Neurobiology of Aging 32 (2011) 1505–1513
Age-related changes in the functio
odu
Gut
ld T.
entre, T
b Department of Psychology, University of Windsor, Ontario, Canada
c Communication Disorders, Baycrest, Toronto, Ontario, Canada
d Department of Speech-Language Pathology, University of Toronto, Ontario, Canada
e Rotman Research Institute, Baycrest, Toronto, Ontario, Canada
f Department of Medical Biophysics, University of Toronto, Ontario, Canada
Abstract
Alteration
described fo
speech prod
experimenta
older individ
primary mo
/a/ and /pata
of the exper
temporal pla
bilateral mid
of variance
complex reo
© 2009 Else
Keywords: H
1. Introdu
Due to
uals are a
industrializ
∗ Correspon
Disorders, Un
Tel.: +1 803 7
E-mail ad
0197-4580/$
doi:10.1016/jg Heart and Stroke Foundation of Ontario Centre for Stroke Recovery, Toronto, Ontario, Canada
h Department of Psychology, University of Toronto, Ontario, Canada
i Department of Medicine (Neurology, Rehabilitation Science), University of Toronto, Ontario, Canada
Received 23 December 2008; received in revised form 13 August 2009; accepted 28 August 2009
Available online 25 September 2009
s of existing neural networks during healthy aging, resulting in behavioral deficits and changes in brain activity, have been
r cognitive, motor, and sensory functions. To investigate age-related changes in the neural circuitry underlying overt non-lexical
uction, functional MRI was performed in 14 healthy younger (21–32 years) and 14 healthy older individuals (62–84 years). The
l task involved the acoustically cued overt production of the vowel /a/ and the polysyllabic utterance /pataka/. In younger and
uals, overt speech production was associated with the activation of a widespread articulo-phonological network, including the
tor cortex, the supplementary motor area, the cingulate motor areas, and the posterior superior temporal cortex, similar in the
ka/ condition. An analysis of variance with the factors age and condition revealed a significant main effect of age. Irrespective
imental condition, significantly greater activation was found in the bilateral posterior superior temporal cortex, the posterior
ne, and the transverse temporal gyri in younger compared to older individuals. Significantly greater activation was found in the
dle temporal gyri, medial frontal gyri, middle frontal gyri, and inferior frontal gyri in older vs. younger individuals. The analysis
did not reveal a significant main effect of condition and no significant interaction of age and condition. These results suggest a
rganization of neural networks dedicated to the production of speech during healthy aging.
vier Inc. All rights reserved.
ealthy aging; Speech; Plasticity; Reorganization; Functional magnetic resonance imaging; Brain; Cortex
ction
modern advances in healthcare, elderly individ-
rapidly growing proportion of the population in
ed nations. Considerable efforts are under way to
ding author at: Department of Communication Sciences and
iversity of South Carolina, Columbia, SC 29208, USA.
77 1087.
dress: peter.soros@gmail.com (P. Sörös).
understand the mechanisms of aging better and to unravel
novel approaches to modify the aging process. Tradition-
ally, normal aging has been regarded as an inevitable decline
of cognitive, motor, and sensory functions, accompanied
by brain atrophy and neuronal loss (Reuter-Lorenz and
Lustig, 2005). Recently, converging evidence has suggested
that age-related changes in behavior, brain structure, and
brain function might be far more complex than previously
thought. With the advent of functional brain imaging, in par-
ticular positron emission tomography (PET) and functional
– see front matter © 2009 Elsevier Inc. All rights reserved.
.neurobiolaging.2009.08.015of overt speech pr
Peter Sörös a,∗, Arpita Bose b, Lisa
Simon J. Graham a,e,f,g, Dona
a Imaging Research, Sunnybrook Health Sciences Cnal neuroanatomy
ction
tman Sokoloff c,d,
Stuss d,g,h,i
oronto, Ontario, Canada

1506 P. Sörös et al. / Neurobiology of Aging 32 (2011) 1505–1513
magnetic resonance imaging (fMRI), it has become possi-
ble to compare brain activity associated with cognition (for
an early st
(e.g., Cerf
(e.g., Ward
Riecker et
In many o
pants has b
the neural c
younger ad
changes in
rimotor fun
performanc
Speakin
skills. Duri
executed a
100 differ
adults, aged
phonologic
et al., 200
isolated vo
eral cortica
motor area
mentary m
activation
putamen. T
connection
initiation a
tion, produ
activation i
phonologic
utterance /p
the bilatera
control of s
labic uttera
of the bila
phonologic
isolated vo
Many o
downs in s
(Searl et al
lables, and
al., 1987).
tion are like
as shown b
and increas
al., 2001), a
in particula
and James
the results
younger ad
pare the ne
healthy old
utterances
To study
lates of spe
dependent (BOLD) fMRI at 3 T was used. To minimize
artifactual fMRI signal changes due to motion-correlated
ments
999), c
s et al
RI e
itively
s an e
its det
; Sörö
he rap
tial m
BOL
iated
ave th
ethod
Partic
lood o
ired in
n) wit
group
an ave
nts w
re inc
g a te
ondit
ated v
diabet
us sy
ders,
dividu
ited w
r data
appro
th Scie
for pa
cipant
tudy w
he fM
r pap
Exper
rticip
le spe
d betw
(Sör
ds we
ka/. In
“say p
trans
ith acudy, see Grady et al., 1994), sensory processing
-Ducastel and Murphy, 2003), and motor tasks
and Frackowiak, 2003; Heuninckx et al., 2005;
al., 2006) between younger and older individuals.
f these studies, brain function of older partici-
een characterized by overactivation in parts of
ircuitry under investigation when compared with
ults. These changes may result from neuroplastic
the aging brain that compensate for loss of senso-
ction and contribute to maintaining of behavioral
e (Reuter-Lorenz and Cappell, 2008).
g is one of the most complex and important human
ng speaking, phonological plans are formed and
t 5–10 syllables per second, using approximately
ent muscles. In a previous study of younger
22–32 years, we identified a large-scale articulo-
network that mediates speech production (Sörös
6b). In younger adults, overt production of the
wel /a/ was associated with the activation in bilat-
l and subcortical motor centres. Activated cortical
s included the primary motor cortex, supple-
otor area, and cingulate motor area. Subcortical
was found in the thalamus, globus pallidus, and
hese areas, together with their extensive inter-
s, constitute the neural circuitry that controls
nd execution of articulatory movements. In addi-
ction of an isolated vowel was associated with the
n the bilateral superior temporal gyrus, reflecting
al processing. The production of the polysyllabic
ataka/ was associated with additional activation in
l cerebellar hemispheres, which are crucial for the
equential movements. The production of polysyl-
nces was also associated with stronger activation
teral temporal cortex, reflecting an increase in
al processing compared to the production of an
wel.
lder individuals experience difficulties and break-
peech production, such as reduced speaking rate
., 2002) and increased durations of segments, syl-
sentences compared to younger adults (Smith et
These age-related impairments in speech produc-
ly related to a decline in oro-facial motor control,
y decreased accuracy of movement amplitudes
ed temporal variability of movements (Ballard et
s well as impairment of phonological processing,
r the sequencing of phonological units (MacKay
, 2004). Based on these behavioral findings and
of previous functional brain imaging studies in
ults, the aim of the present study was to com-
ural correlates of overt speech production between
er and younger adults using simple non-lexical
with varying complexity.
potential age-related changes in the neural corre-
ech production, whole-brain, blood-oxygenation
move
al., 1
Sörö
cal fM
repet
leave
perm
2005
rate t
poten
of the
assoc
not h
2. M
2.1.
B
acqu
7 me
and a
with
ticipa
Befo
durin
ical c
untre
sion,
nervo
disor
as in
recru
untee
was
Heal
sent
parti
this s
and t
earlie
2.2.
Pa
simp
perio
ously
soun
/pata
and
were
tem wof the head and of the articulatory organs (Birn et
lustered image acquisition (Edmister et al., 1999;
., 2006b) was performed. Rather than the typi-
xperimental design in which images are acquired
at fixed time intervals, clustered acquisition
xtended silent interval for speech production and
ailed scanning of the brain 5 s later (Gracco et al.,
s et al., 2006b). Not only does the approach sepa-
id onset and offset of articulatory movements (and
otion artifacts) from the comparatively slow rise
D signal (Birn et al., 2004), but the acoustic noise
with imaging is also separated such that it does
e potential to distract behavioral performance.
s
ipants
xygenation level dependent (BOLD) fMRI was
a group of healthy younger volunteers (7 women,
h an average age of 25 years (range: 21–32 years)
of healthy elderly volunteers (7 women, 7 men)
rage age of 71 years (range: 62–84 years). All par-
ere right-handed and fluent speakers of English.
lusion into the study, volunteers were screened
lephone interview for the past and present med-
ions, medication and drug use. Individuals with
ascular risk factors (including arterial hyperten-
es, hypercholesterolemia), disorders of the central
stem (including stroke and dementia), psychiatric
and hearing impairment were excluded as well
als taking psychoactive drugs. Volunteers were
ith the help of the Rotman Research Institute vol-
base and by personal communication. The study
ved by Research Ethics Boards at Sunnybrook
nces Centre and Baycrest. Informed written con-
rticipation in the project was obtained from all
s according to the Declaration of Helsinki. Parts of
ere published as an abstract (Sörös et al., 2006a),
RI data of 9 young volunteers were reported in an
er (Sörös et al., 2006b).
imental tasks
ants were asked to repeat acoustically presented
ech sounds of varying complexity in the silent
een fMRI data acquisitions as described previ-
ös et al., 2006b) (Fig. 1). The required speech
re the vowel /a/ and the polysyllabic utterance
structions were “say ah” (for the /a/ condition),
ataka” (for the /pataka/ condition). Instructions
mitted through an fMRI-compatible audio sys-
oustically padded headphones to reduce acoustic