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Assessing the Role of the Basal Ganglia in Human Decision-Making

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Simona Mrakic-Sposta (simona.mrakicsposta@policlinico.mi.it) Abstract Deep Brain Stimulation (DBS), besides an effective therapeutic tool, is a fascinating physiological "window" on human subcortical structures. In fact, local field potential (LFPs) recordings in patients provide an amount of physiological data on basal ganglia, especially in relation to their motor, cognitive and affective functions. In this study we aimed to assess a novel methodological approach for estimating the functional role of the basal ganglia. In particular, we focus here on decision making processes, by recording the scalp Electroencephalogram and Local Field Potentials oscillations from the Sub-Thalamic Nucleus in patients with Parkinson's disease who underwent neurosurgical procedures for Deep Brain Stimulation. Our results show that STN oscillations is modulated by the execution of gambling task. In particular, this modulation was different from that induced by the execution of a motor control task: whereas the motor task induced a desychronization in the low-and high-beta oscillation (10-20 Hz), gambling tasks synchronized beta activity in both sub-bands. We conclude that LFPs oscillations provide a direct window on STN activity during decision making. Since LFPs oscillations were differentially modulated by the gambling and motor task, the STN could be involved in a circuit encoding non-motor information during decision making processes.
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Assessing the Role of the Basal Ganglia in Human Decision-Making
Claudio Lucchiari (claudio.lucchiari@unimi.it)
Department of Social and Political Studies, University of Milan, 20122, Via Conservatorio,
Milano, Italy
Manuela Fumagalli (manuela.fumagalli@policlinico.mi.it)
Department of Neurological Sciences, University of Milan, 20122, Via Sforza, 28, Milano, Italy
Sara Marceglia (sara.marceglia@policlinico.mi.it)
Neuronanotechnology and Neurostimulation Clinical Centre; Neurophysiopathology Division, IRCCS Ospedale
Maggiore Policlinico, 20122, Via Sforza, 35, Milano, Italy
Simona Mrakic-Sposta (simona.mrakicsposta@policlinico.mi.it)
Neuronanotechnology and Neurostimulation Clinical Centre; Neurophysiopathology Division, IRCCS Ospedale
Maggiore Policlinico, 20122, Via Sforza, 35, Milano, Italy
Domenico Servello (servello@libero.it)
Neurosurigical Division, Centre for Extrapyramidal Disease and Tourette Syndrome, IRCCS Galeazzi, 20161, Via
Galeazzi, 4, Milano, Italy
Sergio Barbieri (sergio.barbieri@policlinico.mi.it)
Neurophysiopathology Division, IRCCS Ospedale Maggiore Policlinico, 20122, Via Sforza, 35, Milano, Italy
Alberto Priori (alberto.priori@unimi.it)
Department of Neurological Sciences, University of Milan, 20122, Via Sforza, 28, Milano, Italy
Gabriella Pravettoni (gabriella.pravettoni@unimi.it)
Department of Social and Political Studies, University of Milan, 20122, Via Conservatorio,
Milano, Italy
Abstract
Deep Brain Stimulation (DBS), besides an effective
therapeutic tool, is a fascinating physiological “window” on
human subcortical structures. In fact, local field potential
(LFPs) recordings in patients provide an amount of
physiological data on basal ganglia, especially in relation to
their motor, cognitive and affective functions.
In this study we aimed to assess a novel methodological
approach for estimating the functional role of the basal
ganglia. In particular, we focus here on decision making
processes, by recording the scalp Electroencephalogram and
Local Field Potentials oscillations from the Sub-Thalamic
Nucleus in patients with Parkinson’s disease who underwent
neurosurgical procedures for Deep Brain Stimulation. Our
results show that STN oscillations is modulated by the
execution of gambling task. In particular, this modulation was
different from that induced by the execution of a motor
control task: whereas the motor task induced a
desychronization in the low- and high-beta oscillation (10-20
Hz), gambling tasks synchronized beta activity in both sub-
bands.
We conclude that LFPs oscillations provide a direct window
on STN activity during decision making. Since LFPs
oscillations were differentially modulated by the gambling
and motor task, the STN could be involved in a circuit
encoding non-motor information during decision making
processes.
Keywords: Decision-making; Gambling; Parkinson Disease;
Deep Brain Stimulation; Local Field Potentials.
Introduction
Decision making involves different brain structures. Though
functional neuroimaging studies provided data on the
contribution of several cortical areas, the role of subcortical
nuclei in decision-making is still unclear. Yet, patients with
subcortical lesions can have impaired decisional processes
(Opris & Bruce, 2005). Lesion studies are however difficult
to be interpreted, especially for inferring the function of
relatively small nuclei as, for instance, the basal ganglia. For
the same reason studies of functional neuroimaging of
subcortical structures during decision-making have
important methodological limitations.
Ideally, the best experimental approach to study the role
of subcortical structures during decision-making would be to
record neuronal activity directly from subcortical nuclei.
The fascinating opportunity to study the
electrophysiological correlates of decision making processes
in the human basal ganglia is offered by patients undergoing
electrode implantation for deep brain stimulation (DBS).
DBS treatment is presently indicated for complicated
Parkinson’s disease, torsion dystonia, tremor, Tourette
syndrome, obsessive compulsive disorder (Limousin &
Martinez-Torres, 2008; Johnson et al., 2008). After
neurosurgical implantation of the electrodes in the basal
ganglia, they can be used for few days for recording the
local electrical field potential oscillations (LFPs) in the
target structure where the electrode is implanted while the
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patients is awake and free to move without constraints.
DBS, besides an effective therapeutic tool, is therefore a
fascinating physiological “window” on human subcortical
structures that through Local Field Potentials (LFPs)
recordings in patients provided an amount of physiological
data on basal ganglia, especially in relation to their motor,
cognitive and affective functions. Depending on the
condition to be treated, DBS electrode can be implanted in
the subthalamic nucleus (STN), in the internal segment of
the globus pallidus or in the thalamic nuclei.
In this study we aimed to assess a novel methodological
approach for estimating the functional role of the basal
ganglia in decision making processes during the execution
of the gambling task by recording the scalp
Electroencephalogram (EEG) and LFPs oscillations from
the STN in patients who underwent neurosurgical
procedures for DBS.
Methods
Patients
Five patients (2 females, 3 males) with Parkinson’s disease
were studied after their informed consent and local ethical
committee approval.
Surgical Procedure
All patients were bilaterally implanted in the STN with
macroelectrodes for DBS (model 3389 Medtronic,
Minneapolis, USA). The STN was targeted by direct
visualization through a CT-MRI fusion-based technique
before surgery, as detailed elsewhere (Rampini et al., 2003).
The site of electrode implantation was then adjusted during
surgery with recordings from the explorative
microelectrodes (Priori et al., 2003), and by clinically
assessing changes induced by stimulation through probe
microelectrodes and through the implanted macroelectrodes.
Postoperative imaging CT scans were fused with
preoperative T2-weighted MRI to assess the final position of
the DBS electrode and to verify the consistent placement of
contact 1 within the STN (Figure 1).
Figure 2: Axial projection of the (A) postoperative
stereotactic CT (slice 25 of 85, 43.0 mm) matched with
(B) preoperative stereotactic MR (slice 19 of 22, 36.9
mm) of one representative patient. The two red circles
represent the electrodes in the two images. The same
software used for preoperative planning procedures was
used to match the two images.
Experimental protocol
The experimental protocol included two sessions. First, one
or two days before surgery, after a brief mood and anxiety
evaluation a scalp EEG was recorded while the patient
executed the gambling and the motor tasks. Second,
two/three days after surgery, the psychological assessment
was repeated and LFPs and EEG were simultaneously
recorded during the execution of the gambling and the motor
tasks. Both experimental sessions were conducted about one
hour after patients received their usual dopaminergic
medication, to reach the most physiological condition.
Psychological assessment Mood and anxiety (state and
trait) were assessed through HAD and STAI (Y-1, Y-2).
Mood, anxiety and distress were also subjectively evaluated
through three visual analogue scales (VASs). After surgery,
patients were re-assessed with STAI Y-1 and VASs.
Gambling tasks Two gambling tasks were administered: a
80/20 and a 60/40. Six different stimulus pairs (AB, AC,
AD, BC, BD, CD) were presented in random order, and
participants had to choose one of the two stimuli. Feedback
followed the choice to indicate the consequent result and the
total amount of money accumulated by the subject. In the
80/20 (60/40) task, for instance, the AB pair indicates that a
choice of stimulus A led to positive outcome (+60 euros) in
80% (60%) of trials and to a negative outcome (-30 euros) in
20% (40%) of trials, whereas a choice of stimulus B led to
negative outcome (-30 euros) in 80% (60%) of trials and to
positive outcome (+60 euros) in 20% (40%) of trials. This
represents a low conflictual decision context. The BC pair
indicates that the selection of stimulus B led to negative
outcome (-30 euros) in 80% (60%) of trials and to positive
outcome (+60 euros) in 20% (40%) of trials, whereas a
choice of stimulus C led to high gain (+100 euros) in 20%
(40%) of trials and to a high loss (-70 euros) in 80% (60%)
of trials. This represents a high conflictual decision context.
Selections and reaction times (RTs) were collected and
analyzed.
Motor task To exclude the effect of the pure motor
component of the gambling task, a motor task was
administered to the subject. Subjects were presented a white
circle on a black screen. The circle can appear on the right
or on the left of the screen. Subjects were instructed to press
as fast as possible the button omolateral to the stimulus,
using the right hand for the right button, and the left hand
for the left button. Accuracy and RTs were collected and
analyzed.
Electrophysiological recordings and analysis During
the first session (pre-surgery) scalp EEG was recorded
through Ag/AgCl electrodes and following the standard
international 10/20 system. EEG were first recorded at rest
(3 minutes with eyes closed and 3 minutes with eyes open)
to have a basal recording and then synchronized with the
execution of the gambling or motor task: when the patient
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pressed the response button, a trigger signal was sent to the
recording system.
During the second experimental session (post-surgery),
subthalamic LFPs and scalp EEG were recorded at rest
(basal recording, 3 minutes eyes closed, 3 minutes eyes
open) and during the execution of the motor/gambling tasks.
LFPs were captured from the implanted electrodes, before
the subcutaneous high-frequency stimulator was connected,
while macroelectrodes were still externalized and accessible.
The 3389 Medtronic electrode has four cylindrical contacts
(1.27 mm in diameter, 1.5 mm in length, spaced 2 mm
centre to centre) denominated 0-1-2-3, beginning from the
more caudal electrode. According to intraoperative and
postoperative tests, contact 1 was consistent with placement
within the STN. LFPs were captured from the 3389
electrode using the central closely spaced pair of contacts
(contacts 1–2) using a bipolar recording.
Scalp EEG was recorded only from frontal electrodes,
namely Fp1, Fp2, F3, F4, F7, F8 of the 10/20 international
system because of the presence of wounds from the surgery.
All the signals were captured through the Galileo BE
Light EEG amplification system (EBNeuro SpA, Italy),
preamplified, differentially amplified, analogically band-
passed (2-500 Hz), and digitally sampled at 1024 Hz, with
12 bit quantization with 5V range. All further analysis was
conducted off-line with the Matlab software (version 6.5,
The Mathworks, Natik, MA, USA).
Quantitative EEG analysis was performed through power
spectral analysis and coherence analysis.
STN oscillations at rest were quantified by standard LFPS
power spectral analysis.
Spectra were calculated using Welch’s averaged, modified
periodogram method: signals were divided into segments of
1024 samples, with no overlap; in each segment, the mean
was subtracted; each segment was windowed by a Hanning
window; the squared magnitude of the discrete Fourier
transform of each segment was calculated; and the squared
magnitudes of each segment were averaged, to obtain the
estimated power spectral density (PSD). The resolution of
the calculated spectrum was 1 Hz.
Task-related analysis was performed by averaging the
power spectrum over all the trials available (Figure 2). For
each gambling trial, the starting point was the stimulus
presentation, calculated as the difference between the trigger
occurrence time and the reaction time registered by the
software and the end point was placed 750 ms after the
trigger, at the end of the feedback presentation. For the
motor task, the starting point was the stimulus presentation,
as in the gambling task, but the end point was 500 ms after
the trigger.
3
5s
3
3
0 5 10 15 20 25 30 35
10
-3
10
-2
0 5 10 15 20 25 30 35
10
-3
10
-2
AVERAGE
f(Hz) f(Hz)
LogPSD
LogPSD
0 5 10 15 20 25 30 35
10
-3
10
-2
10
-1
f(Hz)
LogPSD
TRIAL2
TRIAL1
Figure 2: Triggered data analysis.
Results
All the patients had normal mood and anxiety before and
after surgery. The performance of motor and gambling tasks
before and after surgery did not change. Gambling tasks
revealed that patients choose the riskiest and the most
conflictual choices.
5 10 15 20 25 30 35
0.05
0.1
0.15
0.2
0.25
0.3
f(Hz)
PSD (mV
2
/Hz)
TaskMotorio
Basale
DecisionTask80/20
DecisionTask60/40
Figure 3: Electrophysiological results. STN-LFPS Power
spectra at baseline (black line), during motor (blue line),
and gambling (red and grey lines) tasks. X-axis:
frequency; y-axis power spectral density (PSD).
STN oscillations were modulated by the execution of
gambling task and this modulation was different from that
induced by the execution of the motor task: whereas the
motor task induced a desycnhronization in the low- and
high-beta oscillation (10-20 Hz), the gambling tasks
synchronized beta activity in both sub-bands (Figure 3).
Conclusion
We reported here preliminary results about the role of basal
ganglia in decision making processes. The possibility to
record LFPs oscillations during gambling tasks provides a
novel direct window on STN activity during decision
making and, more generally, the opportunity to assess its
role in complex cognitive processes. This methodological
approach might contribute to the analysis of executive
functions in human subjects.
The fact that the STN neural activity may be directly
recorded and coupled with scalp EEG with high spatial and
temporal resolution, may contribute to overcome some
important limitations of neuroimaging techniques.
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In this preliminary study, STN-LFPs oscillations were
differentially modulated by the gambling and motor task.
STN could hence be involved in a circuit encoding non-
motor information during decision making processes. LFPs
oscillations reflect the activity of large populations of
neurons and they provide a complex and articulate view of
information processing in the brain. Our preliminary data
suggest that neural processes underlying gambling involve
the STN and, possibly, the whole basal ganglia circuit.
References
Opris, I., Bruce, C. J. (2005). Neural circuitry of judgment
and decision mechanisms. Brain Research Review
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509-26.
Limousin, P., Martinez-Torres, I. (2008). Deep brain
stimulation for Parkinson's disease. Neurotherapeutics,
5(2), 309-19
Johnson, M. D., Miocinovic, S., McIntyre, C. C., Vitek, J. L.
(2008). Mechanisms and targets of deep brain stimulation
in movement disorders. Neurotherapeutics, 5(2), 294-308
Rampini, P. M., Locatelli, M., Alimehmeti R., Tamma, F.,
Caputo, E., Priori, A., Pesenti, A., Rohr, M., Egidi, M.
(2003). Multiple sequential image-fusion and direct MRI
localisation of the subthalamic nucleus for deep brain
stimulation.
Journal of Neurosurgical Sciences, 47(1), 33-
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Priori, A., Egidi, M., Pesenti, A., Rohr, M., Rampini, P.,
Locatelli, M., Tamma, F., Caputo, E., Chiesa, V., Barbieri,
S. (2003). Do intraoperative microrecordings improve
subthalamic nucleus targeting in stereotactic neurosurgery
for Parkinson's disease ? Journal of Neurosurgical
Sciences, 47(1), 56-60.
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The clinical importance of intraoperative microrecordings for subthalamic nucleus (STN) localization in neurosurgical practice remains a matter of debate in the various groups. To investigate their usefulness in localizing the STN, we retrospectively evaluated how intraoperative microelectrode recordings changed the targeting of the STN estimated only on intraoperative stimulation and neuroanatomic targeting procedures. For neuroradiologic targeting of the nucleus we used a TC-MRI fusion algorithm and direct visualization of the STN. Besides standard microrecordings we also analyzed the power spectral density (PSD) pattern of physiological signals along the track and its neuroanatomic and clinical correlations. In our series of 12 patients with Parkinson's disease undergoing surgery for implantation of deep-brain stimulation (DBS) electrodes in the STN we found that in 25% (1/4) of patients, microrecordings determined the choice of the optimal track. In all the tracks analyzed the PSD peak coincided with the point selected for the final electrode implantation on the basis of the standard procedure for intraoperative monitoring based on both microstimulation and recordings. Intraoperative microrecordings are of determinant importance for accurate STN localization and are essential for optimal results in neurosurgical practice. PSD analysis is a simple and quick quantitative signal descriptor that will probably provide even more precise, simple and rapid tool for intraoperative neurophysiological localization of the STN.
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Neural circuitry of judgment and decision mechanisms
  • I Opris
  • C J Bruce
Opris, I., Bruce, C. J. (2005). Neural circuitry of judgment and decision mechanisms. Brain Research Review, 48(3), 509-26.