From the Department of Neurosurgery, China-Japan Friendship Hospital
(K.S., H.Z.); the Department of Rehabilitation, China-Japan Friendship
Hospital (Y.X.); Tsinghua University China-Japan Friendship Institute of
Medical Sciences, China-Japan Friendship Hospital (K.S., W.L., H.Z.); Group of
Detection & Analysis of Human Body Movement, Program of BME, Department of
Electrical Engineering, Tsinghua University (W.L.); and the Department of
Neurology, Beijing Union Hospital (S.L.), Beijing, China.
Correspondence and reprint requests to Kaoru Sakatani, MD, DMSc, PhD, Department of Neurosurgery, China-Japan Friendship Hospital, Yinghua East Rd, Hepingli, Beijing 100029, China. E-mail sakatani{at}public.east.cn.net
Methods—Twenty-nine participants performed speech tasks, such as
confrontational naming, to evaluate changes among poststroke nonfluent
(Broca's) aphasia patients (10 cases; mean±SEM, 56.9±2.2 years),
age-matched normal subjects (13 cases; 50.7±2.2 years) and poststroke
nonaphasic patients (6 cases; 52.5±3.9 years). The optodes of NIRS
were placed over the left prefrontal cortex. We analyzed the
NIRS parameter (oxyhemoglobin [oxy-Hb], deoxyhemoglobin
[deoxy-Hb], and total hemoglobin [total-Hb]) changes by qualitative
pattern analysis of the parameter changes and
quantitative analysis of the parameter values among
the groups.
Results—The most common NIRS parameter change was an
increase in oxy-Hb and total-Hb, with a slight decrease or no change in
deoxy-Hb in the normal subjects (5 of 13 cases, 38.5%) and the
nonaphasic cerebrovascular disease (CVD) patients (3 of 6 cases,
50.0%). In contrast, the most common pattern in the aphasic patients
was an increase of deoxy-Hb, with an increase of oxy-Hb and total-Hb (5
of 10 cases, 50%). However, this pattern was observed in only 3 of 13
cases (23.1%) in the normal subjects and 1 of 6 cases (16.7%) in the
nonaphasic CVD patients. The mean (±SEM) changes of deoxy-Hb of the
aphasic patients, the normal subjects, and the nonaphasic CVD patients
were 0.78±0.29, 0.06±0.16, and –0.18±0.22, respectively. The
statistical analysis demonstrated a significant effect for
deoxy-Hb (P<0.05), with the aphasic patients differing
significantly from the normal subjects and the nonaphasic CVD patients,
while the 2 nonaphasic groups did not differ from each other.
Conclusions—The present results demonstrate a multiplicity of
language-activated cerebral blood oxygenation
and hemodynamic changes in the left prefrontal cortex
in the nonaphasic and aphasic groups. The increase of deoxy-Hb with
increases of oxy-Hb and total-Hb in the aphasics during language tasks
suggests that the left prefrontal cortex of the aphasics utilizes more
oxygen than the nonaphasics during language tasks. Finally, functional
MRI, which images the activation area in the brain by detecting the
reduced concentration of deoxy-Hb during neuronal activation, should be
performed on the patients with cerebral dysfunction, giving special
consideration to the possible multiplicity of the rCBF and cerebral
oxygen metabolism responses to functional tasks.
PET activation studies on visual8 or
somatosensory functions9 10 demonstrated that
rCBF is greatly increased by focal increases in neuronal activity,
whereas the CMRO2 increases only slightly,
leading to a decrease in the extracted fraction of available
O2.8 9 10 Therefore, the rCBF
increase induced by neuronal activity decreases the concentration of
deoxy-Hb in the cerebral vessels. By detecting the reduced
concentration of the paramagnetic species, deoxy-Hb, during neuronal
activation, fMRI images the activation area in the
brain.11 12 However, it is not clear whether
language activity in the language-relevant areas of poststroke aphasics
is associated with similar changes of cerebral blood
oxygenation and hemodynamics induced by
relatively simple physiological stimulations such
as visual or somatosensory stimulation. This is particularly important
in the fMRI studies on cerebral function, since the activation area in
the brain may be overlooked by fMRI if the activation area is not
associated with the reduction of deoxy-Hb.
NIRS is an optical method to measure concentration changes of oxy-Hb
and deoxy-Hb in cerebral vessels by means of the characteristic
absorption spectra of hemoglobin in the near-infrared
range.13 14 Changes in total-Hb (sum of oxy-Hb
and deoxy-Hb) indicate blood volume changes and correlate with CBF
changes under conditions with constant hematocrit levels and perfusion
pressures.15 16 17 Thus, NIRS can measure both
blood oxygenation and hemodynamics in
the brain noninvasively. NIRS has been applied to the evaluation of
cerebral blood oxygenation and
hemodynamic changes during neuronal activities
including cognitive functions.18 19 20 21 22 23 24
Simultaneous measurements made with NIRS and PET
demonstrated that neuronal activation during mental tasks resulted in
changes in cerebral oxygenation and
hemodynamics measured by NIRS that were
consistent with PET results.20
In the present study, we used NIRS to investigate the difference in
the changes of cerebral blood oxygenation and
hemodynamics induced by language activities between
normal subjects, poststroke nonaphasics patients, and nonfluent aphasic
patients. We evaluated these changes in the left prefrontal cortex,
which plays an important role in language function in normal
subjects.1
Three speech tasks that are commonly difficult for aphasics to perform
were administered. The primary task confrontational naming is included
in most aphasia test batteries25 because of its
sensitivity to nonfluent (Broca's) aphasia. To further evaluate the
ability of NIRS to detect aphasia-related differences, 2 additional
speaking tasks were given that are not generally included in standard
aphasia tests. These were counting (from 1 to 50) and talking about
what happened yesterday. The evaluation included a rest period (5 to 10
minutes), followed by the cognitive performance. Participants
were seated and had their eyes open during the entire experiment.
Near-Infrared Spectroscopy
Data Analysis
In addition to the pattern analysis, we analyzed the
quantitative data of the NIRS parameters for the following
reasons. First, the path length factor is constant once the interoptode
distance exceeds 2.5 cm27; in view of the fact
that the interoptode distance was 3 or 4 cm in the present study,
intersubject variability related to path length factor was minimal.
Second, the reported NIRS studies, including our study on the
CO2 response of normal
adults,16 support the feasibility of analyzing
the absolute values of NIRS parameters as measured by
NIRO-500 when comparing groups of subjects.21 22 23 24
We analyzed the maximum value from the preactivation baseline
rather than the average value during task performance, since
the NIRS parameters tended to return toward the
preactivation baseline after reaching the maximum value or to fluctuate
during the task, possibly because of attention changes. One-way ANOVAs
were conducted to compare age-matched normal subjects, nonaphasic CVD
patients, and aphasic patients, and the Student-Newman-Keuls test was
performed to compare group means.
The patterns of the NIRS parameter changes observed in the
nonaphasic CVD patients were similar to those in the normal subjects
(Figure 1
Although aphasic patients had some difficulty performing the language
task, the task altered the oxygen metabolism and
hemodynamics in the left prefrontal cortex for all of
the aphasic patients except 1.
In contrast to the normal subjects and the nonaphasic CVD patients, the
most common pattern in the aphasic patients was an increase of deoxy-Hb
with an increase of oxy-Hb and total-Hb (pattern C). This pattern was
observed in 5 of 10 cases (50%). Figure 2B
The second most frequent pattern was an increase in oxy-Hb and total-Hb
with a slight decrease or no change in deoxy-Hb (pattern A). This
pattern was observed in 3 of 10 cases (30%) from the aphasic patient
group. One of the aphasic patients showed an increase in deoxy-Hb with
a decrease in oxy-Hb and total-Hb. Another aphasic patient (No. 10)
could perform the language task to some degree; however, no changes of
the NIRS parameters were observed during the task.
Table 2
Finally, we evaluated a variety of possible reasons for the NIRS
parameters of the aphasic patients. These include types of
CVD (ie, infarction or hemorrhage), the degree of aphasia, the
Aphasia Quotient from the WAB test, age, lesion location, and interval
between stroke and NIRS measurements. None of these factors illuminate
the findings.
In the normal subjects and nonaphasic CVD patients, increases of oxy-Hb
and total-Hb were the most commonly observed changes during the
language tasks. These changes are consistent with the reported
NIRS parameter changes induced by various neuronal
activations including mental tasks.18 19 20 21 22 23 24
Although increases of oxy-Hb and total-Hb can be induced by either an
increase in CBF or any impedance to cerebral venous
return,30 the changes induced by neuronal
activations reflect an increase in rCBF.18 19 20 21 22 23 24
The increase of rCBF induced by neuronal activity decreases the
concentration of deoxy-Hb in the cerebral vessels since the increase of
CMRO2 is much less than that of
rCBF.8 9 10
In the present study, however, the decrease of deoxy-Hb was not
observed consistently in the subjects who showed increases of
oxy-Hb and total-Hb. A lack of deoxy-Hb responses during neuronal
activity was reported in the NIRS study on cognitive
function.18 It was suggested that if an increase
of CMRO2 was sufficient to compensate for the
decrease of deoxy-Hb induced by increased rCBF during the task, a
decrease of deoxy-Hb might not be observed. Another possibility was the
relationship between the optodes and the activating foci. Kleinschmidt
et al22 found a similar lack of deoxy-Hb
responses during sensorimotor stimulation; slight mispositioning of the
optodes with respect to activation foci, which were detected by fMRI,
caused the lack of deoxy-Hb responses. Further studies are necessary to
clarify the physiological mechanism of the lack of
deoxy-Hb responses.
Although the aphasic patients had difficulty performing the task, 30%
of them showed alterations similar to those seen in most nonaphasic
patients, specifically increases of oxy-Hb and total-Hb with little or
no change in deoxy-Hb during the language task. These results indicate
that despite the poor language function the left prefrontal cortex
outside Broca's area was activated by the language task in
those aphasic patients, with preservation of coupling of rCBF and a
neuronal activity and a normal relationship between oxygen delivery and
oxygen utilization during neuronal activity.
One of the important findings in the present study is that 50% of
the aphasic patients showed an increase of deoxy-Hb during the language
task that can be associated with increases in oxy-Hb and total-Hb,
whereas this pattern was observed in only 23.1% and 16.7%,
respectively, of the normal subjects and the nonaphasic CVD patients.
In addition, the statistical analysis demonstrated a
significant effect for deoxy-Hb, with the aphasic patients differing
significantly from the normal subjects and the nonaphasic CVD patients.
In the aphasic patients with an increase of deoxy-Hb, the rCBF in the
left prefrontal cortex must be increased by the language task since
both oxy-Hb and total-Hb were increased by the task, indicating the
presence of coupling between rCBF and neuronal activity. However, the
mean increase of total-Hb in the aphasic patients was larger than that
seen in normal subjects and nonaphasic CVD patients, suggesting that a
larger increase of rCBF is induced by the language task in the aphasic
patients. On the other hand, the increase of deoxy-Hb indicates that
the oxygen consumption in the left prefrontal cortex of the aphasic
patients was increased more by neuronal activity than seen in the
nonaphasic patients. These observations suggest that the left
prefrontal cortex, in most of the aphasic patients, is more
activated during language processing, resulting in more oxygen
delivery and oxygen utilization compared with the nonaphasic patient
group. However, several of the normal subjects and the nonaphasic CVD
patients showed a similar increase of deoxy-Hb with an increase of
oxy-Hb and total-Hb during the language task. Therefore, the increase
of deoxy-Hb should not be interpreted as an abnormal cerebral
oxygenation metabolism during neuronal
activity. Finally, it should be emphasized that fMRI, which assesses
neuronal activation as a decrease of deoxy-Hb, may misinterpret such an
increase of deoxy-Hb with an increase of oxy-Hb and total-Hb as
deactivations.
Another interesting finding is that both oxy-Hb and total-Hb decreased
with a decrease or no change of deoxy-Hb in some of the normal adults
and the nonaphasic CVD patients during the language task. Similar
changes of NIRS parameters in the left frontal lobe were
reported in some normal adults during mental
tasks20,23; simultaneous measurements
with NIRS and PET demonstrated that the decreases in oxy-Hb and
total-Hb were associated with a decrease in rCBF at the NIRS
recording region.20 The
physiological mechanisms and roles of the rCBF
decrease during neuronal activity are not yet clear; however, several
possible mechanisms should be considered. First, the baseline CBF
before tasks may affect the rCBF response induced by neuronal activity.
Second, neuronal activities near the NIRS recording area may
steal the blood flow at the NIRS measurement area, resulting in a
decreased rCBF. Finally, the synaptic activity in the measurement area
might be depressed by the language task; PET studies have demonstrated
that regional depressions of synaptic activity decreased rCBF and
CMRO2.10 Indeed, in most cases
with decreases of oxy-Hb and total-Hb, deoxy-Hb decreased or did not
change during the task; however, 1 normal subject and 1 aphasic patient
showed an increase of deoxy-Hb associated with decreases of oxy-Hb and
total-Hb, suggesting that relative ischemia was induced by the
neuronal activation. Further studies are necessary to clarify the
physiological mechanisms and roles of the rCBF
decrease during neuronal activity.
In summary, the present results demonstrated that the
language-activated cerebral blood oxygenation
and hemodynamic changes of the left prefrontal cortex
showed several response patterns in the nonaphasic and aphasic
patients. The multiplicity of the language-activated responses
differs from the responses induced by visual8 21
or somatosensory stimulation9,10,22; visual or
somatosensory stimulation evokes predictable and consistent
neuronal activities in corresponding cortical areas associated with
relatively consistent changes of rCBF and cerebral oxygen
metabolism. This difference suggests that neuronal
activities such as participation of inhibitory and
facilitatory synaptic activities in the language-relevant area varies
in subjects during language processing, resulted in the multiplicity of
the language-activated responses of cerebral blood
oxygenation and hemodynamics. In
addition, the difference in the response patterns between the aphasic
and nonaphasic groups suggests that neuronal activities induce
different activity-dependent changes of rCBF and cerebral oxygen
metabolism compared with those during normal function.
Finally, it should be emphasized that fMRI should be performed, giving
special considerations to the possible multiplicity of the rCBF and
cerebral oxygen metabolism responses to cognitive
tasks.
Received December 16, 1997;
revision received March 5, 1998;
accepted March 26, 1998.
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Original Contributions
Language-Activated Cerebral Blood Oxygenation and Hemodynamic Changes of the Left Prefrontal Cortex in Poststroke Aphasic Patients
A Near-Infrared Spectroscopy Study
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Background and Purpose—In normal
subjects, regional cerebral blood flow (rCBF) is greatly increased by
neuronal activity, whereas the cerebral metabolic rate for
O2 is increased only slightly. However, it is not clear
what kinds of cerebral blood oxygenation and
hemodynamic changes can be induced by language
activities in language-relevant areas of poststroke aphasics. In the
present study, we investigated the difference in the changes of
cerebral blood oxygenation and
hemodynamics in the left prefrontal cortex induced by
language activities between normal subjects, poststroke nonaphasic
patients, and nonfluent aphasic patients using near-infrared
spectroscopy (NIRS).
Key Words: aphasia • cerebral blood flow • cognition • language • spectroscopy, near-infrared
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Aphasia is a disorder
of language functions and 1 of the major symptoms caused by CVD. To
address the processing mechanism of language functions, PET or fMRI has
been performed on normal subjects to image activation areas during
language tasks.1 2 3 4 5 These studies have
demonstrated that several cortical areas outside the classic language
centers such as Broca's area and Wernicke's area are also
activated by language processing, associated with an activation
of the language centers. In addition, recent PET activation studies on
aphasics demonstrated that cortical areas, which are not
activated in normal subjects, are functioning in aphasics
during language tasks.6 7
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Subjects
Twenty-nine participants performed speech tasks to evaluate
changes among poststroke aphasic patients (10 cases; age [mean±SEM],
56.9±2.2 years), age-matched normal subjects (13 cases; age, 50.7±2.2
years), and poststroke nonaphasic patients (6 cases; age, 52.5±3.9
years). The groups did not differ in age (P=0.20). The
poststroke aphasia was caused by infarction in 4 cases,
hemorrhage in 5, and mixed (infarction and hemorrhage)
in 1. CT or MRI was taken of each poststroke patient to obtain
morphological information before the NIRS study. The clinical profiles
of the patients are shown in Table 1
. The
subjects were all strongly right-handed, as confirmed by the Edinburgh
Handedness Inventory. Each poststroke aphasic patient underwent the WAB
before the NIRS study. The nonfluent (Broca's) aphasics were of
varying severity, ranging from mild impairment to severe global
aphasia. Four of the poststroke nonaphasic patients had suffered an
infarction, and 2 had suffered a hemorrhage. The NIRS
measurement area (see next section) in the left frontal lobe was
morphologically normal in all the subjects. Informed consent to
participate in the study was obtained from each subject.
View this table:
[in a new window]
Table 1. Clinical Profiles of the Aphasic Patients and
Nonaphasic CVD Patients
We measured cerebral blood oxygenation and
hemodynamics with NIRO-500 (Hamamatsu Photonics K.K.),
which has been used in previous NIRS activation
studies.21 22 23 24 Near-infrared light from laser
diodes (wavelengths, 775, 825, 850, and 904 nm) was directed at the
head through a fiberoptic bundle ("optode"), and reflected light
was collected in the receiving fiberoptic bundle and transmitted to a
photomultiplier tube. With the use of an algorithm developed by Cope et
al,26 absolute concentration changes of oxy-Hb,
deoxy-Hb, and total-Hb (equal to oxy-Hb plus deoxy-Hb) were
continuously analyzed by means of a computer interfaced with
the apparatus. NIRS data are expressed in arbitrary units.
If the differential path length factor of the adult head is assumed to
be 5.9, which was determined by time-of-flight measurement of a
picosecond-length optical pulse through the tissues, 1 arbitrary unit
equals 1 µmol/L.27 The optodes were placed
at a distance of 3 or 4 cm on the left forehead; the center of the 2
optodes was identical to the Fp2 position of the international EEG
10–20 system. In 5 subjects, the location of the optodes was
identified by MRI with use of vitamin E capsules. MRI showed that the
optodes were placed over the left prefrontal cortex. With an optode
distance of 3.5 cm, the maximum depth of the region is 4
cm,28 and thus the NIRS measurement area in the
present study corresponded to the left prefrontal cortex.
In many NIRS studies on neuronal activation using NIRO-500, the
values of NIRS parameters were compared between different
individuals.21 22 23 24 However, the values of NIRS
parameters can be affected by individual differences in
anatomic structures through which light passes, including skull
thickness, skin absorption, and scattering properties of underlying
brain structures such as subarachnoid space. Therefore, some of
the NIRS activation studies analyzed only qualitative changes
of NIRS parameters, such as pattern changes of NIRS
parameters, with an NIRS instrument that does not indicate
absolute values of the parameter
changes.18 19 20 In the present study, we
mainly analyzed the changes of NIRS parameters
(oxy-Hb, deoxy-Hb, and total-Hb) induced by the language tasks by
qualitative pattern analysis of the parameter
change: we classified several common patterns according to the changes
of the NIRS parameters during the language tasks.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
In the normal subjects, the language task significantly altered
oxygen metabolism and hemodynamics in the
left prefrontal cortex. The changes measured by NIRS were classified
into 4 patterns. Figure 1 summarizes
these patterns of NIRS parameter changes induced by the
language task. Figure 2A shows the most
common pattern of the NIRS parameter changes, an increase
in oxy-Hb and total-Hb with a slight decrease or no change in deoxy-Hb
(pattern A as seen in Figure 1). This pattern was observed in 5 of 13
cases (38.5%). The second most frequent pattern (pattern B) was a
decrease in oxy-Hb and total-Hb with no change or slight decrease in
deoxy-Hb (4 of 13 cases; 30.8%). The third most common pattern
(pattern C) was that not only oxy-Hb and total-Hb but also deoxy-Hb
showed a tendency to increase (3 of 13 cases; 23.1%). Finally, 1 of 13
cases showed a decrease of oxy-Hb and total-Hb with a slight increase
in deoxy-Hb (pattern D).
View larger version (22K):
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Figure 1. Patterns of NIRS parameter
changes induced by naming task in normal age-matched control subjects,
nonaphasic CVD patients, and aphasic patients. "A through E" on the
abscissa represent the patterns of NIRS parameter
change during the task. "+" and "–" below A through E indicate
an increase and a decrease, respectively, of the NIRS
parameters designated in the left during the task. The
ordinate indicates percentage of the patterns in normal age-matched
control subjects ( 
), nonaphasic CVD patients (
), and aphasic
patients (
).
View larger version (17K):
[in a new window]
Figure 2. A, Typical example of the most common pattern of
NIRS parameter change in the normal subjects during naming
task. B, Typical example of the most frequent pattern of NIRS
parameter change in the aphasic patients (No. 5; see Table 1 
) during the task. The ordinates indicate concentration changes of
oxy-Hb, deoxy-Hb, and total-Hb in arbitrary units (a.u.). Horizontal
thick bars indicate the period of the task. Note the difference in
changes of deoxy-Hb between A and B during the task.). The most common pattern of NIRS parameter in
the nonaphasic CVD patients was the same as that in the normal
subjects; 3 of 6 cases (50%) showed an increase in oxy-Hb and
total-Hb, with no change or a slight decrease in deoxy-Hb (pattern A).
A decrease of oxy-Hb, total-Hb, and deoxy-Hb (pattern B) was observed
in 2 of 6 cases (33.3%). An increase of deoxy-Hb associated with an
increase in oxy-Hb and total-Hb (pattern C) was observed in only 1 of 6
cases (16.7%). shows a typical example of
the NIRS parameter change during the language task. Within
10 seconds from the start of the task, first oxy-Hb began to increase,
and then deoxy-Hb gradually increased. These increases in oxy-Hb and
deoxy-Hb led to an increase of total-Hb. summarizes the mean changes of
oxy-Hb, deoxy-Hb, and total-Hb in the aphasic patients, the normal
subjects, and the nonaphasic CVD patients. Results of a 1-way ANOVA
comparing the performance of the 3 groups in the naming task
demonstrated a significant effect for deoxy-Hb
[F(2,27)=4.47, P<0.05[, with
aphasic patients differing significantly from normal subjects and
nonaphasic CVD patients, while the 2 nonaphasic groups did not differ
from each other. In contrast, there were no significant differences in
oxy-Hb or total-Hb among the groups (P>0.05).
Generalizability about the results was supported by the statistical
analyses for the talking and counting tasks. As evident in
Table 2, the results of the 1-way ANOVAs support the naming findings in
that significance was attained for deoxy-Hb (P<0.05) but
not for oxy-Hb or total-Hb. Outcomes of the naming task were replicated
in that aphasia patients differed significantly from the 2 nonaphasic
groups only on deoxy-Hb and that for deoxy-Hb the normal subjects and
CVD patients without aphasia did not differ.
View this table:
[in a new window]
Table 2. Changes of Oxy-Hb, Deoxy-Hb, and Total-Hb in
Age-Matched Control Subject, Nonaphasic CVD Patients and Aphasic
Patients
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
The left prefrontal cortex is related to various higher brain
functions including language processing.1 2 3 4 29
Recent fMRI studies have demonstrated that the left prefrontal cortex
outside the classic "Broca's area" is also activated by
language processing that is associated with activation of Broca's
area.1 In the present study in which NIRS was
used, we demonstrated that the language task caused changes in the
oxygen metabolism and hemodynamics of the
left prefrontal cortex. In addition, these changes of the oxygen
metabolism and hemodynamics measured by
NIRS showed several different patterns in subjects.
Selected Abbreviations and Acronyms
CMRO2
=
cerebral metabolic rate for O2
CVD
=
cerebrovascular disease
deoxy-Hb
=
deoxyhemoglobin
fMRI
=
functional MRI
NIRS
=
near-infrared spectroscopy
oxy-Hb
=
oxyhemoglobin
PET
=
positron emission tomography
rCBF
=
regional cerebral blood flow
total-Hb
=
total hemoglobin
WAB
=
Western Aphasia Battery
Acknowledgments
This research was partially funded by Japan International
Cooperation Agency (JICA).
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
1.
Binder JR, Frost JA, Hammeke TA, Cox RW, Rao SM,
Prieto T. Human brain language areas identified by functional magnetic
resonance imaging. J Neurosci. 1997;17:353–362.
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