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Disorders of affective and linguistic prosody in children after early unilateral brain damage.

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Disorders of Mective and Lmpstic Prosody
in Children atter Early Unilateral
Brain Damage
Doris A. Trauner, MD,* Angela Ballantyne, MS,* Susan Friedland, MD,* and Christopher Chase, PhDf
Prosody is that quality of speech that imparts meaning by changes in intonation, pitch, and stress. The right hemisphere
(RH) appears to be dominant for affective prosody in adults, while the left hemisphere (LH) mediates the more linguistic
aspects of nonverbal communication. Few similar studies have been reported of individuals who suffered early unilateral
brain damage, when brain reorganization or plasticity might be expected to play a role in ameliorating the adverse
effects of focal brain damage. In this study, comprehension and expression of affective and linguistic prosody were
tested in subjects with documented unilateral brain damage of pre- or perinatal onset and in matched controls. Both
RH- and LH-lesion groups demonstrated difficulty on tasks involving expretsion of affective prosody, and on tests of
linguistic prosody, compared with controls. Only the RH-lesion group was impaired on an affective comprehension
task. The results indicate that even after very early unilateral brain damage, prosodic deficits may be present. However,
only for affective comprehension does the side of the lesion appear to determine such deficits. The findings suggest that
during brain development there is not clear brain lateralization for prosody and there may be bilateral representation
for these skills during early development. There may be limitations to the ability of the developing brain to reorganize
after early injury.
Trauner DA, Ballantyne A, Friedland S, Chase C. Disorders of affective and linguistic prosody in children
after early unilateral brain damage. Ann Neurol 1996;39:361-367
Interest in the neurologic basis of social competence
has increased in the last two decades. Recent research
has focused on the neurology of nonverbal communication, or prosody. The term prosody was coined in
1947 by Monrad-Krohn [l] to mean “melody of
speech,” and is defined as that faculty of speech that
conveys states of meaning by variations in stress and
pitch, regardless of the words used or the grammatical
constructions. Emotive or affective prosody imparts
emotional nuances to speech, eg, anger, fear, happiness,
and so on, by the use of intonation, pitch, and emphasis. Linguistic prosody is that quality of speech that
imparts meaning through syllable, word, or sentence
level stress and intonation; eg, question versus declarative statement, lexical stress (“bluebird” vs “blue
bird”), and contrastive stress (“Mary reads the book”
vs “Mary reads the book”).
Disorders of nonverbal communication have been
observed for many years; but more recently these disorders have been studied systematically in adults with
strokes. Ross [2] has labeled the disorders of nonverbal
language the “aprosodias.” Most of the studies in
adults with strokes suggest that the right hemisphere
(RH) is dominant for the processing of nonverbal, and
particularly the emotional aspects of communication
[2-151. There is some controversy with regard to the
role of the RH in linguistic prosody, however. Whereas
some investigators believe that the RH is dominant for
all prosodic information [6, 111, others [16, 171 suggest that the left hemisphere (LH) may be responsible
for the processing of nonverbal linguistic cues, while
the RH controls only the emotional aspects of prosody.
Thus, the neuroanatomic substrates for processing of
emotional and linguistic cues are not clearly defined in
adults with late acquired lesions.
Even less is known about children who suffered early
focal brain damage. Few studies have investigated prosodic skills in children. Normal children can identify
emotional meanings of vocal expressions from an early
age [IS]. The majority of study populations have consisted of children with clinical evidence of RH dysfunction (eg, left-sided abnormalities on neurologic exami-
From the ‘Departments of Neurosciences and Pediatrics, University
of California, San Diego School of Medicine, La Jolla, CA; and
tSchool of Cognitive Science and Cultural Studies, Hampshire College, Amherst, MA.
Received Apr 19, 1995, and in revised form Oct 30. Accepted for
publication Nov 6, 1995.
Address correspondence to Dr Trauner, Department of Neurosciences, UCSD School of Medicine, 9500 Gilman Drive, La Jolla,
CA 92033-0935.
Copyright 0 1996 by the American Neurological Association
361
nation) [ 191, children with learning disabilities [2O251 or developmental language delay [26, 271, or children with focal epilepsy [28, 291. Denckla [21] observed that children with left-sided neurologic findings
had problems with social failure. These children had
difficulty attending to nonverbal cues and providing
such cues to others. Weintraub and Mesulam [22] described 14 patients with learning disabilities and difficulties with interpersonal skills who had evidence of
RH abnormalities on neurologic examination. Based
on clinical evaluation, these individuals were found to
lack “the gestures and prosody that normally accompany and accentuate speech” [22]. The authors suggested that early damage to the RH may lead to
chronic emotional difficulties and disturbances in interpersonal skills. Tranel and colleagues [24] reported on
a similar group of individuals, all of whom showed
clinical evidence of RH dysfunction but with normal
brain computed tomographic (CT) scans. In another
study of 15 children with behavioral disturbances and
learning disabilities, Voeller [ 191 reported neurologic
findings consistent with RH dysfunction. Some of her
subjects were unable to interpret social cues, while others were unable to express their feelings but appeared
to have intact comprehension of emotions in others.
CT scan results were varied in her group of patients;
some were reportedly normal, others had ‘‘atypical”
right/left asymmetries, and a few were reported to have
RH “lesions.”
Many of these previous studies began with groups
of children and adults who had social difficulties 2
learning disabilities, and found suggestions of RH dysfunction. In the present study, we began with a group
of children who had known unilateral brain lesions and
devised experimental measures to evaluate their prosodic skills. The goal of the study was to determine if
normal development of linguistic and affective prosody
would take place in the face of very early (pre- or perinatal) unilateral brain damage.
Materials and Methods
Subject Selection
Sixty-two individuals participated in the 5tudy. Of these, 31
subjects had a single, unilateral focal brain lesion, each documented by a neuroimaging procedure. Fifteen subjects had
LH lesions, and 16 had RH lesions (Table 1). All lesions
were the result of ischemic or hemorrhaglc infarcts; no children with chronic or progressive lesions, such as tumors or
arteriovenous malformations, were included in the study.
Time of onset of the lesion in each case was determined to
be pre- or perinatal based on review of niedical records and
detailed medical history. Potential subjects were excluded
from the study if there was evidence of a medical condition
that might have produced global or multitbcal brain damage,
such as closed head trauma, anoxia, or bacterial meningitis.
Lesion severity was assessed from the neuroimaging study
362
Annals of Neurology
Vol 39
No 3 March 1996
using a five-point rating scale modified from Vargha-Khadem
and associates [30]. The smallest lesion was rated as 1 ,signifying
ventricular dilatation or atrophy seen on fewer than three cuts
on CT or magnetic resonance imaging (MRI); 2, ifventricular
dilatation or atrophy was seen on three or more cuts; 3, if focal
porencephaly was present involving one lobe only, and seen on
less than three cuts; 4, if focal porencephaly involved one lobe
only but was seen on three or more cuts; and 5, if porencephaly
involved multiple lobes.
Thirty-one control subjects also participated in the study.
Each control was individually matched by age (t1 year),
sex, and socioeconomic status (SES) [31] to a subject in the
focal lesion group. All controls had normal developmental
histories.
Age range of the LII group was 5.25 to 15.58 years (mean
-C SD; 8.5 -C 3.1 years); for LH controls, 6.17 to 16.08
years (8.8 +- 2.8 years); for the RH group, 5.5 to 20.33
years (1 1.2 -C 5.1 years); and for RH controls, 6.17 to 20.92
years (11.2 -C 5.0 years). There were 22 males and 9 females
in both the focal lesion and the control groups.
Studies were conducted in accordance with procedures
specified by the Institutional Review Board at UCSD. Informed consent was obtained from all subjects and/or guardians prior to entry into the study.
Procedures
Tests of comprehension and expression of affective and linguistic intent (prosody) were administered to every subject
enrolled in the study. Some of the tests were adapted from
the work of previous investigators [3, 4,6, 11, 261. In every
case the tests were administered in a randomized fashion.
Tests o f Affective (Emotive) Prosody
Two tasks were
utilized to assess the subject’s ability to comprehend affective
intent in voice. In the first comprehension task, each subject
listened to a tape prerecorded by a professional actress that
consisted of 15 short phrases of neutral content (eg, “There
he is,” “It’s over”). Each phrase was said in an angry, happy,
or sad tone of voice. After listening to each phrase, the child
was instructed to identify the emotion as happy, sad, or
angry. A practice session using two examples was given prior
to beginning the test to ensure that the subjects understood
the directions.
For the second task, each subject listened to a tape that
was prerecorded by a professional actress. The tape contained
10 pairs of short, neutral-content phrases. Each pair consisted of the same phrase repeated twice, using either the
same emotional intonation both times, or using different
emotional intonations in each phrase of rhe pair. T h e subject
merely had to respond to each pair by telling rhe examiner
whether the two phrases sounded the same or different.
COMPREHENSION OF AFFECTIVE INTENT.
EXPRESSION OF AFFECTWE I N T E N T . Two kinds of tasks
were used to test the abiliry of the subject to express affective
information appropriately. One involved imitation and the
other involved spontaneous elicited affect.
In the imitation task, each subject listened to a tape prerecorded by a professional actress that contained 15 short
Table 1. Location of Lesions and Associated Neurologic Findings in Children with Focal Brain Lesions
Sex
Site of Lesion
Thalamic
andlor
Basal
Ganglia
Damage
11
M
M
F
M
M
M
M
F
M
F
F
Rt.
Rt.
Rt.
Rt.
Rt.
Rt.
Rt.
Rt.
Rt.
Rt.
Rt.
Y
N
Y
Y
Y
Y
Y
N
N
N
Y
12
13
F
M
Rt. P > T
Rt. T
14
15
M
M
16
17
Severity
of Lesion
5
Hemiparesis
3
3
5
Moderate
No
Mild
No
Moderate
Mild
No
Mild
No
No
Moderate
N
N
5
3
No
No
Rt. P-T
Rt. F-T-P-0
Y
Y
5
5
F
Rt. P
N
4
No
Moderate/
severe
No
18
M
M
Lt. T
Lt. F-P-T
N
Y
4
5
19
M
Lt. F
Y
2
20
21
22
F
M
M
Lt. T-P
Lt. F-T-P
Lt. P-T-0
Y
Y
Y
5
5
23
24
25
M
M
M
Lt. T - P - 0 > F
Lt. F-T-P-0
Lt. T-P
Y
Y
N
5
26
27
28
29
30
31
M
M
M
F
F
M
Lt.
Lt.
Lt.
Lt.
Lt.
Lt.
N
N
N
N
N
N
1
2
3
4
5
6
7
8
9
10
F
=
F-T-P
P
T
F
F-T-P
F-T-P
F-T-P-0
F-T
F
P
F-T-P > 0
P-T-F
P
F
P-0
T
P-0
frontal; T = temporal; P =
parietal; 0
2
1
4
5
5
5
5
5
5
5
5
3
3
5
1
3
Mild
Moderate1
severe
No
Moderate
Moderate
Moderate
Moderate
No
Mild1
moderate
No
No
No
No
Mild
No
Other Neurologic
Findings
Presumed Etiology
None
None
None
None
Seizures
Seizures
None
Seizures
None
None
Seizures, visual
field cut
None
Hydrocephalus,
V-P shunt
None
Seizures
Ischemic infarct at birth
Ischemic infarct at birth
Parenchymal hemorrhage at birth
Parenchymal hemorrhage at birth
Prenatal infarct
Ischemic infarct at birth
Ischemia at birth
Prenatal infarct
Lacunar infarct ?prenatal
?Prenatal infarct
Intrauterine stroke
Seizures, hydrocephalus
Visual field cut
None
Prenatal porencephaly
Right hyperreflexia
Seizures
Seizures
Dense visual field
cut
Seizures
Neonatal seizures
Cortical sensory
deficit, visual
field cut
Neonatal seizures
None
None
None
No
None
Parenchymal hemorrhage at birth
= occipital; Lt. = left; Rt. = righr;
Y
=
Parenchymal hemorrhage at birth
Parenchymal hemorrhage at birth
Ischemia at birth
Prenatal porencephaly
Ischemic infarct at birth
Ischemic infarct at birth
Intrauterine infarct
Parenchymal hemorrhage at birth
Ischemic infarct at birth
Prenatal infarct
Ischemic infarct at birth
Ischemic infarct at birth
Prenatal porencephaly
?Prenatal gliosis
?Prenatal gliosis
?Prenatal infarct
?Prenatal ischemia
Ischemic infarct at birth
yes; N = no.
Trauner et al: Prosody after Perinatal Stroke 363
phrases similar to those used for the comprehension task.
The children were then asked to repeat the phrases exactly
as they heard them, using the same intonation as they heard
on the tape. Their responses were audiotaped for later analysis. As before, a practice session consisting of rwo examples
was used to ensure that the subjects understood the test.
T o test spontaneous elicited affective skills, a task was devised in which subjects were asked to complete a series of
10 short stories that were designed to elicit an emotional
response. (Example: “The rat stole the mouse’s cheese. That
made the mouse angry. The mouse said to the rat . . .”
Expected response: “Give me back my cheese!” in an angry
tone of voice.) The subjects were instructed to “act out” the
responses with their voices. Responses were audiotaped for
later analysis.
Audiotapes were analyzed by three independent raters who
were naive to the purpose of the experiments and who had
no knowledge of the subjects involved in the study. They
reviewed each segment of the tape and were asked to decide
if the subject sounded happy, sad, or angry, or if they were
unable to tell. The subject was given credit for a correct
response if at least two of the three raters ‘correctly identified
the emotion intended.
were designed to elicit a specific type of response. Emphasis
on either the subject or object was elicited by asking the
subject to respond to the examiner’s question after each story
was read (eg, “Mary liked the play. Sam hated the movie.
Who liked the play, Mary or Sam?” Expected response:
‘‘Maryliked the play.”).
As with the tests of affective prosody, audiotapes of the linguistic prosody experiments were analyzed by three independent raters who were naive to the purpose of the experiments
andwho had no knowledgeofthesubjects involved in thestudy.
Theyreviewedeachsegment oftherapeandwereasked todecide
if the individual was making a statement or a question, or if
subject or object was emphasized, depending on the experiment, or if they were unable to tell. The child was given credit
for a correct response if at least two of the three raters correctly
identified the intended emphasis.
Since adequate language comprehension is a prerequisite
for successful performance on all of the prosody tasks, the
Token Test [32], a test of language comprehension, was administered to all subjects.
Statistical analyses of all data were performed using analysis of variance and paired t tests.
Results
Tests of Linguistic Prosody
COMPREHENSION OF ImcuIsric
Tests of Afective Prosody
Two comprehension tasks were utilized, and each was analogous to
the tasks used to test affective prosodic skills. In the first test
of comprehension of linguistic prosody, the subject listened
to a prerecorded tape consisting of 10 sentences, each of
which was said as either a question or a sixement using the
appropriate intonation. The senrenccs were content-neutral
so that the correct response could not be ascertained from
the words alone. After listening to each sentence, the subject
was asked to respond with “question” or “statement” as a
response. As before, rwo practice trails were given prior to
beginning the actual test tape, to ensure that the subject
understood the instructions and could perform the task.
The second task consisted of 15 pairs of sentences prerecorded by a professional actress. Each pair consisted of either
identically emphasized sentences, or of sentences with contrasting emphasis (eg, question vs statement, subject vs object
emphasized). After subjects listened to the: pair of sentences,
they were asked to tell the examiner whether the two sentences sounded the same or different.
PROSODY.
’Two kinds of tasks
EXPRESSION OF LINGUISTIC PROSOI)Y.
were used to test theability ofthe subject to express information
in a linguistically appropriate manner. One involved imitation
and the other involved spontaneous elicited linguistic prosody.
In the imitation task, each subject listened to a tape prerecorded
by a professional actress that contained 20 short sentences similar to those used for the linguistic cornprehension task. Listeners
were then asked to repeat the phrase exactly as they heard it,
usingthe same intonation they heard on the tape. The responses
were audiotaped for later analysis. As before, a practice session
consisting of two examples was used to emure that the individual understood the test.
T o test spontaneous elicited linguistic prosody, the subjects were asked to complete a series of 10 short stories that
364 Annals of Neurology
Vol 39
No 3 March 1996
Subjects with RH lesions scored significantly lower
than their matched controls on tests of comprehension
a n d expression of affective prosody (Table 2). T h e only
task on which the RH group performed at a level similar to controls was the identification of the appropriate
emotion after listening t o tape-recorded phrases (mean
5 SD; 11.7 5 2.1 correct responses for the RH group
vs 12.3 5 1.7 for controls). However, o n a discrimination task involving recognition of the vocal emotion as
“same” o r “different,” the RH group did not do as
: 1.4 vs 9.6 +- 0.5;
well as their control group (8.4 I
p = 0.004). On expressive measures of affective prosody, the RH group performed more poorly than their
controls on both imitation (9.8
2.8 vs 11.4 2 1.8;
p = 0.037) a n d spontaneous elicited (6.0 rt 2.1 vs 7.9
1.8; p = 0.006) tasks.
Subjects with LH lesions did n o t differ significantly
from their matched control group on tests of affective
comprehension (see Table 2). However, affective expression was impaired in the LH group compared with
controls. On these tasks, the performance of the LH
group was significantly poorer than that of the control
group (imitation task, 8.4 i 3.4 for LH vs 10.6 rt
1.7 for controls, p = 0.026; spontaneous elicited task,
5.3 I
:0.7 for the LH group vs 6.9 rt 2.1 for controls;
p = 0.020).
*
*
Tests of Linguistic Prosody
Individuals with RH lesions exhibited difficultywith tests
involving comprehension of linguistic cues (question vs
statement, 7.2 5 2.3 for the RH group vs 8.8 t 1.5 for
contro1s;p = 0.026; discrimination, 11.8 5 2.5 vs 13.8
Table 2. Pevformance of Left Hemisphere (LH) and Right Hemisphere (RH) Groups and Matched Control Groups on Tasks of
Affective and Linguistic Prosody
LH
Test
Mean
SD Mean
SD
RH Control
RH
LH Control
p
p
Mean
NS
NS
0.026
0.020
11.7
8.4
9.8
6.0
f 2.1
2 1.4
-C 2.8
t 2.1
12.3 -f 1.7
9.6 +- 0.5
11.4 i 1.8
7.9 2 1.8
NS
0.004
0.033
0.006
0.012
0.004
<0.001
NS
7.2
11.8
13.5
4.5
i 2.3
f 2.5
5 4.2
-C 1.6
8.8
13.8
18.1
5.5
0.026
0.013
0.014
NS
SD Mean
SD
~
1A.
2A.
3A.
4A.
1L.
2L.
3L.
4L.
Identification of emotions in voice
Discrimination of emotions in voice
Imitation of emotions in voice
Spontaneous elicitation of emotional tones
in voice
Identification of linguistic stress
Discrimination of linguistic stress
Imitation of linguistic stress
Spontaneous elicitation of linguistic stress
10.7 -C 2.5
8.8 -C 1.2
8.4 -C 3.4
5.3 -C 0.7
12.2
9.6
10.6
6.9
6.0 5 1.9
11.0 5 3.2
12.2 -C 4.8
5.2 -C 2.4
14.0
19.0
t 1.7, p = 0.013), and also with imitation of diflkrent
types of linguistic stress (subject vs object or question vs
statement; 13.5 t 4.2 vs 18.1 t 3.6; p = 0.014) (see
Table 2). Their performance on spontaneous production
of linguistic cues did not differ significantly from that of
controls (4.5 t 1.6 vs 5.5 2 2.7).
The LH group performed significantly more poorly
than their control group on both comprehension and
imitation of linguistic prosody as well (see Table 2).
O n comprehension measures, they exhibited difficulty
with both identification (6.0 t 1.9 vs 8.5 +- 2.0; p =
0.012) and discrimination (11.0 k 3.2 vs 14.0 t 1.6;
p = 0.004) tasks. The performance of the subjects with
LH lesions was most deficient, compared with controls,
on the imitation of linguistic stress (12.2 t 4.8 vs 19.0
t 1.4; p < 0.001). There were no significant differences in performance between LH and control groups
on spontaneous elicitation of linguistic cues (5.2 t 2.4
vs 6.3 t 2.4).
Test o f Language Comprehension
Both the RH and LH groups scored lower than did their
matched control groups on the Token Test [32], a standardized measure of language comprehension, although
there was a wide variation in test scores within groups.
Established norms for this test utilize 500 as the average
score, with a standard deviation o f t 5. The performance
of the LH group was 492.5 t 10.4 versus 501.5 t 4.3
for LH controls, p = 0.018. Results for the RH group
were492.1 i 16.9versus 500.5 i 5.6 for the RH control
group (no significant difference).
Discussion
The results of this study indicate that children and
young adults who had very-early-onset (pre- or perinatal) unilateral brain damage exhibit deficits in the comprehension and expression of prosody, compared with
age-, sex-, and SES-matched controls. Specifically, indi-
-C 1.7
-C 0.5
-C
1.7
-C 2.1
8.5 i 2.0
-C 1.6
-C 1.4
6.3 -C 2.4
1.5
1.7
t 3.6
-C 2.7
?
-C
viduals with documented lesions of the RH demonstrate difficulties in the comprehension and expression
of both affective and linguistic cues. Subjects with lesions of the LH demonstrate difficulty primarily with
expression of affective prosody, and with receptive and
expressive components of linguistic prosody.
There are some differences between our findings and
the results of studies in adults after later-acquired focal
brain lesions (strokes). In a study by Heilman and coworkers [9], adults with RH lesions had poorer comprehension of emotive prosody than either patients
with LH lesions or controls. Both LH and RH groups
performed equally poorly on tests of linguistic prosody
when compared with controls. These findings are quite
similar to those of the present study. Other studies
[2- 171, however, have also documented a right brain
dominance for receptive and expressive components of
emotive prosody but mixed results for localization of
linguistic prosody. Our LH-lesion subjects demonstrated impairments in expressive affect, a finding that
differs distinctly from results in adults.
Based on the current findings, it is possible that children with early focal brain damage might be more
likely to have problems with social interactions than
normal children. As in adults, deficits in affective nonverbal communication skills may impair a child’s ability to interpret the emotional states of others, to be
sensitive to nuances in social situations, and to behave
in a socially appropriate manner. In addition, children
with linguistic dysprosodia may experience social difficulties, not necessarily because of deficiencies in affective comprehension and expression, but because
their difficulty communicating and interpreting nonverbal linguistic cues may cause their speech to appear
“strange” to others. This could also lead to social difficulties, especially rejection by peers. There have been
some clinical indications of social difficulties in children with “right hemisphere deficit syndrome” [I 9,
Trauner et al: Prosody after Perinatal Stroke
365
241. A recent study from this laboratory suggests that
children with either LH or RH lesions may have more
difficulty with social interactions 1331. A potentially
analogous situation exists with children who have developmental language impairment (LI), possibly secondary to LH dysfunction [34]. Berk and associates
[26] and Trauner and colleagues [27] have demonstrated prosodic deficits in a group of LI children, and
others [35-371 have identified psychosocial problems
in a similar population.
The results of our study do not appear to be related
to limitations in the ability of our subjects to comprehend verbal instructions. Although the lesion groups
scored slightly lower than their matched control groups
on a test of language comprehension, we would not
expect the differential patterns of defcits that we observed in each of the lesion groups simply as a result
of a comprehension problem. Rather, we would expect
globally impaired performance by both groups if they
simply did not comprehend the instructions as well as
the controls. Furthermore, the length of the verbal
stimuli used for the tasks showed no relation to performance among any of the groups tested. In fact, on the
task that involved the highest verbal comprehension
demands (spontaneous elicited linguistic prosody),
there was no difference between the lesion groups and
their controls.
The prosodic deficits observed in our subjects with
focal brain lesions follow patterns somewhat similar to
those observed in adults with late-acquired lesions, suggesting that there may be limitations to the ability of
the developing brain to reorganize after early brain
damage. Certain areas of the brain may be specialized
for these functions from very early in life, potentially
even in utero. However, given that affective expression
and linguistic prosodic skills are impaired with a lesion
in either hemisphere, it is possible that during brain
maturation, there is bilateral cerebral representation for
the skills necessary for normal prosodic development.
The results of this study have clinical implications
for children with evidence of focal brain damage. It is
possible that early intervention, in the form of social
skills development and an affect awareness program
such as outlined by Minskoff [38, 331 and more recently by Nowicki and Duke [40].,may ameliorate
some of the detrimental effects of early brain lesions.
This work was supported by grant 12-203 from the March of
Dimes Birth Defects Foundation.
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