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The Journal of Neuroscience, 2001, 21:RC157:1-4
RAPID COMMUNICATION
Repetitive Transcranial Magnetic Stimulation of the Human
Prefrontal Cortex Induces Dopamine Release in the Caudate
Nucleus
Antonio P.
Strafella,
Tomá
Paus,
Jennifer
Barrett, and
Alain
Dagher
Montreal Neurological Institute, McGill University, Montréal,
Québec, Canada H3A 2B4
 |
ABSTRACT |
Dopamine is implicated in movement, learning, and motivation, and
in illnesses such as Parkinson's disease, schizophrenia, and drug
addiction. Little is known about the control of dopamine release in
humans, but research in experimental animals suggests that the
prefrontal cortex plays an important role in regulating the release of
dopamine in subcortical structures. Here we used [11C]raclopride and positron emission tomography
to measure changes in extracellular dopamine concentration in
vivo after repetitive transcranial magnetic stimulation (rTMS)
of the dorsolateral prefrontal cortex in healthy human subjects.
Repetitive TMS of the left dorsolateral prefrontal cortex caused a
reduction in [11C]raclopride binding in the left
dorsal caudate nucleus compared with rTMS of the left occipital cortex.
There were no changes in binding in the putamen, nucleus accumbens, or
right caudate. This shows that rTMS of the prefrontal cortex induces
the release of endogenous dopamine in the ipsilateral caudate nucleus.
This finding has implications for the therapeutic and research use of
rTMS in neurological and psychiatric disorders.
Key words:
positron emission tomography; transcranial magnetic
stimulation; basal ganglia; prefrontal cortex; raclopride; dopamine
| |
INTRODUCTION |
Animal
experiments have shown that descending pathways from the frontal cortex
modulate the release of dopamine in subcortical areas such as the
striatum (Murase et al., 1993 ; Taber and Fibiger, 1993, 1995; Karreman
and Moghaddam, 1996). There is evidence that, in the rat, this occurs
both directly, via glutamatergic corticostriatal projections (Taber and
Fibiger, 1995), and indirectly by an effect on mesostriatal dopamine
neurons in the midbrain (Murase et al., 1993; Karreman and Moghaddam,
1996). This modulation may be relevant to the pathophysiology of
disorders associated with subcortical dopamine dysfunction such as
Parkinson's disease (Kish et al., 1988), schizophrenia (Grace, 1991),
and depression (Willner, 1983). Little is known, however, about the
anatomical pathways involved in the control of dopamine release in
humans. Previous studies (Fox et al., 1997; Paus et al., 1997, 1998;
Siebner et al., 1998) have shown that functional brain imaging can be
used to measure changes in cerebral blood flow and glucose metabolism
induced by transcranial magnetic stimulation. The aim of the present
study was to use positron emission tomography (PET) to determine
whether repetitive transcranial magnetic stimulation (rTMS) of the left mid-dorsolateral prefrontal cortex (MDL-PFC) induces dopamine release
in the striatum of the human brain.
We used the dopamine receptor ligand
[11C]raclopride to detect changes in
levels of extracellular dopamine after rTMS. In vivo binding
of benzamide tracers such as
[11C]raclopride has been shown to be
inversely proportional to levels of extracellular dopamine (Endres et
al., 1997; Laruelle et al., 1997). In humans, this method has been used
to measure dopamine release in response to drugs (Dewey et al., 1993;
Smith et al., 1997; Volkow et al., 1997; Breier et al., 1998) and
behavioral tasks (Koepp et al., 1998). We now report results from eight
healthy volunteers who underwent two
[11C]raclopride PET scans, one
immediately after rTMS of the left MDL-PFC and one after rTMS of the
left occipital cortex for control purposes. Statistical parametric maps
representing the change in
[11C]raclopride binding potential (BP)
were generated to infer changes in the levels of extracellular dopamine
(Aston et al., 2000).
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MATERIALS AND METHODS |
Experimental design. Five female and three male
healthy volunteers (ages, 19-42 years) participated in the study after
having given written informed consent. All subjects but one were
right-handed, and none had a history of neurological or psychiatric
illness. Each underwent two
[11C]raclopride PET scans (total
injected dose, 20 mCi), one after rTMS of the left MDL-PFC and one
after rTMS of the left occipital cortex. The scan order was randomized
across subjects, and the scans were always performed at the same time
in the afternoon on consecutive days. Autonomic parameters and
subjective ratings were collected throughout both sessions of rTMS and
PET. During the study, the subjects kept their eyes closed; earplugs
were used to attenuate the coil-generated clicks. The experiments were approved by the Research Ethics Committee of the Montreal Neurological Institute and Hospital.
Transcranial magnetic stimulation. Repetitive TMS was
performed with the Cadwell high-speed magnetic stimulator (Cadwell
Laboratories, Kennewick, WA) using a circular coil (external diameter,
9 cm). The coil was held outside the scanner in a fixed position by a mechanical arm over the left MDL-PFC or the left occipital cortex. It
was positioned so that the anterior tip of the coil was closest to the
cortical site, with the rest of the coil tilted away from the skull.
The induced current under the coil flowed in a lateromedial direction.
Three rTMS blocks were delivered, each block separated by a 10 min
interval. In each block, 15 10-pulse trains of 1 sec duration were
delivered at a stimulation frequency of 10 Hz and with a between-train
interval of 10 sec. Thus, a total of 450 stimuli were delivered over a
period of 30 min preceding the start of PET acquisition. The stimulus
intensities, which were expressed as a percentage of the maximum
stimulator output, were set at the resting motor threshold (MT). MT was
defined as the lowest stimulus intensity able to elicit, in the right
first dorsal interosseous (FDI), five motor-evoked potentials (MEPs) of
at least 50 µV amplitude in a series of 10 stimuli delivered
over the left primary motor cortex at intervals >5 sec. MEPs were
recorded from the right FDI muscle with AgCl surface electrodes
that were fixed on the skin with a belly-tendon montage. The EMG signal
was filtered (10 Hz-1 kHz bandpass) and displayed on a computer
screen. Repetitive TMS at MT over either of the experimental
stimulation sites, MDL-PFC and occipital cortex, did not induce EMG
activation in the right FDI.
Subjective ratings and autonomic measures. The following
autonomic parameters were collected for 2.5 min during a baseline period at the start of the study and during the rest periods after each
block of rTMS: electrodermal level, respiration rate, and temperature. After the baseline period and after each rest period, subjects completed a behavioral questionnaire in which they rated the
level of their comfort, fatigue, anxiety, mood, irritation, and pain.
Ratings were made on a seven-point Likert scale ranging from  3 to 3, with 3 indicating the highest negative level and 3 indicating the
highest positive level for each dimension. Baseline ratings focused on
how subjects were currently feeling, whereas ratings after blocks of
rTMS focused on how subjects felt during the preceding rTMS stimulation.
Location of the target site. To target the desired sites in
all of our subjects, we used a procedure that takes advantage of the
standardized stereotaxic space of Talairach and Tournoux (1988) and
frameless stereotaxy (Peters et al., 1996). A high-resolution magnetic
resonance image (MRI) of the subject's brain was acquired and
transformed into standardized stereotaxic space (Collins et al., 1994).
The chosen Talairach coordinates of the left MDL-PFC (X = 40, Y = 32, Z = 30) (Petrides et
al., 1993) and left occipital cortex (X = 56,
Y = 58, Z = 3) were converted into
each subject's native MRI space using the reversed native-to-Talairach
transformation (Paus et al., 1997). The positioning of the TMS coil
over these locations, marked on the native MRI, was performed with the
aid of a frameless stereotaxic system (Paus, 1999).
Positron emission tomography. PET scans were obtained with a
CTI/Siemens HR plus tomograph operated in 3-D mode, yielding images of
resolution 4.2 mm full width at half maximum. Within 5 min of the
completion of the rTMS session, 10 mCi of
[11C]raclopride was injected into the
left antecubital vein over 60 sec, and emission data were acquired over
a period of 60 min in 26 frames of progressively increasing duration.
After the emission scan, a transmission scan was performed with a
rotating radioactive source for attenuation correction.
PET frames were summed, registered to the corresponding MRI (Woods et
al., 1993), and transformed into standardized stereotaxic space
(Talairach and Tournoux, 1988) by means of an automated feature-matching algorithm (Collins et al., 1994). Voxel-wise [11C]raclopride BP was calculated using
a simplified reference tissue method (Lammertsma and Hume, 1996; Gunn
et al., 1997) to generate statistical parametric images of change in BP
(Aston et al., 2000). Only peaks falling within the striatum were
considered for further analysis, because this is the only brain
structure in which receptor-specific [11C]raclopride binding is detected. A
reduction in [11C]raclopride BP is
indicative of an increase in extracellular dopamine concentration
(Endres et al., 1997; Laruelle et al., 1997). In each subject, BP
values from the left and right caudate nuclei were extracted with two
regions of interest drawn on three adjacent axial sections
(z, 4-8 mm) of the subject's MRI in stereotaxic space and
confined to the head of the caudate nucleus. These BP values were
analyzed using repeated measures ANOVA.
| |
RESULTS |
Repetitive TMS of the left MDL-PFC decreased
[11C]raclopride BP in the left caudate
nucleus compared with rTMS of the left occipital cortex (Fig.
1, Table
1). This is most likely because of an
increase in extracellular dopamine concentration after prefrontal
stimulation. Table 1 shows BP values from the left and right caudate
nuclei that were derived from a region-of-interest drawn on the MRI of each subject at the level of the statistical peak revealed by the
parametric map. Repeated measures ANOVA revealed a significant effect
of stimulation site for the left caudate nucleus
(F(1,7) = 91.3; p < 0.0001), but not for the right caudate nucleus
(F(1,7) = 0.94; NS). The mean
magnitude of change in [11C]raclopride
BP in the left caudate nucleus was 7.3%. There was no significant
relationship between the intensity of TMS and the change in
[11C]raclopride BP. Repetitive TMS of
the left MDL-PFC did not lead to a statistically significant change in
[11C]raclopride BP in the putamen or the
nucleus accumbens. The autonomic measures and replies to the
questionnaires were analyzed using repeated measures ANOVA. Because
there were no significant differences between the three rTMS periods,
data were pooled. ANOVA revealed no significant main effect of site of
stimulation (MDL-PFC, occipital) or condition (before and after rTMS)
nor any significant site-by-condition interaction (Tables
2,
3).
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Figure 1.
A, Location (red
markers) of the two stimulation sites, the left
mid-dorsolateral prefrontal cortex and the left occipital
cortex, on the MRI of one subject in stereotaxic space.
B, Transverse (Z = 6; left
panel) and sagittal (X = 8;
right panel) sections of the statistical
parametric map of the change in [11C]raclopride BP
overlaid on the average MRI of all subjects in stereotaxic space. The
peak in the left caudate nucleus shows the location at which
[11C]raclopride BP changed significantly after
rTMS of the left mid-dorsolateral prefrontal cortex.
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View this table:
[in this window]
[in a new window]
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Table 1.
[11C]raclopride binding potential in the
caudate nucleus after stimulation of the prefrontal and occipital
cortex
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View this table:
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Table 2.
Mean behavioral ratings of the eight subjects before and
after rTMS of the prefrontal and occipital cortex
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[in this window]
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Table 3.
Mean autonomic activity of the eight subjects before and
after rTMS of the prefrontal and occipital cortex
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DISCUSSION |
We have shown that rTMS of the left MDL-PFC can evoke release of
striatal dopamine in humans, as detected by
[11C]raclopride PET. The fact that the
BP change was seen only in the ipsilateral head of the caudate nucleus
suggests that corticostriatal fibers originating in the MDL-PFC were
involved in promoting local dopamine release at their striatal target
site. Anatomical studies in rhesus monkeys have shown that the MDL-PFC
projects to the dorsal caudate nucleus (Selemon and Goldman-Rakic,
1985; Yeterian and Pandya, 1991). Moreover, corticostriatal fibers
originating in the PFC are thought to project only or predominantly to
the ipsilateral striatum (Kemp and Powell, 1970). Thus, the area of statistically significant change in
[11C]raclopride binding in our study
corresponds to the major projection site of corticostriatal fibers
originating in the stimulated area in MDL-PFC.
These excitatory corticostriatal projections could promote dopamine
release by a local effect of glutamate on adjacent nigrostriatal nerve
terminals (Cheramy et al., 1986). Such an effect may be mediated by
ionotropic (Leviel et al., 1990) or metabotropic (Taber and Fibiger,
1995) glutamate receptors in the striatum, perhaps acting on dopamine
nerve terminals via nitric oxide (Hanbauer et al., 1992). The existence
of this mechanism is supported by the fact that cortical neurons
originating in the PFC and dopamine neurons from the ventral tegmental
area synapse in close proximity to one another on the spines of
striatal medium spiny neurons (Sesack and Pickel, 1992).
However, the possibility of indirect modulation of striatal dopamine
via corticonigral projections also must be taken in consideration. In
rats, stimulation of the PFC can promote bilateral striatal dopamine
release by activation of dopamine neurons in the ventral tegmental area
(Murase et al., 1993; Taber et al., 1995; Karreman and Moghaddam,
1996). This could occur via direct and indirect connections between the
PFC and midbrain dopamine neurons. On the basis of these animal
experiments, one would expect that dopamine released by this mechanism
would not be confined to one area of the dorsal caudate, but rather
that it would involve the neostriatum and nucleus accumbens, possibly
bilaterally (Karreman and Moghaddam, 1996). In this experiment, we did
not detect such widespread release of striatal dopamine, suggesting
that our results reflect only the action of the direct corticostriatal
projections. Grace (1991) has suggested that dopamine released under
direct corticostriatal influence diffuses into the extrasynaptic space,
whereas the dopamine that is released because of midbrain dopamine
neuron burst firing is rapidly cleared from the synapse by reuptake
into the nerve terminal. It is possible that the
[11C]raclopride PET technique is most
sensitive to extrasynaptic dopamine.
The rTMS-induced release of dopamine in the caudate nucleus could be a
consequence of direct stimulation of the corticostriatal axons
(Rothwell, 1997), indirect trans-synaptic activation of corticostriatal
neurons caused by a reduction in GABA-mediated intracortical inhibition
(Chen et al., 1997; Nakamura et al., 1997; Rothwell, 1997;
Pascual-Leone et al., 1998), or both.
In conclusion, these results show for the first time the ability of PET
to detect in humans changes in levels of extracellular dopamine after
rTMS of MDL-PFC. This technique opens up new avenues for in
vivo studies of corticostriatal interactions in humans and for
clinical studies of neurological and psychiatric disorders associated
with subcortical dopamine dysfunction.
| |
FOOTNOTES |
Received March 28, 2001; revised May 3, 2001; accepted May 9, 2001.
Correspondence should be addressed to Dr. Antonio P. Strafella,
Montreal Neurological Institute, Webster 2B, 3801 University Street,
Montréal, Quebec, Canada H3A 2B4. E-mail:
antonio{at}bic.mni.mcgill.ca.
This article is published in
The Journal of Neuroscience, Rapid Communications Section,
which publishes brief, peer-reviewed papers online, not in print. Rapid
Communications are posted online approximately one month earlier than
they would appear if printed. They are listed in the Table of Contents
of the next open issue of JNeurosci. Cite this article as:
JNeurosci, 2001, 21:RC157 (1-4). The
publication date is the date of posting online at
www.jneurosci.org.
| |
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C. Buhmann, A. Gorsler, T. Baumer, U. Hidding, C. Demiralay, K. Hinkelmann, C. Weiller, H. R. Siebner, and A. Munchau
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H. R. Siebner, S. R. Filipovic, J. B. Rowe, C. Cordivari, W. Gerschlager, J. C. Rothwell, R. S. J. Frackowiak, and K. P. Bhatia
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A. P. Strafella, T. Paus, M. Fraraccio, and A. Dagher
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F. X. Castellanos
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TOP
ABSTRACT
INTRODUCTION
Compound via MeSH
