Clinical Neurophysiology 116 (2005) 2592–2598
www.elsevier.com/locate/clinph

Reduced sensorimotor inhibition in the ipsilesional motor cortex
in a patient with chronic stroke of the paramedian thalamus
A. Olivieroa,*, A. Molina Leónb, I. Hollera,c, J. Florensa Vilad, H.R. Siebnerc,
G. Della Marcae, V. Di Lazzaroe, J. Tejeira Álvarezb
a

FENNSI Group, Hospital Nacional de Parapléjicos, SESCAM, Finca ‘la Peraleda’ s/n, 45071 Toledo, Spain
b
Servicio de Neurofisiologı́a, Hospital Virgen de la Salud, SESCAM, Toledo, Spain
c
Department of Neurology, Christian-Albrechts-Universitat Kiel, Kiel, Germany
d
Servicio de Radiologı́a, Sección de Neurorradiologia, Hospital Virgen de la Salud, SESCAM, Toledo, Spain
e
Institute of Neurology, Università Cattolica, largo A. Gemelli 8, 00168 Rome, Italy
Accepted 30 July 2005

Abstract
Objective: Unilateral or bilateral paramedian infarction in the region of the thalamus and upper midbrain may lead to hypersomnia. To
determine whether unilateral infarction of the paramedian thalamus leads to changes in excitability of ipsilesional primary motor hand area
(M1).
Methods: We describe a patient with chronic stroke of the right dorsomedian and intralaminar thalamic nuclei, who suffered from mild
persistent hypersomnia. We studied the excitability of the right and left M1 with transcranial magnetic stimulation (TMS) in the patient, and
in 10 healthy controls.
Results: In contrast to healthy controls, contralateral electrical stimulation of the median nerve failed to induce short-latency afferent
inhibition (SAI) in the ipsilesional M1. Other measures of corticomotor excitability and somatosensory evoked potentials were normal.
Conclusions: The selective loss of ipsilateral SAI in a patient with paramedian thalamic stroke suggests that during wakefulness, the intact
paramedian thalamus facilitates the excitability of intracortical inhibitory circuits, which process thalamocortical sensory inputs in the
ipsilateral M1. This preliminary finding suggests that measurements of SAI may provide a means of probing the integrity of some neural
pathways, which are involved in the control of wakefulness and arousal.
Significance: In addition to the established role of the paramedian thalamus in arousal and memory, our observation suggests that
thalamocortical projections from the paramedian thalamus contribute to the integration of sensory input at the cortical level during
wakefulness.
q 2005 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
Keywords: Transcranial magnetic stimulation; Thalamus; Motor cortex; Arousal; Sleep

1. Introduction
Unilateral or bilateral paramedian infarction in the region
of the thalamus and upper midbrain may produce
neuropsychological disturbance predominantly affecting
arousal and memory. Paramedian thalamic stroke can
cause hypersomnia, which has been attributed to disruption
* Corresponding author. Tel.: C34 925247700x263; fax: C34
704600810.
E-mail address: antonioo@sescam.jccm.es (A. Oliviero).

of ascending activating impulses and considered to
be produced by deficient arousal during the day (Bassetti
et al., 1996).
Several studies have used transcranial magnetic stimulation (TMS) to show that lesions in the thalamus can cause
changes in excitability in the ipsilateral primary motor
cortex (Classen et al., 1997; Munchau et al., 2002; von
Giesen et al., 1994). Here, we evaluated motor cortex
excitability and the sleep patterns of a patient 6 months after
a right paramedian thalamic stroke. The patient suffered
from mild hypersomnia at the time of neurophysiological

1388-2457/$30.00 q 2005 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.clinph.2005.07.015

A. Oliviero et al. / Clinical Neurophysiology 116 (2005) 2592–2598

evaluation. We gave focal TMS to the ipsilesional
and contralesional primary motor hand area (M1), and
assessed several measures of corticomotor excitability
(Siebner and Rothwell, 2003). Our aim was to examine
whether a lesion of paramedian thalamus has a selective
effect on intracortical processing of afferent sensory stimuli
in the ipsilesional M1.

2. Methods
2.1. Case report
A 43-year-old right-handed female patient was admitted
with right ptosis, paresis and sensory deficit of the left upper
limb and severe somnolence. Sensory deficit was evaluated
clinically by comparing light touch and pinprick tests with
the contralateral side. The patient was a smoker and was on
oral anticonceptive treatment. MRI revealed an acute stroke
in the territory of the right paramedian artery involving the
dorsomedial and centromedian thalamic nuclei, the perilesional oedema also involved the upper portion of the right
red nucleus and the fibres of III cranial nerve (MRI not
shown). In the following days, the patient fully recovered
from right ptosis, left upper limb weakness and sensory loss.
Somnolence gradually improved but the patient remained
hypersomnic with 12–14 h of sleep behaviour per day.
The patient was re-examined 6 months after the stroke.
Initial sensorimotor deficits had fully recovered. Light touch
and pinprick tests, two-point discrimination and position
sense were normal. No abnormal postures or involuntary
movements were present. The only residual symptom was
mild hypersomnia. She complained of prolonged night sleep
and excessive daytime sleepiness with difficulty in
maintaining an alert awake state during times of rest or
when little attention was required. The patient was not
treated with drugs in the 60 days prior to re-examination.
Follow-up included a structural MRI scan of the brain,
polysomnography (PSG) and electrophysiological
examination.
2.2. Sleep and daytime sleepiness measurements
Full-night sleep was assessed in the sleep laboratory.
Daytime sleepiness was measured the day after PSG using
the multiple sleep latency test (MSLT) and the Epworth
sleepiness scale (Johns, 1991). The MSLT was performed
five times during the day, at 2 h intervals starting at 8 am.
2.3. Electrophysiological measurements
Electrophysiological measurements of sensorimotor
function were carried out during wakefulness and compared
to normal values obtained in 10 healthy controls with no
history of sleep disorders (5 females, two left-handed, age
32.4G8.1 years).

2593

We evaluated motor cortex excitability and the integrity
of corticospinal and somatosensory pathways using TMS.
Measurements included: (i) the resting and active motor
threshold (RMT and AMT), which reflect the intrinsic and
extrinsically modulated excitability properties of corticospinal neurons (Hallett, 2000; Ziemann et al., 1996); (ii)
central motor conduction time (CMCT), which reflects the
integrity of the corticospinal tract (Rossini et al., 1994); (iii)
short-latency intracortical inhibition to paired TMS (SICI),
long latency intracortical inhibition to paired TMS (LICI)
and the cortical silent period (CSP); which are all believed
to reflect the excitability of inhibitory GABAergic cortical
circuits (Di Lazzaro et al., 2000a, b; Ziemann et al., 1996);
(iv) intracortical facilitation (ICF) to paired TMS that is
thought to depend on the activity of intracortical glutamatergic excitatory circuits and is also modulated by gabaergic
inputs (Kujirai et al., 1993; Ziemann et al., 1998a); and (v)
short-latency afferent inhibition (SAI) which is facilitated
by cholinergic circuits as demonstrated by the sensitivity to
the muscarinic blockade (Di Lazzaro et al., 2000a, b). We
also recorded somatosensory evoked potentials (SSEPs)
after contralateral median nerve stimulation to demonstrate
the functional integrity of the thalamocortical sensory
pathway (Mauguiere, 1996).
Electrophysiological measurements were always performed at the same time of the day (between 4 and 6 pm).
The study adhered to the guidelines for scientific conduct
specified in the Declaration of Helsinki and was approved
by the local ethics committee. The patient and controls gave
informed consent before participation.
Electrophysiological measurements were conducted
6 months after stroke. The patient was instructed to stay
awake with eyes open. Since cortical excitability is largely
influenced by drowsiness or sleep, the patient was studied
during full wakefulness, which was continuously monitored
with two EEG electrodes placed at Cz and Pz (10–20
system). Drowsiness was defined as either slowing of alpha
activity (stage 1A) or appearance of theta activity (stage 1B)
(Valley and Broughton, 1983). EEG revealed no signs of
drowsiness or sleep during the course of the experiment.
TMS was performed with a high power Medtronic
Magpro X100 (Medtronic, Minneapolis, MN, USA). A
figure-of-eight coil with external loop diameters of 9 cm
was held over the motor cortex at the optimum scalp
position to elicit motor responses in the contralateral first
dorsal interosseous (FDI) muscle. The induced current
flowed in a postero-anterior direction and the pulse form
was monophasic.
RMT was defined as the minimum stimulus intensity that
produced a liminal motor evoked response (about 50 mV in
50% of trials) at rest. AMT was defined as the minimum
stimulus intensity that produced a liminal motor evoked
response (about 200 mV in 50% of trials) during isometric
contraction of the tested muscle at about 20% maximum
(Rossini et al., 1994). CMCT was calculated by subtracting the
peripheral conduction time from cervical roots to muscles

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A. Oliviero et al. / Clinical Neurophysiology 116 (2005) 2592–2598

(obtained by magnetic stimulation at cervical level) from the
latency of responses evoked by cortical stimulation (Rossini
et al., 1994). CSP was elicited whilst subjects held a tonic
voluntary contraction of approximately 50% of MVC. Five
stimuli at 150% AMT were given. The duration of the silent
period was measured from the start of the motor potential to
the reappearance of sustained EMG activity. SICI and ICF
were studied using a conditioning-test paradigm introduced by
Kujirai et al. (1993). Two magnetic stimuli were given through
the same stimulating coil to the motor cortex, and the effect of
the first (conditioning) stimulus on the second (test) stimulus
was investigated. The conditioning stimulus was set at an
intensity of 90% of AMT. The test stimulus was adjusted to
evoke a MEP in relaxed FDI muscle with an amplitude of
approximately 1 mV peak-to-peak. The timing of the
conditioning shock was altered in relation to the test shock.
Interstimulus intervals (ISIs) of 2 and 3 ms and 10 and 12 ms
were investigated. Ten stimuli were delivered at each ISI. The
amplitude of the conditioned MEPs was expressed as
a percentage of the amplitude of the test MEPs. Inhibition
and facilitation of the conditioned responses at the two
different ISIs studied was averaged to give grand mean values.
LICI was studied in the following way: two magnetic
stimuli were given through the same stimulating coil; both
conditioning and test stimuli were set at an intensity
adjusted to evoke a MEP in relaxed FDI muscle with an
amplitude of approximately 1 mV peak-to-peak (about
110% RMT). An interstimulus interval of 100 ms was
investigated. The amplitude of the conditioned MEPs was
expressed as a percentage of the amplitude of the test MEPs.
SAI was studied using the technique described by Tokimura
et al. (Di Lazzaro et al., 2002; Tokimura et al., 2000). The

intensity of the test cortical magnetic shock was adjusted to
evoke a muscle response in relaxed FDI with an amplitude
of approximately 1 mV peak-to-peak. Conditioning stimuli
were single pulses of electrical stimulation applied through
bipolar electrodes to the median nerve at the wrist. The
intensity of the conditioning stimulus was set at just over
motor threshold to evoke a visible twitch of the thenar
muscles. The conditioning stimulus to the peripheral nerve
preceded the magnetic test stimulus. Interstimulus intervals
(ISIs) were determined relative to the latency of the N20
component of the somatosensory evoked potential evoked
by stimulation of the median nerve. The active electrode for
recording the N20 potential evoked by left median nerve
stimulation was attached 3 cm posterior to C3 (10–20
system) (or C4 for right median nerve stimulation) and the
reference was 3 cm posterior to C4 (or C3 for right median
nerve stimulation). One thousand consecutive potentials
were averaged to identify the mean latency of the N20 peak.
ISIs were adjusted to individual N20 latency and seven ISIs
were tested ranging from N20C2 ms to N20C8 ms.. Ten
stimuli were then delivered at each ISI. The amplitude of the
conditioned MEPs was expressed as a percentage of
the amplitude of the test MEPs. The percentage inhibition
of the conditioned responses at the seven different ISIs was
averaged to obtain a grand mean.
RMT, AMT, SICI, LICI, ICF, SAI, duration of the CSP,
CMCT, N20 latency and N20 amplitude were evaluated
bilaterally, both in the patient and in controls. Interhemispheric differences (dominant hemisphere minus nondominant hemisphere) were calculated for each measure. In
the control group, we calculated meanG2.5 SD to define
the upper and lower limits of the normal range for each

Fig. 1. T1 weighted sagittal MRI (A) shows a chronic lesion in the right thalamus. T2 weighted axial MRI (C–F) shows the cranio-caudal extension of the
chronic lesion in the right thalamus involving dorsomedial and centromedian nuclei (white arrows). T2 weighted axial MRI (B, G and H) shows the upper and
lower scans without pathological signals (H: grey arrow indicates the normal red nucleus).

A. Oliviero et al. / Clinical Neurophysiology 116 (2005) 2592–2598

neurophysiological parameter and the inter-hemispheric
differences (ID).

3. Results
At 6-month follow-up, structural T1 and T2-weighted
MRI showed a chronic lesion in the right thalamus
involving dorsomedial and centromedian nuclei (Figs. 1
and 2). The results of PSG are summarized in Table 1. PSG
did not show any major abnormality of sleep. In particular,

2595

PSG revealed no apnoea or periodic limb movements during
sleep. The MSLT revealed a sleep latency of 8.4 min
(normal value O10 min, pathologic sleepiness ! 5 min,
dubious between 5 and 10 min). We observed no epoch of
REM sleep within the first 10 min during five consecutive
tests. The patient reached a score of 12 on the Epworth
sleepiness scale (normal value !10), indicating mild
hypersomnia.
Table 2 summarizes the electrophysiological results.
RMT, AMT, SICI, ICF, duration of the CSP, CMCT, N20
latency and N20 amplitude were within normal limits. LICI

Fig. 2. Atlas image (modified from Talairach and Tournoux, 1988) showing the location of the dorsomedian nucleus (black arrow) and a T2 weighted axial
MRI, showing the lesion of the dorsomedian and cenrtomedian nuclei (white arrow). DM, dorsomedian nucleus; CM, centromedian nucleus.

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A. Oliviero et al. / Clinical Neurophysiology 116 (2005) 2592–2598

Table 1
Polysomnographic parameters of the patient

4. Discussion

Polysomnographic parameters

In the waking state, we observed a selective attenuation
of the SAI in the ipsilesional M1 6 months after a thalamic
stroke that had destroyed the dorsomedian and intralaminar
nuclei. The reduction of SAI was evenly distributed across
all ISIs, resulting in a loss of SAI at short ISIs and an
abnormal sensorimotor facilitation at longer ISIs. Previous
work has shown that an electrically induced afferent volley
from the median nerve can produce short-latency facilitation (Deletis et al., 1992) and inhibition (Tokimura et al.,
2000) of the corticomotor output to the stimulated limb. In
our patient, a loss of thalamocortical input from the
dorsomedian and intralaminar nuclei onto intracortical
circuits was associated with a shift in the balance between
short-latency sensorimotor inhibition and facilitation
towards a stronger facilitation. TMS measurements showed
that the change in motorcortical excitability was restricted
to the conditioning effect of afferent somatosensory stimuli.
There was no evidence for a damage of the corticospinal
output tract or additional abnormalities in the excitability of
the M1. EEG monitoring excluded the possibility that the
changes in sensorimotor excitability were confounded by an
altered state of vigilance during the electrophysiological
measurements. Sensory testing, SSEP measurements and
structural MRI showed that the somatosensory thalamocortical pathways and the sensory nuclei of the thalamus were
not affected by the paramedian thalamic stroke. Taken
together, our findings suggest that during wakefulness, SAI
is under the control of neuronal networks located in the
paramedian thalamus.
SAI starts only a few milliseconds after the arrival of
the somatosensory input at the cortex, and implies a
relatively direct pathway from sensory input to motor
output (Tokimura et al., 2000). SAI has been shown to
depend upon the activity of cholinergic circuits

Macrostructure
Sleep onset latency
Sleep efficiency on time in bed
Sleep period time
Total sleep time
Number of REM periods
REM latency
Sleep stages percentages
REM
Stage 1
Stage 2
Stage 3
Stage 4
Wake parameters
Total number of awakenings
Awakenings O2 min
Apnea–hypopnea index

11.0 min
97.0%
503 min
493 min
4
1 h 22 min
22.0%
13.0%
39.0%
18.0%
8.0%
2
0
0 events/h

showed a tendency to be more pronounced in the affected
hemisphere (AH) than in the unaffected hemisphere (UH)
while SICI showed a tendency to be reduced in the AH
when compared with the UH.
In healthy controls, the magnitude of SAI showed a
tendency towards a stronger SAI in the dominant
hemisphere (DH) compared with the non-dominant hemisphere (NDH), but both hemispheres showed a clear SAI.
In contrast to healthy controls, the amount of SAI
markedly differed between hemispheres in the patient
(Table 2). While SAI in the contralesional M1 was
normal, the patient showed a complete loss of SAI in
the ipsilesional M1 (Fig. 3). Sensory stimulation had
even a facilitatory effect on the MEP amplitude at longer
ISIs (Fig. 3).

Table 2
Neurophysiological findings in the patient and in 10 control subjects
Test

RMT (%)
AMT (%)
CSP (ms)
SICI (%)
ICF (%)
LICI (%)
SAI (%)
N20 lat/amp
(ms/uV)
CMCT (ms)

Control subjects

Patient

DH

NDH

ID (DHKNDH)

ID lower limit

ID upper limit

UH (DH)

AH (NDH)

ID (UHK
AH)

61.8 (4.4)
46.9 (6.9)
146.3 (42.5)
40.5 (8.9)
131.4 (42.5)
35.2 (22.6)
53.9 (22.1)
19/2.8 (0.6/0.8)

62.2 (3.3)
47 (4.8)
156.3 (28.8)
43.1 (24.5)
123.6 (20.8)
35.7 (20)
64.2 (17.9)
19/2.9 (0.6/0.6)

K0.4 (3)
K0.1 (8.2)
K10 (47)
K2.6 (20)
7.8 (45.2)
K0.4 (27.7)
K10.4 (11.7)
0/K0.1 (0.6/0.8)

K8
K20.6
K128
K53.5
K105.3
K69.8
K39.6
K1.6/K1.9

7.2
20.4
108
48.3
120.8
68.9
18.9
1.6/2.1

60
44
108
24.3
106.1
64.5
54.2
17.8/2.4

58
43
101
52.6
121.8
17.8
125.6
17.9/2.4

2
1
K7
K28.3
K15.7
46.7
K71.4
K0.1/0

5.9 (0.6)

5.8 (0.6)

0.1 (0.2)

K0.4

0.6

5.7

5.6

0.1

DH: dominant hemisphere; NDH: non-dominant hemisphere; ID: interside difference; UH: unaffected hemisphere; AH: affected hemisphere; SICI: mean SICI
at 2 and 3 ms ISIs; ICF: mean ICF at 10 and 12 ms ISIs; LICI: mean LICI at 100 ms ISI; SAI: mean SAI at N20C2–8 ms ISIs; RMT and AMT %: % of
maximum stimulator output; SICI, ICF, LICI and SAI %: % of test response; CMCT: central motor conduction time; ( ): standard deviations; bold: out of
normal limits.

A. Oliviero et al. / Clinical Neurophysiology 116 (2005) 2592–2598
200

Short Latency Afferent Inhibition

% of test response

180
160
140
120
100
80
60
40

DH (controls)
NDH (controls)

20
0
N20 lat +2ms +3ms

+4ms

+5ms

+6ms

+7ms

UH (patient)
AH (patient)
+8ms

Fig. 3. SAI time course at different interstimulus intervals in both the
patient and in controls. The loss of SAI was consistent across all ISIs. At
late ISIs the mean amplitude of the conditioned response was evenly
facilitated. DH, dominant hemisphere; NDH, non-dominant hemisphere;
UH, unaffected hemisphere; AH, affected hemisphere.

2597

studies focused on this asymmetry could confirm this result
and provide information about its functional role
and the relationship with handedness. The slight asymmetry
of CSP between DH and NDH in healthy subjects confirms
preview reports (Garvey et al., 2003; Priori et al., 1999). Our
patient had symmetric CSPs, which showed a tendency to be
slightly shorter respect to the healthy group. Thalamic
lesions had been reported associated with shorter or
prolonged CSP depending on the lesion location (Classen
et al., 1997; Liepert et al., 2005; Munchau et al., 2002).
Further studies can clarify the exact relationship between
CSP and the thalamus.

Acknowledgements

as demonstrated by its sensitivity to the muscarinic
blockade (Di Lazzaro et al., 2000a, b). The dorsomedial
nucleus and intralaminar nuclei (thalamic paramedian
structures) are under control of excitatory projections from
pontomesencephalic cholinergic neurons (peduncolopontine and laterodorsal tegmental cholinergic nuclei) through
muscarinic receptors (Jones, 2003; Steriade, 2004). These
pontomesencephalic cholinergic neurons have no direct
projection to the cortex but they do have a prominent
indirect effect on the functional state (and excitability) of
cortical neurons as they activate thalamocortical neurons
(Steriade, 2001; Steriade, 2004). At the time of this
neurophysiological study (i.e. 6 months after stroke), the
only residual symptom was mild hypersomnia probably
due to the interruption of the pontomesencephalic(paramedian) thalamo-cortical pathway. The pontomesencephalic-(paramedian) thalamo-cortical pathway is
thought to be important for arousal, and cholinergic
projections (during wakefulness) are also thought to
facilitate the responsiveness of cortical neurons to sensory
stimuli (e.g. promoting sensory-motor inhibition, see
Jones, 2003) (Jasper and Tessier, 1971; Jones, 2003).
Our results indicate that during wakefulness, the intact
paramedian thalamus exerts a facilitatory effect on the
excitability of intracortical inhibitory circuits. This
supports the concept that the pontomesencephalic-(paramedian) thalamo-cortical pathway also plays a prominent
role in regulating intracortical sensory (motor) processing.
We propose that the measurement of SAI can be used to
test how this pathway related to arousal modulates the
integration of sensory input at the cortical level. We found
a marked loss of SAI, while only mild hypersomnia was
evident at the time of the neurophysiological study. The
unilateral lesion and the sparing of other arousal systems
could explain this discrepancy.
It is interesting to note that SAI was slightly more
pronounced in the DH in healthy controls: further

This work was partially sponsored by the ‘Instituto de
Ciencia de la Salud’, Junta de Comunidades de Castilla La
Mancha, Ayudas 2003-project n 03058-00.

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