NEUROLOGY AND PRECLINICAL NEUROLOGICAL STUDIES - ORIGINAL ARTICLE
Jou nal o Neu al T ansmission (2024) 131:791–797
h ps://doi.o g/10.1007/s00702-024-02771-5
he e idence sugges s ha le odopa has no signi ican sho -
e m e ec s on speech (Skodda e al. 2010; Ca allie i e al.
2021). Longi udinal s udies (Rusz e al. 2016; Tykalo a
e al. 2015) e ealed ha le odopa adminis a ion in he
ea ly s ages o PD may imp o e consonan a icula ion bu
also lead o mo e dys luen speech. A ecen s udy (Rusz e
al. 2021) ound a iable esponses o long- e m le odopa
adminis a ion among ea ly PD pa ien s depending on spe-
ci ic HD pheno ypes.
Speech indings a e he deep b ain s imula ion (DBS)
also a y (Skodda e al. 2014; Baudouin e al. 2023). P e i-
ous esea ch showed ha DBS may imp o e oice emo
o oice in ensi y (T ipoli i e al. 2011; Tsuboi e al. 2014),
bu a he same ime, i may wo sen speech in elligibili y
(T ipoli i e al. 2011, 2014; Pin o e al. 2014; Tsuboi e al.
2014). P edic i e ac o s o his de e io a ion include longe
disease du a ion and lowe speech in elligibili y be o e su -
ge y (T ipoli i e al. 2014; Pin o e al. 2023). Taken oge he ,
he e ec s o pha macological and su gical in e en ions
on HD a e limi ed and a ied. The e o e, he e is a need o
In oduc ion
App oxima ely 90% o indi iduals wi h PD expe ience
hypokine ic dysa h ia (HD) as he disease p og esses
(Ramig e al. 2008). HD is de ined by dec eased a iabili y
in pi ch and olume, imp ecise a icula ion, impai ed speech
p osody, and inapp op ia e silences (B abenec e al. 2017).
S udies examining he e ec o dopamine gic medica ion
on HD epo mixed esul s (B abenec e al. 2017). Mos o
I ena Rek o o a
[email p o ec ed]
1 Applied Neu oscience Resea ch G oup, Cen al Eu opean
Ins i u e o Technology – CEITEC, Masa yk Uni e si y,
B no, Czech Republic
2 Depa men o Telecommunica ions, B no Uni e si y o
Technology, B no, Czech Republic
3 Facul y o Medicine and S . Anne’s Uni e si y Hospi al, Fi s
Depa men o Neu ology, B no, Czech Republic
Abs ac
In oduc ion: Hypokine ic dysa h ia (HD) is a common mo o speech symp om o Pa kinson’s disease (PD) which does
no espond well o PD ea men s. We in es iga ed sho - e m e ec s o ansc anial di ec cu en s imula ion ( DCS)
on HD in PD using acous ic analysis o speech. Based on ou p e ious s udies we ocused on s imula ion o he igh
supe io empo al gy us (STG) - an audi o y eedback a ea. Me hods: In 14 PD pa ien s wi h HD, we applied anodal,
ca hodal and sham DCS o he igh STG using a c oss-o e design. A p o ocol consis ing o speech asks was pe o med
p io o and immedia ely a e each s imula ion session. Linea mixed models we e used o he e alua ion o he e ec s
o each s imula ion condi ion on he ela i e change o acous ic pa ame e s. We also pe o med a simula ion o he mean
elec ic ield induced by DCS. Resul s: Linea mixed model showed a s a is ically signi ican e ec o he s imula ion
condi ion on he ela i e change o median du a ion o silences longe han 50 ms (p = 0.015). The ela i e change a e
he anodal s imula ion (mean = -5.9) was signi ican ly lowe as compa ed o he ela i e change a e he sham s imula-
ion (mean = 12.8), p = 0.014. We also ound a co ela ion be ween he mean elec ic ield magni ude in he igh STG
and imp o emen o a icula ion p ecision a e anodal DCS (R = 0.637; p = 0.019). Conclusions: The explo a o y s udy
showed ha anodal DCS applied o e he audi o y eedback a ea may lead o sho e pauses in a speech o PD pa ien s.
Keywo ds Pa kinson’s disease · Hypokine ic dysa h ia · T ansc anial elec ic s imula ion · Acous ic analysis · Supe io
empo al gy us
Recei ed: 9 Feb ua y 2024 / Accep ed: 25 Ma ch 2024 / Published online: 9 Ap il 2024
© The Au ho (s) 2024
Sho - e m e ec s o ansc anial di ec cu en s imula ion on mo o
speech in Pa kinson’s disease: a pilo s udy
LubosB abenec1· DanielKo ac2· Ji iMekyska2· LenkaRehulko a1,3· Ve onikaKab o a1,3· I enaRek o o a1,3
1 3
L. B abenec e al.
explo e o he me hods ha a ge di e en aspec s o speech
and could po en ially be used also in la e s ages o PD.
We ocused ou esea ch on non-in asi e b ain s imula-
ion me hods (NIBS). In PD pa ien s wi h HD, epe i i e
ansc anial magne ic s imula ion ( TMS) has been mos ly
applied o e a p ima y o o acial a ea (OFSM1) wi h incon-
sis en esul s (B abenec e al. 2017). Howe e , p e ious
esea ch showed ha pa icula ly he igh pos e io supe io
empo al gy us (STG), a co ical egion in ol ed in audi-
o y speech eedback (Liu e al. 2023), plays an impo an
ole in modula ion o mo o aspec s o speech p oduc ion in
PD pa ien s (New e al. 2015; Klobusiako a e al. 2021). In
ou p e ious s udy (B abenec e al. 2019), we demons a ed
ha a single session o 1 HZ TMS o e he igh STG may
lead o signi ican imp o emen o a icula ion in PD. The
imp o emen s we e signi ican ly highe han imp o emen s
a e 10 Hz s imula ion o e he le OFSM1, and mo e p o-
nounced han he s imula ion o a con ol s imula ion si e
(B abenec e al. 2019). A subsequen s udy also showed
ha mul iple sessions o ac i e TMS o e he igh STG,
as compa ed o sham s imula ion, had long-las ing posi i e
e ec s on HD, pa icula ly on pe cep ual measu es o a ic-
ula ion, p osody, and speech in elligibili y. These e ec s
we e suppo ed by emo e s imula ion-induced b ain plas-
ici y changes wi hin he a icula o y ne wo ks (B abenec
e al. 2021).
In ou cu en p ojec , we aim o de elop a p og am o
emo e ea men o HD. To achie e ou goal, we chose
ansc anial di ec cu en s imula ion ( DCS) ha can be
used emo ely by pa ien s a home oge he wi h a concu -
en Lee Sil e man Voice T ea men (LSVT), i.e., he bes
documen ed he apy o symp oms o HD in PD (Yuan e
al. 2020). In PD pa ien s, DCS and o he modes o em-
po al elec ical s imula ion ( ES) ha e mos ly been used o
modula e gai speed, eezing o gai , limb b adykinesia,
a en ion and execu i e unc ions, and b ain exci abili y
(Ni e al. 2022). S udies also p o ided e idence ha home-
based DCS ea men is easible and sa e o PD pa ien s
(Dobbs e al. 2018). To ou knowledge, esea ch on he
e ec s o DCS/ ES on HD symp oms in PD has no ye
been conduc ed.
In his pilo s udy, we pa icula ly concen a ed on iden i-
ying a sui able elec ode mon age and examined immedia e
a e e ec s o a single session o DCS on HD symp oms.
These acu e e ec s could las up o an hou (Ni sche e al.
2008; B unoni e al. 2012). S udies ha e also shown ha
di e en cu en low di ec ions may esul in di e en a e -
e ec s, and he di ec ion o he exci abili y shi migh be
di e gen , dependen no only on s imula ion pola i y, bu
also on he speci ic elec ode mon age (Ni sche e al. 2008).
The e o e, we applied bo h anodal and ca hodal DCS o he
igh STG. We also used SimNIBS (Thielsche e al. 2015)
so wa e o simula ion o he mean elec ic ield induced by
DCS. Rega ding beha io al ou comes, we ocused on he
acous ic pa ame e s ha we e esponsi e o non-in asi e
b ain s imula ion me hods in ou p e ious s udies (B abenec
e al. 2017, 2019).
Me hods
Pa icipan s
The inclusion c i e ia o en olmen in o he s udy we e
as ollows: (1) clinically es ablished PD (c i e ia by Pos-
uma e al. 2016), (2) igh -handedness, (3) p esence o
HD symp oms based on he assessmen o a speech he a-
pis and he esul s o a 3F Tes Dysa h ic p o ile o al
sco e (Kos alo a 2013), (4) Czech as hei i s language.
Exclusion c i e ia we e (1) alcohol o d ug abuse, (2) hal-
lucina ions, (3) any diagnosed psychia ic diso de (4)
demen ia, based on he Mon eal Cogni i e Assessmen
(MoCA) es o demen ia, MoCA > 20 (Biundo e al.
2014), and on a clinician’s in e iew wi h a ca egi e (5)
ca dio pacemake o any MRI-incompa ible me al in he
body, (6) epilepsy.
The disease se e i y was assessed using he Uni ied Pa -
kinson’s Disease Ra ing Scale (UPDRS), pa III (Mo o
Examina ion) scale. All pa icipan s we e on a s able dopa-
mine gic medica ion a leas 4 weeks p io o baseline
assessmen and du ing he whole s udy. The pa ien s we e
es ed in he ON medica ion s a e wi hou dyskinesias since
we wan ed o modula e HD symp oms in a eal-li e scena io
in pa ien s on dopamine gic medica ion. All pa ien s signed
an in o med consen o m ha was app o ed by he local
e hics commi ee.
S udy design
Pa icipan s unde wen DCS o e he igh pos e io
STG. A he baseline isi , each pa icipan unde wen a
speech assessmen using he 3F Tes Dysa h ic p o ile
(Kos alo a 2013) ( o de ails see Table S1 in Supple-
men a y ma e ials). S uc u al MRI scans (T1 MPRAGE)
we e pe o med o ameless s e eo ac ic na iga ion o
he elec ode placemen . A e he baseline isi , each
pa icipan unde wen h ee s imula ion sessions (anodal,
ca hodal, and sham s imula ion), sepa a ed by one day
wi hou s imula ion. A c osso e double-blind design was
used, and s imula ion p o ocols we e andomized ac oss
subjec s and sessions.
A p o ocol consis ing o speech asks las ed up o 10 min
and was pe o med p io o and immedia ely a e each
s imula ion session.
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Sho - e m e ec s o ansc anial di ec cu en s imula ion on mo o speech in Pa kinson’s disease: a pilo …
Acous ic analysis o speech
The speech p o ocol con ained a special eading ask ( ead-
ing a phone ically balanced pa ag aph con aining 150
wo ds; pa ien s we e allowed ead he ex in ad ance). HD
symp oms we e assessed using speech pa ame e s o in e -
es based on ou p e ious esea ch.(B abenec e al. 2019)
Mo e speci ically, we quan i ied ongue and jaw igidi y
( elF1SD and elF2SD), monopi ch ( elF0SD), du a ion o
silences (Du MED), and i egula speech hy hms (SPIR)
(see Table 1 o de ailed desc ip ion o he pa ame e s).
TDCS p o ocol
S imula ion was applied h ough a ba e y-d i en de ice
(DC-S imula o Plus, neu oConn GmbH, Ge many). Bo h
elec odes we e posi ioned o e he igh and le pos e io
supe io empo al gy us (STG) (MNI coo dina es: X = 40,
Y = − 38, Z = 14; X = − 40, Y = − 38, Z = 14; based on ou
p e ious esea ch) (B abenec e al. 2021). We used he T1
MRI scan-based ameless s e eo ac ic neu ona iga ion o
speci y he exac loca ion o he elec ode cen e in each
indi idual. Fo anodal s imula ion, he anode was placed
o e he igh STG and he ca hode o e he le STG. Fo
ca hodal s imula ion, he ca hode was placed o e he igh
STG and he anode o e he le STG.
A cu en o 2 mA was deli e ed using wo ubbe elec-
odes (5 × 5 cm) o 20 min. The elec ode was held in place
by a conduc i e gel. The sham s imula ion was applied wi h
he same se ings, bu he s imula o was u ned o a e
30 s.
S a is ical analysis
We used linea mixed models (LMM) o e alua e he e ec s
o each s imula ion condi ion on he ela i e changes in
acous ic pa ame e s. The s imula ion condi ion was a ixed
ac o in LMM. Pos -hoc pai wise compa isons o es ima ed
ma ginal means we e made wi h he Bon e oni co ec ion.
Age, gende , and le odopa equi alen dose (LED) we e
used as co a ia es in all LMMs. Wilcoxon signed- ank es s
we e used o compa e he alues o hese pa ame e s p io
o and a e each s imula ion condi ion. A Spea man co -
ela ion analysis was used o assess associa ions be ween
he DCS-induced changes and he simula ion o he elec ic
ield in igh STG. These s a is ical p ocedu es we e pe -
o med wi h IBM SPSS Ve sion 25.0 (IBM Co p., A monk,
NY, USA).
Table 1 Analyzed acous ic ea u es in eading ask
HD dimension and speci ic diso de Acous ic ea u e Fea u e de ini ion Fea u e in e p e a ion
Rigidi y o ongue and jaw elF1SD, elF2SD S anda d de ia ion o i s (F1) and second (F2) o man ela i e o i s mean. Highe alue means be e
pe o mance
Monopi ch elF0SD Pi ch a ia ion, de ined as a s anda d de ia ion o F0 con ou ela i e o i s mean. Highe alue means be e
pe o mance
I egula hy hm o speech SPIR Numbe o pauses ela i e o o al speech ime a e emo ing pe iods o silence las ing
less han 50 ms.
Highe alue means be e
pe o mance
Longe du a ion o silences Du MED Median du a ion o silences longe han 50 ms. Lowe alue means be e pe o mance
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793
L. B abenec e al.
Resul s
We en olled 14 igh -handed pa ien s wi h clinically es ab-
lished PD. All had mild o mode a e HD based on he
assessmen o a speech he apis and he esul s o a 3F Tes
Dysa h ic o al sco e (Kos alo a 2013). The maximum
o al sco e is 90 (no mal speech), and he minimum sco e is
0. See Table 2 o demog aphic and clinical da a.
Using linea mixed model analysis (LMM) (see Table 3),
we obse ed a signi ican e ec o he s imula ion condi-
ion on changes in he median du a ion o silences longe
han 50 ms (F(2,21.8) = 5.1, p = 0.015), i.e. inapp op ia e
silences ha nega i ely impac speech hy hm and speech
luency (B abenec e al. 2017). The ela i e dec eases in
long pauses a e anodal s imula ion (mean = -5.9) we e
signi ican ly highe han he changes a e he sham s imula-
ion (mean = 12.8), p = 0.014, and non-signi ican ly highe
han he changes induced by he ca hodal s imula ion (mean
= -0.5), p = 0.111 (see Fig. 1). Resul s o Pos -hoc Wilcoxon
es showed ha anodal s imula ion induced a signi ican
dec ease o his pa ame e (p = 0.047) (see Table 4).
Elec ic ield simula ion, as assessed by SimNIBS, (Thiel-
sche e al. 2015) indica ed a signi ican co ela ion be ween
he mean elec ic ield in he igh STG and ela i e changes
in he s anda d de ia ion o he second o man a e anodal
DCS (R = 0.637; p = 0.019) (see Table 5 and Fig. 2). This
pa ame e desc ibes he ongue and jaw mo emen s, and i
is used o e alua ing a icula ion p ecision (B abenec e al.
2017). Howe e , his pa ame e did no signi ican ly change
due o he s imula ion.
Elec ic ield simula ion in SimNIBS
SimNIBS so wa e ( e sion 4.0.1) was used o calcula e he
elec ic ield induced by DCS, based on he ini e elemen
me hod and indi idualized e ahed al head meshes gene -
a ed om he s uc u al T1 images o he pa icipan . Elec-
ic ield simula ions we e compu ed o bo h ca hodal and
anodal mon ages. Bo h elec odes we e posi ioned based
on he MNI coo dina es men ioned p e iously. The mean
elec ic ield in he igh STG (sphe e adius = 10 mm) was
calcula ed using a MATLAB sc ip .
Table 2 Demog aphic and clinical a iables
Gende Female/Male 7/7
Age (yea s) Mean 70.78 (SD 7.84)
Du a ion o PD (yea s) Mean 5.03 (SD 4.18)
LED (mg/day) Mean 1014.04 (SD 343.16)
UPDRS III Mean 11.21 (SD 4.24)
3F Tes To al sco e Mean 74.42 (SD 7.41)
MOCA Mean 25.43 (SD 2.14)
M - Mean; SD - S anda d de ia ion; PD - Pa kinson’s disease; LED -
Le odopa equi alen dose; UPDRS III - Uni ied Pa kinson’s disease
a ing scale; MOCA - Mon eal Cogni i e Assessmen
Table 3 Acous ic analysis - Resul s o linea mixed models
Acous ic pa ame e Fp alue
elF1SD 5.136 0.211
elF2SD 2.528 0.104
elF0SD 1.657 0.214
SPIR 0.759 0.481
Du MED 5.135 0.015
Fig. 1 Rela i e changes in he median du a ion o silences longe han 50 ms a e dis inc ac i e and sham DCS
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Sho - e m e ec s o ansc anial di ec cu en s imula ion on mo o speech in Pa kinson’s disease: a pilo …
Discussion
This explo a o y c oss-o e andomized s udy ound ha
anodal DCS a ge ing he audi o y eedback a ea in he
igh hemisphe e can signi ican ly imp o e mo o speech
luency in PD pa ien s. Mo eo e , he elec ic ield in his
egion was posi i ely co ela ed wi h anodal DCS-induced
changes in a icula ion p ecision.
These esul s a e in pa ial acco d wi h he esul s o ou
TMS s udy in which low- equency s imula ion was used.
No ably, TMS-induced BOLD signal inc eases o he igh
STG we e associa ed wi h changes o he same a icula ion
pa ame e as in he cu en s udy (B abenec e al. 2019).
The e o e, i seems plausible ha bo h s imula ion p o o-
cols may lead o simila neu al changes, bu unlike in ou
TMS s udy he e ec o anodal DCS alone was p obably
oo weak o ansla e in o signi ican beha io al imp o e-
men s in a icula ion. Imp o ed mo o speech luency was
no iden i ied in ou single session TMS s udy; howe e ,
Table 4 Resul s o Wilcoxon es ; p alues
Acous ic
pa ame e
Median be o e
s imula ion
Median a e
s imula ion
p
alue
Anodal
DCS
elF1SD 0.560 0.586 0.463
elF2SD 0.249 0.249 0.650
elF0SD 0.162 0.160 0.087
SPIR 2.011 1.913 0.861
Du MED 0.110 0.110 0.047
Ca hodal
DCS
elF1SD 0.589 0.559 0.064
elF2SD 0.249 0.237 0.039
elF0SD 0.156 0.158 0.311
SPIR 2.031 1.834 0.087
Du MED 0.105 0.100 0.670
Sham
DCS
elF1SD 0.579 0.557 0.136
elF2SD 0.249 0.256 0.695
elF0SD 0.170 0.166 0.272
SPIR 1.991 1.971 0.638
Du MED 0.110 0.110 0.127
Table 5 Co ela ions be ween s imula ed elec ic ields in he igh STG and ela i e changes in acous ic pa ame e s a e s imula ion
elF1SD elF2SD elF0SD SPIR Du MED
Anodal DCS Spea man R 0.231 0.637 -0.192 -0.159 -0.450
P alue 0.448 0.019 0.529 0.603 0.123
Ca hodal DCS Spea man R 0.165 0.033 0.099 -0.407 0.093
P alue 0.590 0.915 0.748 0.168 0.762
Fig. 2 Co ela ion be ween he mean elec ic ield in he igh STG and ela i e changes in he s anda d de ia ion o he second o man a e
anodal DCS
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L. B abenec e al.
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he e was a end o imp o ed speech hy hmici y; in
o he wo ds, bo h s imula ion p o ocols posi i ely modu-
la ed empo al aspec s o mo o speech ou pu . I has o be
poin ed ou ha di e en asks we e used in he wo s udies:
eading o simple sen ences in he TMS s udy and eading
o he whole pa ag aph in he cu en s udy.
This s udy has se e al limi a ions. We used he same
MNI coo dina es o all pa icipan s and did no implemen
indi idualized s imula ion. Howe e , i is impo an o no e
ha DCS s imula ion is inhe en ly less ocal, and his pilo
s udy se ed as a p epa a ion o home-based s imula ion,
whe e achie ing p ecise indi idualiza ion is no p ac ically
easible. Ou sample size was de e mined based on he
immedia e medium a e e ec s obse ed in a single ses-
sion o TMS (B abenec e al. 2019), bu he e ec s o DCS
could be much weake . Ne e heless, we obse ed signi i-
can e ec o DCS on speech.
The main di e ence be ween he e ec s o TMS and
DCS is ha TMS can igge an ac ion po en ial and DCS
can only modula e es ing memb ane po en ial and change
he p obabili y o he ac ion po en ial occu ence (Ni sche e
al. 2008). Thus, DCS a ec s ac i e neu ons and is usually
combined wi h beha io al aining o mo e p onounced
and long- e m e ec s (Ni e al. 2022). In clinical p ac ice,
he gold s anda d o ea men o HD is cu en ly he LSVT
(Yuan e al. 2020). This high-e o speech he apy is p i-
ma ily ocused on imp o ing speech loudness; p e ious
s udies showed ha LSVT also inc eased he ac i a ion o
he igh STG and hese changes co ela ed wi h imp o ed
speech in elligibili y (Baumann e al. 2018).
The e o e, in a u u e s udy, we will in es iga e long-
e m beha io al e ec s and b ain plas ici y changes due o
he home-based long- e m DCS as an add-on ea men o
emo e LSVT, deli e ed ia elep ac ice.
Acknowledgemen s This p ojec ecei ed unding om he Czech
Minis y o Heal h, g an NU22J-04-00074 and om p ojec
n .LX22NPO5107(MEYS): Funded by Eu opean Union – Nex Gen-
e a ion EU. We also acknowledge he co e acili y MAFIL suppo ed
by MEYS CR (LM2023050 Czech-BioImaging), pa o he Eu o-Bio-
Imaging (h ps://www.eu obioimaging.eu/) ALM and Medical Imag-
ing Node (B no, CZ).
Funding Open access publishing suppo ed by he Na ional Tech-
nical Lib a y in P ague. This p ojec ecei ed unding om he
Czech Minis y o Heal h, g an NU22J-04-00074 and om p ojec
n .LX22NPO5107(MEYS): Funded by Eu opean Union – Nex Gen-
e a ion EU.
Da a a ailabili y The da a ha suppo he indings o his s udy a e
a ailable om he co esponding au ho upon easonable eques .
Decla a ions
Con lic s o in e es None.
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