GVS
a
for hemispheric lateralization of cognitive style, mood and mood disorders. This model specifically predicted that left-ear CVS would
Postlesional disorders • Attentional, intentional, and representational neglect • Anosognosia • Somatoparaphrenia • Macrosomatognosia • Hemianaesthesia • Aphasic syndrome • Prosopagnosia (GVS) • Figure copying deficit (GVS) • Disturbed arm position sense (GVS) • Postural control • Minimally conscious state
reduce the signs and symptoms of mania (restoring toward normal
Other neurological disorders • Cervical dystonia (GVS) • Autonomic/motor responsiveness in Parkinson’s disease and multisystem atrophy (GVS)
peutic predictions was a report that left-ear CVS induced a striking
Psychiatric disorders • Mania in bipolar disorder and schizoaffective disorder • Insight in mania and schizophrenia • Conversion disorder with involuntary movements
the ‘stuck’ left greater than right imbalance) while right-ear CVS would do the same for depression (restoring toward normal the ‘stuck’ right greater than left imbalance).7
2 | VESTIBULAR NEUROMODULATION OF MANIA AND INSIGHT The first empirical evidence to support these CVS psychiatric therareduction in Young Mania Rating Scale score (from 32 to 10), with a concomitant improvement in insight, in an inpatient in the manic phase of bipolar disorder.8 This patient had become intolerant of pharmacotherapy and refractory to five ECT treatments (despite ECT having been effective for previous episodes) and had been manic for two months. Left-ear CVS caused immediate slowing of thoughts and
Pain disorders • Phantom limb pain and sensations • Complex regional pain syndrome • Spinal cord injury pain • Thalamic pain syndrome (central pain) • Allodynia • Migraine
speech (subjectively and objectively observed), a reduction in spon-
Normal brain functions • Spatial perception and localization • Auditory space perception • Spatial and verbal memory • Visual recall (GVS) • Visual and mental imagery • Binocular rivalry/ambiguous figure perception • Tactile perception • Pain thresholds • Bodily misperception • Positively biased beliefs • Purchase decision-making • Positive and negative mood • Affective control • Sleep and dreams (GVS)
second confirmation of CVS psychiatric therapeutic predictions came
CVS, caloric vestibular stimulation; GVS, galvanic vestibular stimulation. a As cited in Miller and Ngo3 and Grabherr et al.,5 and in the text. Other reported effects of vestibular stimulation, particularly motion-induced stimulation in neurodevelopmental disorders, are not listed here but can be found in Grabherr et al.5
taneous laughter and movement, calming of behaviour, and embarrassment regarding recent behaviour. This effect of CVS remained evident 24 hours later and had fully diminished by 72 hours. It was able to be repeated with a second stimulation with a longer duration of effect (although longer-term outcomes were not reported). A in a report that a patient with schizoaffective disorder exhibited a response to left-ear, but not right-ear, CVS, with reduced mania, including reduced psychomotor agitation, increased insight, and calmer, more cooperative behaviour.9 In this case, the effect lasted 20 minutes, had diminished by 60 minutes, and was repeatable. Consistent with these case studies, it has also been shown that CVS modulates both affective control and mood in healthy subjects.10 In that study, drawing on lateralized CVS mood modulation predictions,7 16 participants received left-ear CVS and sham CVS while another 16 received right-ear CVS and sham CVS. An affective Go/NoGo task was employed, utilizing pictures from the International Affective Picture System. Affective control in response to target pictures improved following right-ear CVS when viewing positive stimuli but decreased following left-ear CVS, relative to sham stimulation. In addition, positive mood ratings on the Positive and Negative Affect Schedule decreased following left-ear CVS, again relative to sham stimulation (although with no effect on
attempting to treat psychiatric illness with vestibular stimulation
mood ratings following right-ear CVS). Also in healthy subjects, CVS
(usually motion-induced stimulation) is far less known.5 In the mid-
has been shown to modulate binocular rivalry.11 Binocular rivalry
late 20th century, reports also emerged of the remarkable ability
is a visual switching phenomenon that has been repeatedly shown
of cold left-ear CVS – which predominantly activates right-sided
to be anomalous in bipolar disorder,7,12–14 to have substantial ge-
structures – to temporarily reverse unilateral attentional neglect
netic basis,15 and to be a candidate endophenotype for bipolar
and anosognosia (denial of illness) associated with right-hemisphere
disorder.3,16,17
stroke.6 Subsequently, a model of bipolar disorder - the ‘Sticky
Furthermore, following suggestion that CVS be applied in deci-
Interhemispheric Switch’ model - was proposed based on new find-
sion-making contexts3, it was recently shown that left-ear CVS relative
ings of slow binocular rivalry in bipolar disorder (see below) and
to sham stimulation in healthy subjects reduces purchase probability
CVS modulation of binocular rivalry, as well as existing evidence
and the desirability of products.18 Extrapolated to a clinical context,
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3
Commentary
this finding is consistent with the excessive spending and risky finan-
It is worth pointing out though, that CVS additionally activates re-
cial decision-making observed in mania. Vestibular stimulation also
gions outside of the common core/aCIN.3,4 However, the ability of CVS
has (complex) effects on sleep in healthy subjects, and interestingly
to activate from the periphery, vestibular subcortical and cortical targets
in the context of mania, historical records refer to the sedating and
linked to balance, orienting behavior, movement, spatial attention, vision,
sleep-promoting effects of rotation apparatuses.5,19
insight, social cognition, decision-making, motivation, impulse control,
The immediate post-CVS restoration of insight in mania in the case
salience and reward processing, error detection, interoception, bodily
studies described earlier resembles the immediacy of responses ob-
representation, homeostasis, autonomic function, pain, affect, and mood,
served in right-sided stroke patients who deny their left hemiplegia
may represent a key advantage over other stimulation techniques which
(anosognosia) or confabulate to explain it.20,21 Following left-ear CVS,
attempt to intervene only at particular points along this ancient neural
such patients rapidly accept and acknowledge their hemiplegia, and
pathway.3 Nonetheless, further research is needed to fully understand
dispense with confabulation, with the effect usually diminishing around
lateralization of both CVS activations4 and mood disorder modulation,26
20 minutes following stimulation. These similarities between insight
a full discussion of which is beyond the scope of this commentary. These
improvements following left-ear CVS in mania and in right-hemisphere
issues for further investigation need not delay examination of CVS as a
stroke, along with existing comparisons between anosognosia and a
readily accessible neuromodulation procedure in clinical psychiatry. The
lack of insight in schizophrenia, led to prediction that left-ear CVS
next step is for CVS studies to employ larger sample sizes, repeated stim-
might also improve insight in schizophrenia.3 This too has since been
ulation protocols, placebo/sham controls (particularly controlling for the
demonstrated in two such cases.9 In addition, consistent with predic-
cold arousal component of CVS), and adequate longer-term follow-up.
3
tions regarding CVS modulation of belief, a study in which 31 partici-
This is beginning to occur in neurological contexts, such as daily right-
pants received left-and then right-ear CVS successively, showed only
ear CVS for four weeks improving aphasic syndrome in left-hemisphere
left-ear CVS attenuated unrealistically optimistic thoughts regarding
stroke27 and disturbed arm position sense in poststroke neglect improv-
Those authors concluded, on the
ing with galvanic vestibular stimulation (GVS)28 relative to sham stimula-
basis of CVS neuromodulation findings, that a unitary mechanism un-
tion29 (note that GVS does not appear to activate ACC).4 There are also
derlies both anosognosia in stroke patients and unrealistic optimism in
reports of GVS relative to sham GVS improving autonomic, motor and
healthy subjects (see also Gerretsen et al.23). An excess of unrealistic
other functions in Parkinson’s Disease and other central neurodegener-
optimism is also, of course, characteristic of mania, and many of the
ative disorders,30–33 and early evidence that repeated CVS for several
psychiatric and behavioural disorders discussed by Downar et al.,1 and
weeks can induce behavioural improvement in the minimally conscious
even general medical disorders,24 involve reduced insight.
state.34 Moreover, following reports of persistent pain and allodynia
the likelihood of future illness.
22
modulation by CVS in case studies and small case series (discussed in
3 | EXAMINING THE THERAPEUTIC EFFICACY OF VESTIBULAR NEUROMODULATION
Miller and Ngo3; see also McGeoch et al.35), a recent study36 examined 34 subjects with persistent (mostly neuropathic) pain and found that (i) a single session of right-ear CVS induced small but statistically significant short term modulations of pain relative to a forehead icepack cold-arousal control condition, (ii) three of nine subjects with allodynia
While not escaping the attention of cognitive neuroscientists, the
had large, clinically significant CVS modulations, and (iii) CVS was well
remarkable reports described above of CVS neuromodulation of psy-
tolerated, with only one subject experiencing vomiting.
chiatric illness, and supporting studies in healthy subjects, have not
The gold standard for assessing therapeutic efficacy however is the
attracted the attention of clinical psychiatrists, research psychiatrists,
double-blind randomized placebo-controlled trial (RCT). RCTs of re-
and psychiatric brain stimulation researchers. This may be due to a
peated CVS (rCVS) are needed for mania, depression (both bipolar and
general unawareness of such reports, or perhaps even to incredu-
unipolar depression), persistent pain, postlesional conditions, and other
lity that a simple, inexpensive, nontechnological, and nonspecialized
psychiatric and neurological disorders.3,5 RCTs of repeated GVS (rGVS) in
brain stimulation technique – indeed, a bedside neuromodulation
hemispatial neglect have commenced, with enduring therapeutic bene-
technique – could possibly modulate conditions such as mania and
fits reported37 (see also Schindler et al.38; though see Ruet et al.39 for a
schizophrenia. However, with the recent proposal of common core/
negative study). The call for RCTs of rCVS (and rGVS) in psychiatry should
aCIN nodes of dorsal ACC and anterior IC (with PN as a relevant
ring particularly loudly, given issues with current therapeutic brain stim-
subcortical region as well),1,2 and existing meta-analytical evidence
ulation options,40–45 including: (i) complexity of administration variables,
for activation by CVS of dorsal (caudal) ACC, anterior IC, and PN,4
(ii) modest therapeutic effects with rTMS and controversial effects with
the case for examination of CVS psychiatric neuromodulation is now
tDCS, (iii) invasiveness and expense of DBS, with disappointing effi-
strong. Indeed, given the wide-ranging phenomenological modula-
cacy for depression, and (iv) inconvenience and potential side-effects
tions known to occur following CVS (Table 1), particularly clinical psy-
of anaesthesia-requiring ECT. CVS, however, is noninvasive, safe (with
chiatric modulations, the technique itself provides further evidence
guidelines regarding medical contraindications46), inexpensive, easy to
in support of the common core/aCIN proposal. It may also shed light
administer (outlined in Miller and Ngo3), and uncomplicated by adminis-
on other commonalities between psychiatric symptoms and the ves-
tration variables (just left-vs right-ear; although with emerging opportu-
tibular system.25
nities for CVS technological developments).27,34 These features should
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make for relatively straightforward examination of CVS as a therapeutic option in clinical psychiatry and application of CVS as a research tool in cognitive neuroscience and biological psychiatry. Indeed, confirmation of mood improvement in mania and depression with left- and right-ear CVS, respectively, would provide strong support for the Sticky Switch model of bipolar disorder from which such therapeutic predictions arose.7 Moreover, such confirmation may help explain recent findings of corpus callosum and (lateralized) ACC white matter deficits in bipolar disorder.47,48 Finally, it should be noted that the model does, however, imply that induction of mania or depression from repeated right- or leftear CVS, respectively, needs to be considered and monitored for, particularly for psychiatric but also for neurological treatment indications.
4 | CONCLUSIONS While well known as a neurological diagnostic technique, vestibular stimulation has also historically been examined for psychiatric symptom modulation. Only recently, however, has there been clear documentation of the potentially therapeutic psychiatric effects of activating the vestibular system. CVS is a simple, safe, and inexpensive neuromodulation technique, now with ample evidence to suggest that it should be carefully examined for therapeutic efficacy in a variety of psychiatric and neurological conditions. With the common core/ aCIN proposal,1,2 and known activations of nodes in this network by CVS,3,4 evaluating the therapeutic efficacy of CVS becomes an even more urgent priority. The urgency lies not just in illustrative cases of refractory bipolar disorder as described above,8 but also in the field’s obligation to openly examine potential clinical translation of findings from psychiatric neuroimaging studies that have involved tens of thousands of patients1 and to examine noninvasive ahead of invasive potential therapies. The range of psychiatric disorders that may respond to CVS is large, given many such disorders exhibit structural or functional abnormalities in common core nodes;1–3 however, mania, depression and disorders with reduced insight stand out as promising initial candidates.3,7–9 If therapeutic efficacy of CVS is proven, a final common pathway of vestibular neuromodulation for psychiatric and neurological illnesses would indeed align these clinical disciplines. ACKNOWLE DGE ME N TS This work was supported by a grant from Monash Institute of Medical Engineering. D ISCLOSURE The author of this paper does not have any commercial associations that might pose a conflict of interest in connection with this manuscript.
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How to cite this article: Miller, S. M. (2016), Vestibular neuromodulation: stimulating the neural crossroads of psychiatric illness. Bipolar Disorders, 0: 1–5. doi: 10.1111/bdi.12427
