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NEUROCASE
2012, 18 (3), 217–223
Brain stimulation improves associative memory in an
individual with amnestic mild cognitive impairment
Maria Cotelli1, Marco Calabria2, Rosa Manenti1, Sandra Rosini1, Claudio Maioli3,
Orazio Zanetti1, and Carlo Miniussi1,3
1IRCCS Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy
2Department of Technology, Universitat Pompeu Fabra, Barcelona, Spain
3Department of Biomedical Sciences and Biotechnologies, National Neuroscience Institute,
University of Brescia, Brescia, Italy
In patients with cognitive deficits, brain stimulation has been shown to restore cognition (Miniussi et al., 2008,
Brain Stimulation, 1, 326). The aim of this study was to assess whether repetitive Transcranial Magnetic Stimulation
(rTMS) could improve memory performance in an individual with amnestic Mild Cognitive Impairment (aMCI).
Stimulation of the left parietal cortex increased accuracy in an association memory task, and this improvement
was still significant 24 weeks after stimulation began. These findings indicate that rTMS to the left parietal cortex
improved memory performance in aMCI.
Keywords: Neurorehabilitation; Parietal cortex; Face–name association; MCI; Brain stimulation.
Recently, in patients with neurological disease, sev-
eral studies have reported enhanced performance
on specific cognitive tasks following non-invasive
brain stimulation (e.g., repetitive Transcranial
Magnetic Stimulation, rTMS) to specific cortical
areas (see Miniussi et al., 2008).
Episodic memory encoding and retrieval pro-
cesses have been linked to different networks; lesion
and functional imaging studies have indicated
that episodic memory involves a widespread net-
work of brain structures, including the prefrontal
cortex (PFC) and the posterior parietal cortex
(Cabeza, Ciaramelli, Olson, & Moscovitch, 2008).
In elderly subjects, successful memory encoding
and retrieval is associated with activation of the
left inferior parietal lobules (IPL) and the anterior
hippocampus (Kircher et al., 2008).
We wish to thank the patient for his patience and Michela Brambilla for her help with experimental assistance. This research was
supported by a project grant from the ‘Fondazione della Comunità Bresciana-ONLUS’.
Address correspondence to Maria Cotelli, PhD, IRCCS Centro San Giovanni di Dio Fatebenefratelli, Via Pilastroni, 4, 25125 Brescia,
Italy. (E-mail: mcotelli@fatebenefratelli.it).
In healthy participants, rTMS studies have con-
firmed the role of the PFC during encoding and
retrieval of verbal or non-verbal material (Rossi
et al., 2001; Sandrini, Cappa, Rossi, Rossini, &
Miniussi, 2003). However, regarding rTMS stud-
ies in posterior brain areas, the mechanism has
not yet been elucidated. Previous studies have
demonstrated the involvement of parietal areas,
which is in contrast to rTMS studies. In particu-
lar, Rossi et al. (2006) found that the activity of
the intraparietal sulci, unlike that of the dorsolat-
eral prefrontal cortex (DLPFC), are not causally
involved in the encoding and retrieval of visual
scenes; however, by combining functional Magnetic
Resonance Imaging (fMRI) and rTMS, Manenti,
Tettamanti, Cotelli, Miniussi, and Cappa (2010)
provided the first evidence for the causal role of
c
2012 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business
http://www.psypress.com/neurocase http://dx.doi.org/10.1080/13554794.2011.588176
Downloaded by [University of Sydney] at 15:42 15 August 2012
218 COTELLI ET AL.
not only prefrontal but also parietal cortices during
word retrieval.
Furthermore, Sole-Padulles et al. (2006) demon-
strated a beneficial role of high-frequency rTMS
in associative memory among elderly subjects with
memory deficits and low performance on neu-
ropsychological memory tests. The study combined
rTMS and fMRI and showed a selective behavioral
improvement in a face–name association memory
task following an off-line stimulation. Moreover,
this improvement was associated with the recruit-
ment of the right PFC and bilateral posterior
cortices.
Mild Cognitive Impairment (MCI) is widely
used to define the disorder in individuals who
have subjective cognitive deficits, objective memory
impairments, or other cognitive deficits, without
impairments in daily activities (Petersen et al.,
1999).
Despite the clinical impact, there is no published
evidence that rTMS can induce improvements
in patients with selective memory impairment.
Previous imaging and rTMS studies have shown
the involvement of the DLPFC and the parietal
cortex during memory processes, suggesting that,
in patients with memory deficits, stimulation of
these areas could induce improvements in memory.
The aim of this study was to assess whether rTMS
applied to the left parietal cortex, could induce
improvements in memory performance in an indi-
vidual with amnestic Mild Cognitive Impairment
(aMCI).
CASE REPORT
A 61-year-old man, with 18 years of education, was
referred for memory complaints. He was diagnosed
with aMCI (MMSE: 27), according to clinical cri-
teria (Petersen et al., 1999).
His evaluation included formal neuropsycholog-
ical testing (Table 1), a physician interview, and
a neurological examination. The patient had his
first clinic visit 18 months prior to enrolling in the
present study. During this period, he was exam-
ined regularly every 6 months. A physician (O.Z.)
completed a medical history and conducted gen-
eral physical, neurological, and psychiatric exam-
inations. The patient had no history of neurolog-
ical or psychiatric disorders, alcohol abuse, psy-
chosis, major depression (Hamilton Depression
Rating Scale =4), or sleep disturbances. There was
no indication of dementia, according to the clin-
ical interview with the patient and his caregiver
(Clinical Dementia Rating, CDR =0.5). The diag-
nosis of aMCI was confirmed at the follow-up
visits, and the patient had been steadily treated
with Rivastigmine Patch (9.5 mg/day) for the previ-
ous 12 months. The patient did not take any other
medication.
He was selected for this study based on the fol-
lowing criteria (Sarazin et al., 2007): (i) a subjec-
tive memory complaint assessed by the Everyday
Memory Questionnaire (Sunderland, 1984); (ii) an
objective memory impairment assessed by specific
neuropsychological memory tests; (iii) preserva-
tion of general cognitive functioning assessed by
general neuropsychological tests; (iv) a normal
Instrumental Activities of Daily Living (IADL)
score (Lawton & Brody, 1969); and (v) the absence
of the diagnostic criteria for dementia (American
Psychiatric Association, 1987). A structural brain
MRI excluded the presence of cerebrovascular dis-
ease and white matter lesions.
An experienced neuropsychologist (M.C.)
administered and evaluated a comprehensive
diagnostic set of memory tests. The cognitive
assessment included tests to screen for dementia
(Mini Mental State Examination) and neuropsy-
chological tests to assess non-verbal reasoning
(Raven Colored Progressive Matrices), language
comprehension (Token Test), verbal fluency
(phonemic and semantic), memory (Story recall;
Auditory-Verbal Learning Test, immediate and
delayed recall; Rey-Osterrieth Complex Figure,
recall; Digit Span; Spatial Span; Serial Position
Curve), apraxia and visuo-spatial abilities (De
Renzi Imitation Test; Rey-Osterrieth Complex
Figure, Copy), and attention and executive func-
tions (Trail-Making Test A and B; Wisconsin Card
Sorting Test). All of the tests were administered
and scored according to the standard procedures
(Lezak, Howieson, & Loring, 2004). The cognitive
assessment was divided into two parts, a standard
evaluation and an experimental evaluation, and
both were administered at baseline (before the
rTMS treatment), shortly after the rTMS treatment
(2 weeks), and 24 weeks after the baseline. The
results of the baseline cognitive assessment are
reported in Table 1.
For the experimental evaluation, we used an
unfamiliar face–name association task (FNAT)
composed of an encoding and a retrieval phase.
During the encoding phase, the patient was shown
a grey-scale picture of a face on a monitor followed
by a proper name. During the retrieval phase, the
patient was shown a face with two proper names
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BRAIN STIMULATION IMPROVES MEMORY 219
TABLE 1
Patient’s performance on general standard neuropsychological tests
Adjusted score
baseline
Adjusted score after
rTMS (2 weeks)
Adjusted score at follow
up (24 weeks) Cut-offs
Screening for dementia
MMSE 24.5/30 25.5/30 24.6/30 24
Non-verbal reasoning
Raven Colored Progressive
Matrices
33/36 34/36 33/36 >17.5
Memory
Story recall 12 14/28 13/28 >7.5
Auditory-Verbal Learning Test,
immediate recall
33.8/75 30.8/75 31.8/75 >28.52
Auditory-Verbal Learning Test,
delayed recall
3.6/15∗5.4/15 3.6/15∗>4.68
Rey-Osterrieth Complex Figure,
Recall
9.3/36∗8.3/36∗6.8/36∗>9.46
Spatial Span 5.8 5.8 5.8 >3.50
Digit Span 7.5 5.5 5.5 >3.75
Serial position curve
Primacy effect 4∗8 8 >4.5
Recency effect 20 22 23 >7.5
First item 1.25 4.25 0.25 >0
Language
Token Test 30.5/36 32.5/36 31.5/36 >26.25
Fluency, phonemic 56 48 44 >16.0
Fluency, semantic 52 63 59 >24.0
Praxia
Rey-Osterrieth Complex Figure,
Copy
33.5/36 36/36 33.5/36 >28.88
De Renzi Imitation test, dx 71/72 71/72 72/72 >62.0
De Renzi Imitation test, sx 67/72 68/72 71/72 >62.0
Executive funcion
Trail-Making Test A 18 13 13 <93.0
Trail-Making Test B 69 53 52 <282.0
Trail-Making Test B–A 45 34 33 186
Wisconsin Card sorting test,
Global score
23.8/128 14.8/128 20.8/128 <90.60
Wisconsin Card sorting test,
Perseverative Responses
11.2 9.2 6 <42.70
Wisconsin Card sorting test,
Non-perseverative Errors
4.6 5.6 5 <30.0
Wisconsin Card sorting test,
Failure to mantain set
1 0 0 <4.0
Age- and education-adjusted scores are reported. ∗denotes scores below cut-off.
(i.e., the correct name and another previously pre-
sented name), and the patient had to associate the
correct name to the face. During the encoding, the
participant was required to respond if a male or
female face was presented and to encode the face–
name association. During the retrieval, the patient
was required to associate one of the two presented
proper names to the face, as was presented during
the encoding.
The FNAT was used to assess the patient’s
associative memory. Each stimulus consisted of
a grey-scale face associated with a proper name.
Faces were downloaded from an electronic dataset
on the web and processed by Adobe Photoshop 5.0
(http://www.adobe.com). The unfamiliar faces were
photographs of people unknown to the patient. A
set of 50 unfamiliar faces was identified (25 males,
25 females). These pictures were scaled to 210 ×263
pixels and presented on a computer screen (sub-
tending a visual angle of 3.15◦×4◦). With respect
to names, a set of 50 (25 males, 25 females) unfa-
miliar proper names were generated and randomly
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220 COTELLI ET AL.
assigned to the unfamiliar faces. Both the encod-
ing and the retrieval phases were comprised of two
training trials followed by three separate blocks of
16 trials, with each presented in a random order.
Gender of the stimuli were counterbalanced and
randomized across blocks. Responses were col-
lected via a response-box, and the stimuli remained
on the screen until the response was made. Finally,
to exclude any learning effects resulting from its
repeated execution, the task was conducted twice
at baseline (i.e., baseline 1 and baseline 2) before
rTMS treatment.
In addition, the same task was administered to
22 normal control (NC) subjects comparable in age
and education (age: 64 ±4; education: 13 ±4)
to investigate both the experimental performance
and the learning abilities of a healthy aging group.
The evaluation in the NC group was performed
with the same timing as that used for the patient
(i.e., baseline 1, baseline 2, and 2 weeks), with the
exception of the 24-week evaluation. The protocol
was approved by the Ethics Committee of IRCCS
Fatebenefratelli, Brescia, Italy.
rTMS PROCEDURE
Based on previous rTMS and neuroimaging studies
of episodic memory, we defined the DLPFCs and
IPL as potential target areas for rTMS treatment
(Cabeza et al., 2008; Manenti et al., 2010; Rossi
et al., 2006; Sandrini et al., 2003).
To determine the location of a target area for the
off-line rTMS treatment, we initially conducted two
on-line rTMS experimental sessions during which
each of the named areas, DLPFC and IPL, was
stimulated individually.
We localized the left and right DLPFC and
IPLs using the SofTaxic Evolution navigator system
(www.emsmedical.net).
Prior to rTMS application, the motor threshold
was defined as the lowest stimulation intensity over
the primary motor cortex that resulted in a contrac-
tion in the contralateral hand, of at least 50%, in
10 consecutive stimulations (42% of the maximum
stimulator output in our patient).
Two on-line rTMS tests (i.e., during FNAT) were
performed: one for the DLPFCs and one for the
IPLs. On-line rTMS was applied while the patient
was performing the retrieval phase of the FNAT.
We proposed that the stimulation of one of these
areas during the execution of the FNAT could mod-
ify performance (i.e., accuracy). Each on-line rTMS
test included three blocks corresponding to three
stimulation types (left, right and sham stimulation;
20 Hz for 500 ms, from the trial onset, at 100% of
the motor threshold). We found that only stimula-
tion of the left IPL improved accuracy in the FNAT
(p=.04) compared to sham.
Subsequently, the patient received daily rTMS
treatments, 5 days a week for 2 weeks (25 min-
utes per day), to the left IPL (Talairach coordi-
nates –44, –51, 43). A rapid magnetic stimulator
and a figure-eight, double 70 mm, cooled coil
(www.magstim.com) were used for rTMS admin-
istration. Fifty trains of high-frequency (20 Hz)
rTMS were delivered for 2 seconds with an inter-
stimulus interval of 28 seconds (40 stimuli/train,
50 trains, 2000 pulses/session, five sessions/week,
2 weeks). The stimulation intensity was set to 100%
of the motor threshold. These parameters are con-
sistent with the safety recommendations for rTMS
(Rossi, Hallett, Rossini, & Pascual-Leone, 2009),
and the patient reported no adverse effects.
RESULTS
For the two baseline evaluations (baseline 1 and 2;
Figure 1), the patient’s performance did not change;
therefore, no learning repetition effects were present
for the FNAT (χ2<1, df =1, p>.05). In contrast,
for the NC group, the repetition of the task resulted
in an improvement in performance, F(2, 42) =39,
p<.001. Post-hoc analyses (Bonferroni) revealed
that the NC group’s performance during the sec-
ond (2 days after baseline 1) and the third (2 weeks
after) repetitions were higher than the performance
90
80
70
CORRECT RESPONSES %
60
50
40
Baseline 1 Baseline 2 2 weeks 24 weeks
aMCI
NC
Figure 1. Percentage of correct responses (%) in a face–name
association task (FNAT) over several sessions. aMCI, amnestic
mild cognitive impairment patient; NC, normal control group.
Error bars represent the standard errors of only one side. The
dotted line indicates chance performance.
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BRAIN STIMULATION IMPROVES MEMORY 221
during the first presentation (baseline 1; p<.001);
there was no difference between the second and
third repetitions (baseline 2 vs. 2 weeks; p>.05).
Regarding the rTMS treatment, the patient’s per-
formance on the FNAT was compared, using the
non-parametric χ2statistical test (Figure 1), to
the four time points: baseline (pre-treatment; mean
between the first two repetitions of the task, base-
line 1 and 2), 2 weeks (post-treatment) and at the
follow-up (24 weeks after baseline). The analysis
showed a significant improvement in the patient’s
performance on the FNAT after 2 weeks of rTMS
(73%) with respect to baseline (54%) (χ2=6.99,
df =1, p<.001, Yates correction). The improve-
ment was still significant 24 weeks after treatment
(79%) as compared to baseline (χ2=13, df =1,
p<.001). The performance at 24 weeks was not dif-
ferent from the score obtained at 2 weeks (p>.05),
suggesting that the increased performance observed
at 2 weeks was stable until follow-up.
Compared with the NC group, the patient did
not show an improvement in performance resulting
from the repetition of the task (no difference
between the first two repetitions baseline 1 vs. 2),
but the patient did demonstrate an increased
performance after rTMS treatment. The direct
comparison between the patient’s performance and
the performance of the healthy subjects revealed
a significant difference at baseline, t(21) =5.1,
p<.001, at the second repetition, t(21) =11.6,
p<.001, and after 2 weeks, t(21) =5.0, p<.001,
while the patient’s performance after 24 weeks was
not different from the NC group after 2 weeks,
t(21) =1.9, p>.05.
In the baseline neuropsychological standard eval-
uation, the patient had scores below cut-off on
some memory tasks: delayed recall of Auditory-
Verbal Learning Test, recall of Rey-Osterrieth
Complex Figure and Primacy effect of Serial
Position Curve task. Two weeks after rTMS treat-
ment onset, we observed an improvement on
the delayed recall of Auditory-Verbal Learning
Test and the Primacy effect of Serial Position
Curve task. However, only the improvement in the
Primacy effect of Serial Position Curve task per-
sisted 24 weeks after treatment. Primacy is strongly
correlated to the consolidation of long-term
memory. The patient’s improvement in this task
suggests an increase in the ability to encode verbal
items to memory, which parallels the improvement
on FNAT.
DISCUSSION
The goal of this study was to assess whether appli-
cation of high-frequency rTMS to the left IPL for
25 minutes a day, 5 days a week, for 2 weeks
would lead to significant increases in memory per-
formance in an individual with aMCI.
Previous neuroimaging evidence suggests that, in
elderly subjects, successful memory encoding and
retrieval is associated with activation of the left
IPL and the anterior hippocampus (Kircher et al.,
2008). The present study provides direct evidence
for a putative role of the left IPL in associative
memory and its enhancement by rTMS. Similarly,
using imaging data, Sole-Padulles et al. (2006) have
shown that elderly adults who received DLPFC
rTMS temporarily improved their performance in
an association memory task by activating the pre-
frontal and posterior areas.
In this vein, it has also been suggested that the
recruitment of a larger neural network in older par-
ticipants (Dennis & Cabeza, 2010), as well as in
Alzheimer’s patients, might reflect attempts to com-
pensate for functional loss (Backman et al., 1999).
Although the mechanisms involved in enhancing
memory formation from rTMS are still specula-
tive, rTMS might interact with the brain to main-
tain or strengthen the neural connections between
regions. The present findings may reflect rTMS-
induced neuromodulation, which promotes a long-
term rearrangement of synaptic connections within
a precise network. Comparing the patient with
the NC group, which showed learning after the
first repetition, allowed us to exclude the hypoth-
esis that the patient’s improvement was due to
task repetition and therefore practice effects. The
present results are consistent with previous stud-
ies, which have shown that neuromodulation of a
specific behaviourally-activated network produces
an increase in cortical efficacy when performing a
cognitive task.
Several studies have suggested that rhythmic
transcranial stimulation can enhance cognitive
performance (Miniussi et al., 2008). A possible
mechanism might be that the modulation of corti-
cal activity through the use of rhythmic stimulation
may re-adjust pathological patterns of brain activ-
ity, which provides an opportunity to induce new,
improved activity patterns with an enhancement of
the affected functional networks (Thut & Miniussi,
2009).
Downloaded by [University of Sydney] at 15:42 15 August 2012
222 COTELLI ET AL.
The preliminary results presented here highlight
the therapeutic potential of the induction of long-
term neuromodulation using brain stimulation in
the treatment of aMCI. Our patient showed a sta-
ble aMCI diagnosis over 24 weeks, and until the
patient was studied, he did not show any other cog-
nitive or psychiatric disorder. We found that the
improvement due to rTMS treatment was specific to
the associative memory task. In addition, immedi-
ately after 2 weeks of rTMS treatment, we observed
an improvement in performing neuropsychological
tasks that assess long-term memory.
The major limitation in our study was the use of
a single case and the lack of a placebo condition.
However, several factors suggest that the cogni-
tive improvement observed in our study cannot be
solely accounted for by task practice effects. First,
it seems unlikely that the magnitude of improve-
ment found in this study is solely due to a task
practice effect. We also show the absence of any
rTMS effects on language, apraxia, visuo–spatial
abilities, and executive functions, suggesting the
specificity of the result, and the repetition learn-
ing effects cannot be explained by the present data.
Furthermore, normal control subjects, who did not
receive real rTMS treatment, did not show any sig-
nificant improvement in FNAT task when tested
after the third evaluation. We cannot exclude, how-
ever, that the absence of any additional improve-
ment on the FNAT is due to the high performance
obtained rapidly by the control group.
We acknowledge that these are preliminary find-
ings, and present data cannot entirely rule out
the practice effect, therefore future studies should
use parallel versions of the same neuropsycholog-
ical assessments to evaluate cognitive performance
pre- and post-stimulation. However, if confirmed in
larger samples, using a randomized, blinded design
(e.g., real vs. placebo rTMS), these results could
highlight the potential role of transcranial brain
stimulation in modulating and facilitating memory
performances in individuals with aMCI.
As to the long-term effects, we identified an
improvement in the formation of associative mem-
ories 20 weeks after the end of rTMS treatment
(24 weeks from the baseline). To date, this is the
first study that has shown a long-lasting cogni-
tive role of rTMS treatment in aMCI patients. A
recent study described a long-lasting (12 weeks
post-treatment) improvement on sentence compre-
hension tasks after rTMS in Alzheimer’s disease
patients (Cotelli et al., 2011), but no studies have
investigated rTMS effects in aMCI. These find-
ings may reflect a rTMS-induced modulation of
short- and/or long-range cortical synaptic efficacy
and connectivity that potentiates the functional net-
work, which leads to more effective processing. This
neuromodulation could explain the long-lasting
effects even if the mechanism behind these changes
remains poorly understood.
The possibility of using brain stimulation as a
tool to promote neuroplasticity is promising, not
only for advancing our understanding of brain
plasticity mechanisms but also for designing new
neurorehabilitation strategies.
Original manuscript received 22 July 2010
Revised manuscript accepted 11 May 2011
First published online 1 September 2011
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