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Neurocase: The Neural Basis of Cognition
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Smile without euphoria induced by deep brain
stimulation: a case report
a

a

b

b

Takashi Morishita , Kelly D. Foote , Derek B. Archer , Stephen A. Coombes , David E.
bc

cd

e

a

ac

Vaillancourt , Anhar Hassan , Ihtsham U. Haq , Janine Wolf & Michael S. Okun
a

Department of Neurosurgery, Center for Movement Disorders and Neurorestoration,
McKnight Brain Institute, University of Florida College of Medicine, Gainesville, FL, USA
b

Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, FL,
USA
c

Department of Neurology, Center for Movement Disorders and Neurorestoration, University
of Florida College of Medicine, Gainesville, FL, USA

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d

Department of Neurology, Mayo Clinic, Rochester, MN, USA

e

Department of Neurology, Wake Forest School of Medicine, Winston Salem, NC, USA
Published online: 31 Oct 2014.

To cite this article: Takashi Morishita, Kelly D. Foote, Derek B. Archer, Stephen A. Coombes, David E. Vaillancourt, Anhar
Hassan, Ihtsham U. Haq, Janine Wolf & Michael S. Okun (2015) Smile without euphoria induced by deep brain stimulation: a
case report, Neurocase: The Neural Basis of Cognition, 21:6, 674-678, DOI: 10.1080/13554794.2014.973883
To link to this article: http://dx.doi.org/10.1080/13554794.2014.973883

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Neurocase, 2015
Vol. 21, No. 6, 674–678, http://dx.doi.org/10.1080/13554794.2014.973883

Smile without euphoria induced by deep brain stimulation: a case report
Takashi Morishitaa*, Kelly D. Footea, Derek B. Archerb, Stephen A. Coombesb, David E. Vaillancourtb,c, Anhar Hassanc,d,
Ihtsham U. Haqe, Janine Wolfa and Michael S. Okuna,c
a
Department of Neurosurgery, Center for Movement Disorders and Neurorestoration, McKnight Brain Institute, University of Florida
College of Medicine, Gainesville, FL, USA; bDepartment of Applied Physiology and Kinesiology, University of Florida, Gainesville, FL,
USA; cDepartment of Neurology, Center for Movement Disorders and Neurorestoration, University of Florida College of Medicine,
Gainesville, FL, USA; dDepartment of Neurology, Mayo Clinic, Rochester, MN, USA; eDepartment of Neurology, Wake Forest School of
Medicine, Winston Salem, NC, USA

Downloaded by [University of Pennsylvania] at 04:25 22 August 2015

(Received 10 May 2014; accepted 1 October 2014)
Poststroke central pain (PSCP) can be a debilitating medication-refractory disorder. We report a single case where right
unilateral ventral capsule/ventral striatum (VC/VS) deep brain stimulation was used to treat PSCP and inadvertently induced
a smile without euphoria. The patient was a 69 year-old woman who had a stroke with resultant dysesthesia and allodynia in
her left hemibody and also a painful left hemibody dystonia. In her case, VC/VS stimulation induced a smile phenomenon,
but without a euphoric sensation. This phenomenon was different from the typical smile responses we have observed in
obsessive-compulsive disorder cases. This difference was considered to be possibly attributable to impairment in the
emotional smile pathway.
Keywords: deep brain stimulation; chronic pain; smile; ventral capsule; ventral striatum

Poststroke central pain (PSCP) can be medication refractory and debilitating for the majority of sufferers. Pain has
been described as having limbic and sensory components.
There have been various surgical approaches aimed at
specifically targeting each pain component (Sewards &
Sewards, 2002). Motor cortex stimulation (MCS) is the
only food and drug administration-approved surgical procedure for these types of pain patients. Deep brain stimulation (DBS) has been reported to have mixed outcomes
for pain and also does not have a definitive randomized
study supporting its use (Bittar et al., 2005).
In this article, we present a case of a unique DBS
approach that aimed to modulate pain in a patient with
PSCP. In this case, we stimulated the unilateral ventral striatum/ventral capsule (VS/VC) target. The choice of target was
an intentional attempt to address the affective aspects of
PSCP as has been reported in anterior cingulotomy. This
target has been utilized for obsessive-compulsive disorder
(OCD) (Goodman et al., 2010; Greenberg et al., 2006, 2010)
and in medically refractory major depression cases (Malone
et al., 2009), and in both disorders, there has been limited
success. Several authors have reported that DBS in this
region commonly results in intraoperative contralateral
smile with euphoria (Haq et al., 2011; Nuttin et al., 2003;
Okun et al., 2004) and occasionally hypomanic episodes
(Haq et al., 2010; Tsai, Chen, Tsai, Hung, & Chang, 2010).
In this case, we observed an unusual smile response that was
not accompanied by euphoria.

Case report
The patient was a right-handed 69-year-old woman with
history of cerebral infarction in the right middle cerebral
artery region 9 years previous to her DBS surgery. The stroke
lesion involved the cortical areas without directly involving
the basal ganglia (Figure 1). She developed painful and
burning dysesthesias and allodynia in her left hemibody.
She was able to ambulate with a cane until three years ago
and then developed left hemibody dystonia with severe left
foot inward torsion and arm flexion at the elbow and
the wrist. She ambulated only with the use of a wheelchair
or a scooter. She had unsuccessfully tried intrathecal morphine and baclofen, a fentanyl pump, and oral gabapentin
(1600 mg/day) as strategies for the pain. Sertraline (100 mg/
day) was also used, but despite all of these therapies, she
reported only minimal nonmeaningful improvements in pain.
She rated the pain as 8 to 9/10 on a standard visual analogue
pain scale. She reported severe associated depression and a
poor quality of life. On physical examination, the leg dystonia was nearly fixed and could not be manually reduced.
There was severe allodynia of the left upper and lower limbs.
Mild facial weakness on the left was also present. Her baseline modified Rankin scale score was 4.
The DBS procedure was based on our previously published protocol that utilized microelectrode recording (MER)
and macrostimulation (Morishita, Foote, Haq, et al., 2010;
Morishita, Foote, Wu, et al., 2010; Moscovich et al., 2013).

*Corresponding author. Email: tmorishita@fukuoka-u.ac.jp
Present affiliation for Takashi Morishita is Department of Neurosurgery, Fukuoka University Hospital, Fukuoka, Japan.
© 2014 Taylor & Francis

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675

Figure 1. A T1 weighted image showing the stroke lesion in the middle cerebral artery area involving the cortical areas without directly
involving the basal ganglia.

A high-resolution magnetic resonance imaging (MRI)
scan was performed 1 day prior to surgery. On the
morning of the DBS lead implantation, a Cosman–
Roberts–Wells head ring was attached to the skull
under local anesthesia, and then the patient was taken
to a computed tomography (CT) scanner. The CT
images were fused to the MRI. A safe DBS lead trajectory was determined for each target.
MERs were performed to map out the target structures,
and macrostimulation was performed to document stimulation-induced side effects. First, a DBS electrode
(Medtronic, model 3387, Minneapolis, MN, USA) was
implanted in the VC/VS area based on our previously
published procedure for OCD DBS (Figure 2)
(Greenberg et al., 2010; Morishita et al., 2014).
Macrostimulation was then performed. Stimulation of the
most ventral contact (0) was accompanied by an increase
in heart rate. Contralateral smile that rapidly spread to the
ipsilateral face (5–7 volts) was observed without euphoria.
The subject reported “something makes me smile.” She
denied any happy or euphoric feelings during the smile.
This “smile” could be clearly differentiated from facial
muscle movements induced by spread of stimulation to
the internal capsule. The facial muscle movement induced
by the spread of electric current to the internal capsule
usually manifests as a pure unilateral motor response with
and associated subjective uncomfortable feeling. In our
case, the smile response quickly spreads from the contralateral face to the ipsilateral side. Also in our case, the
higher voltage (8–10 volts) resulted in an aggravation of
the burning pain in the left hemibody, but not worsening
facial movements, or other motor (capsular) pulling phenomenon. No acute pain relief was reported with this DBS
lead activation (Table 1).

Figure 2.

Illustration of the VC/VS DBS lead location.

Note: AC = anterior commissure, ALIC = anterior limb of internal
capsule, BN = bed nucleus, CC = corpus callosum, CN = caudate
nucleus, GPe = globus pallidus externa, NAcc = nucleus accumbens,
Vim = ventralis intermedius nucleus, Vo = ventralis oralis.

A second DBS lead implantation was then performed in the same intraoperative session. A single
MER pass was performed for the mapping of the border
between the ventralis caudalis (Vc) and the ventralis
intermedius nucleus (Vim) of the thalamus. We first
implanted an electrode in the Vc region, because of

676
Table 1.

T. Morishita et al.
Postoperative DBS lead location.

DBS
coordinates
X
Y
Z
AC-PC angle
Center-line
angle

Vo

5.5
12
−6.2
56
38

10.5
−1.7
−4.4
79
35

Anatomical lead locations
Ventromedial NAcc

Contact 0
Contact 1
Contact 2

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VC/VS

Dorsolateral NAcc
Intersection of AC and
ALIC
Ventral part of ALIC

Contact 3

Posteromedial
STN
Caudal Zi
Vo-Vim thalamus
Vo-Vim thalamus

Note: DBS coordinates are measured as the tip of the electrode relative to
the mid-commissural point.

reports of effectiveness for chronic pain (Tsubokawa,
Yamamoto, Katayama, Hirayama, & Sibuya, 1984). In
our patient, macrostimulation of Vc induced intolerable
pain even at low voltage and low frequency (Table 2).
We intraoperatively removed this lead and implanted a
DBS electrode in the ventralis oralis (Vo) thalamic area
with the intention that this lead may better address
dystonia (Morishita, Foote, Haq, et al., 2010). There
was no acute side effect or benefit from the implantation
of this lead. Approximately four weeks after the first
surgery, the patient underwent implantation of a dual
Table 2.

channel implantable pulse generator (Medtronic, Activa
PC, Minneapolis, MN, USA).
The patient reported no pain relief from any programming setting during the initial clinic session. The initial
session included a complete monopolar review of all DBS
contacts. The threshold levels of stimulation-induced dysesthesia were unchanged when compared to the levels
observed in the operative setting. There were seven programming sessions during her first post-operative year. At
the 1-year follow-up, she stated that the pain was minimally improved as compared to preoperative levels.
Objectively there was no change in either the pain scale
scores, or dystonia. Interestingly, the patient reported
aggravation of the pain when she turned off her stimulator
with her remote device.
Discussion
Most neurosurgical techniques including MCS, spinal cord
stimulation, and thalamic stimulation for chronic pain have
aimed to modulate signal within the sensory pathways
(Tsubokawa, Katayama, Yamamoto, Hirayama, &
Koyama, 1993). MCS has in particular been reported to
be a potentially favorable option especially when motor
function is preserved (Katayama, Fukaya, & Yamamoto,
1998). The motor function in our case was not preserved.
We felt that MCS would not be the best choice given the
available literature, and we opted for DBS. Interestingly,
Vc thalamic stimulation failed to address the burning pain
sensation and also seemed to worsen pain. We therefore
chose VC/VS and Vo as the final targets. Limbic circuit

Intraoperative macrostimulation results and DBS settings at last visit.
Response to macrostimulation
VC/VS

Active
contacts
0−, 2+
1−, 3+
2−, 0+
3−, 1+

90 µs/135 Hz

Vc
450 µs/120 Hz

90 µs/135 Hz

No response

At 8 V increased burning pain and HR increased Dysesthesia in the left arm and
from 80 to 130
leg at 1 V
At 5 V smile, at 8–10 V more pain At 5 V smile; increased burning pain at 7 V
Dysesthesia in the left arm and
and anxiety
leg at 2 V
No response
At 10 V uncomfortable
Dysesthesia in the left arm and
leg at 2–3 V
At 5 V smile
At 5 V and 7 V smile; 10 V increase pain
Dysesthesia in the left arm and
leg at 2–3 V
DBS setting at last visit
VC/VS

Active contacts
Amplitude (V)
Pulse width (µs)
Frequencey (Hz)

2−3−, case+
2.5 (1.9–3.5)
180
60

Vo
9−, 10+ (equivalent to 1−, 2+)
2.5 (1.9–3.5)
150
60

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Neurocase
neuromodulation, using VC/VS DBS, is currently under
investigation by another group, and the results remain
unpublished but may be useful to later interpret our case
(clinicalTrial.gov Identifier: NCT01072656) (Machado,
Baker, Plow, & Malone, 2013).
A smile is considered to be both a motor and an
emotional response. Additionally, both motor and emotional responses can be observed to increase with increasing voltages. Several authors have reported that unilateral
smile can be intraoperatively induced by the VC/VS stimulation in OCD (Haq et al., 2011; Nuttin et al., 2003),
and Haq et al. reported the intraoperative smile response
was a predictive factor for a favorable outcome of OCD
DBS (2011). In OCD cases, the smile response is typically
accompanied by a positive mood.
In a recent paper, Lauterbach, Cummings, and
Kuppuswamy described three smile pathways: volitional
(motor), emotional, and composite (2013). The volitional
pathway consists of corticopontine projections from premotor, supplementary motor, posterior cingulate, primary
motor, and primary sensory cortices to the pons, as well as
cortico-striato-pallido-thalamo-cortical and cortico-subthalamo-pallido-thalamo-cortical loops. The emotional pathway consists of limbic circuits involving the anterior
cingulate cortex (ACC), orbitofrontal cortex, periaquedactal grey, amygdala, and hypothalamus. The volitional pathway is thought to inhibit the emotional pathway at
multiple levels.
We speculate that the impairment of ACC function
might be attributable to the phenomena described in our
case. ACC is considered part of the emotional smile
pathway (Lauterbach et al., 2013; Morecraft, Stilwell
Morecraft, & Rossing, 2004), and several authors have
reported the association of ACC function with smile and
laughter and it is known that ACC lesions can be associated with gelastic seizure (Alkawadri, Mickey, Madden,
& Van Ness, 2011; Alkawadri, So, Van Ness, &
Alexopoulos, 2013; Arroyo et al., 1993; McConachie &
King, 1997). Intraoperative stimulation of the ACC has
been reported to induce laughter (Iwasa et al., 2002;
Sperli, Spinelli, Pollo, & Seeck, 2006). In addition, the
ACC has direct projections to the amygdala, and the
overall network plays an important role in emotion
(Buchanan, Thompson, Maxwell, & Powell, 1994;
Müller-Preuss & Jürgens, 1976). Electrical stimulation
to the amygdala has been previously reported to induce
various responses such as fear, panic, and smile (King,
1961). Interestingly, increasing the voltage in our patient
aggravated rather than alleviated the burning pain. This
observation might be due to overactivation of the amygdala pain circuitry (Price, 2000); however, this issue will
require further investigations. The impairment in ACC
might also be secondary to ex vacuo changes following
stroke; however, this would be difficult to prove in a
single case.

677

In summary, we report a single unique case of smile
without euphoria that was induced by DBS. The altered
limbic function was considered to possibly contribute to
the smile phenomenon. Further studies will be needed to
refine our findings.
Disclosure statement
No potential conflict of interest was reported by the authors.

Funding
This study was supported by R21MH064161 and in part by the
University of Florida Grant M01 RR000082 National Center for
Research Resources/National Institutes of Health. This work was
also partly supported by Nakatomi foundation of Japan and Japan
Society for Promotion of Science. This study was supported by
the UF Foundation and the UF INFORM database.

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