Impaired speech shadowing after early lesions of either hemisphere

Impaired speech shadowing after early lesions of either hemisphere

Neuropsychologio, Vol. 25, No. 3, pp. 519-525, Printed in Great Britain. IMPAIRED 1987 @X%3932/87 53.00 + 0.00 Pergamon Journals Ltd. SPEECH SHADO...

525KB Sizes 0 Downloads 53 Views

Neuropsychologio, Vol. 25, No. 3, pp. 519-525, Printed in Great Britain.

IMPAIRED

1987

@X%3932/87 53.00 + 0.00 Pergamon Journals Ltd.

SPEECH SHADOWING AFTER EARLY LESIONS OF EITHER HEMISPHERE BRYAN T. WOODS*

Department of Neurology McLean Hospital and Harvard Medical School Boston, Massachusetts, U.S.A. (Accepted

14 November

1986)

Abstract-Patients with unilateral (right, left), non-progressive cerebral lesions incurred in infancy (prior to age one) or childhood (ages one to fifteen) were asked to shadow (rapidly repeat) passages of speech either in the form of syntactically correct sentences or random word order (RWO) sentences presented at varying rates. Both patient groups and same-age controls made more errors with faster rates of presentation. Error frequency was significantly higher for all patient groups than for controls, but did not significantly differ among the patient groups themselves. The abnormal performance of the group with later childhood right hemisphere lesions was remarkable in view of that group’s normal function on other language tests and normal verbal IQ score, and suggested that the cause of the problem in this group was either a specific linguistic factor not assessed by the other tests or a general factor brought out by speech shadowing.

INTRODUCTION THE OBSERVATION that language function is almost always lateralized to the left hemisphere in right-handed adults is a bedrock principle of the neurology of behavior, and there has recently been increasingly strong clinical [17] and experimental evidence [4] that this lateralization of function is already present at the initiation of language development. In a study of children with early nonprogressive unilateral cerebral damage, the author, working with H.-L. Teuber, noted that childhood lesions of the right hemisphere (RH) rarely result in aphasia [17], and do not appear to affect verbal IQ (VIQ) scores adversely [14]. It was further noted (unpublished data) that the same patients with childhood RH lesions perform as well as controls on a series of language tests that have revealed residual language deficits after childhood left hemisphere (LH) lesions [16]. It thus came as a considerable surprise that the same group of patients with childhood RH lesions is significantly impaired on one other test of linguistic performance, speech shadowing, and that the degree of impairment on this one test is quantitatively similar to that of the group of patients with childhood left hemisphere lesions. Speech shadowing [2] requires a person to repeat speech as he hears it. A dual-channel recording is made of the auditory input and spoken input, so that performance may be scored for both latency and accuracy. Reported response latencies for accurately shadowed continuous prose commonly range from 50&1500 msec [13], but Marslen-Wilson has found that some individuals can shadow at latencies of 25&290 msec, a distance of one syllable, with error rates ranging from 2-7% [7]. In spite of this extremely close following, however,

*Correspondence MA 02178, U.S.A.

to be addressed

to Dr B. T. Woods,

Department

519

of Neurology,

McLean

Hospital,

Belmont,

520

BRYAN T. WOODS

it is clear that shadowers make use of preceding syntactic and semantic information in their performance, since shadowing of random word order material increased latency by about 40% and errors by an even greater percentage [lo]. In the only study in which the shadowing technique has been used with adults with lateralized brain lesions [S], it has been found that patients with penetrating head wounds of either RH or LH are impaired relative to controls but that the LH patients are in turn significantly more impaired than the RH patients. Furthermore, the rate of presentation of material to be shadowed has a significantly different effect on patient performance than on control performance.

METHODS The speech shadowing material used in the current study was a portion of that used in the adult study of Lackner and Shattuck-Hufnagel. The material consisted of normal prose (NP) and pseudo-random word order (RWO) prose. Nine NP sentences, each 25 words in length, were read at rates of l-6 words per set (wps), with one sentence each at 1,5 and 6 wps, and two sentences each at 2,3, and 4 wps. The RWO material consisted ofeight of the nine NP sentences rearranged in pseudo-random work order, and presented at rates of I-5 wps, with one sentence each at 1 and 5, and two sentences each at 2, 3 and 4 wps. The NP version and the RWO version of each sentence were presented at the same rate. All passages were recorded by a single experienced female reader, using a stop watch and frequent practice runs to achieve a consistent, error-free presentation at the required rate. The final, single-channel stimulus tape consisted of 17 passages of 25 words each, pseudo-randomized both as to type ofmaterial (NP, RWO) and rate ofpresentation. The material was presented by headphones monaurally. Half the subjects heard the first nine passages with the right ear before reversing earphones; the others started with the left ear before alternating. Subjects were urged to repeat aloud as much as possible of what they heard of each passage. The two-channel output tape recording both the master tape and the subject’s shadowing responses. All scoring was done by a single, independent, blind observer who listened to and compared the two channels in order to determine errors and omissions. The extreme degree ofvariability in performance and the high error rates of many patients made meaningful and accurate latency determinations and qualitative determinations of types of errors impossible. Errors were scored on a word by word basis. An error occurred whenever the subjects produced words that were unrecognizable as target words or out of normal sequence; standards for pronunciation and word form were liberal. Omitted words were each counted as an error. The greatest possible number oferrors per sentence equalled the number of words in the sentence. Preliminary analysis indicated that side of presentation had no significant effect in any group so further analyses did not separate patients by side of initial presentation. The standardization population for the study consisted of 36 normal school children in grades 7, 9 or 11 in a surburban Boston community; there were six boys and six girls from each grade, and ages ranged from 12 to 18, with a median of 15. Single factor analysis of variance (ANOVA) on the data from this control group indicated that performance on shadowing varied significantly with age from both NP material P~0.06) and the RWO material (P~0.05). Mean errors decrease with age. The patient population studied has been described previously [14, 171. It consisted of individuals who had suffered unilateral (L, R) non-progressive cerebral lesions during infancy or childhood. Those whose lesions antedated their first birthday were the early group, while those whose lesions occurred between the first and fifteenth birthdays were the later group. Some patients, who had been included in previous studies, were under age 12 when tested and were excluded from this study; the remainder ranged in age from 12 to 25, with a median age of 16; they were thus somewhat older than the controls. Subdividing by side of lesion and age at lesion yielded four patient groups: right early (RE), n =9; left early (LE), n = 8; right later (RL), n = 1 I; and left later (LL), n = I 1,

RESULTS Figure 1 illustrates the error totals for controls different rates of presentation. ANOVA indicates d$ 4, 91, PC 0.001) and presentation rate effect significant interactions. Figure 2 illustrates the error totals for controls different rates of presentation. Again there are

and patient groups for NP sentences at a highly significant group effect (F= 5.865 (F= 62.034, d.f. 5, 355, P
EARLY

LESIONS

MEAN NUMBER OF ERRORS I

AND

ERRORS,

RATE 2/s

I/S

SPEECH

NP

521

SHADOWING

SENTENCES

OF PRESENTATION 3/s 4/s

5/S

6/S

2 3 4 5 6 7 8 9 IO II 12 I3 14 I5 I6 I7 I8 I9 20

.

RE

21

A

LL

22

0

LE

23

.

c

24 25

FIG. 1. Mean number

of shadowing (NP) sentences

errors per subject for lesion and control groups presented at different rates (l-6 words/set).

on normal

prose

d.j 4, 71 Pt0.005) and rate effects (F= 141.735, d.J 4,284 P
BRYAN T. WOODS

522

MEAN NUMBER OF ERRORS I/S

ERRORS,

RWO SENTENCES

RATE OF PRESENTATION 4/s 2/s 3/S

5/S

I

2 3

n

o

RL RE

5

A

LL

6

0

LE

7

0

c

4

a 9 IO II 12 13 14 15 16 17 I8 19 20 21 22 23 24 25

FIG. 2. Mean number order

of shadowing errors per subject for lesion and control groups on random (RWO) sentences presented at different rates (l-5 words/set).

word

Table 1. Mean and S.D. of verbal (VIQ) and performance (PIQ) scores and correlations of VIQ and PIQ scores to shadowing error scores on NP and RWO sentences for each lesion group.

VIQ

RL RE LL LE * P
Mean

S.D.

102.0 77.6 95.1 94.6

20.9 16.6 21.1 18.7

PIQ Correlation coefficient NP RWO -0.53 -0.70* -0.71* -0.78*

-0.34 -0.73s -0.78** -0.74*

Mean

S.D.

86.3 75.1 94.0 88.4

20.7 12.1 16.0 14.5

Correlation coefficient NP RWO -0.31 -0.50 -0.74** -0.90**

-0.05 -0.44 -0.81** -0.87**

**p<0.01

When one compares the four RL and LL group correlations of NP and RWO with VIQ and PIQ to one another, only the PIQ-RWO correlations differ significantly (Fisher’s r-z transformation, PcO.05). None of the LE vs RE comparisons of correlations differ significantly from one another. DISCUSSION If one assumes that speech shadowing is a language task, the defective performance of the two left lesion and the early right lesion groups are consistent with results of other test

EARLY

LESIONSAND SPEECH SHADOWING

523

procedures, but the equally defective performance of the RL group is not. There would appear to be at least two plausible alternative (but not mutually exclusive) ways of explaining the difference between the shadowing results and all the other language test results for the RL group. First, one might conclude that speech shadowing is a highly demanding and unusual task for all speakers, and that it stresses components of the language comprehension and production process that are not tapped by ordinary discourse, standard tests for aphasia, [S] the Weschler IQ test, or dichotic listening. One might further assume that at least one of these stressed components of language function is dependent on the integrity of the right hemisphere, and under the peculiar conditions of speech shadowing this right-hemispheredependent component is rate-limiting. Alternately, it might be argued that speech shadowing, although obviously a language task, is also highly dependent on other general factors of cerebral functioning, such as attention, motivation, or processing speed, and that one or more of these factors might be sufficiently vulnerable to right-hemisphere lesions to account for the observed impairment of shadowing performance. Though these two forms of explanations do not exclude one another, it is worthwhile to consider them separately. The role of the right hemisphere in speech in right handed adults has been debated since the time of Broca; Hughlings Jackson’s theory of a role of the right hemisphere in emotional utterances still excites interest [19]. Subsequent estimates of the importance of the right hemisphere in language function have varied with the mode of study. Classic lesion studies have indicated at most only minor impairment of speech with right hemisphere lesions, as contrasted to very limited residual speech function after complete adult onset LH lesions (e.g. hemispherectomy) [ll]. Observation of commissurotomy patients has suggested considerable RH comprehension of language but minimal production capability [ 1S]. Inactivation of the right hemisphere by sodium amytal infusion can produce transient speech arrest but otherwise has negligible effects on language in most right handers [9]. Electrical stimulation of the Rolandic fissure and supplementary motor areas of the right hemisphere can also produce speech arrest or even vocalization, apparently by a direct motoric effect on the vocal apparatus [8]. Finally, cerebral blood flow studies indicate that there is a considerable enhancement of right hemisphere blood flow in much of the perisylvian area during speech production [6]. One may conclude from these studies that even if the right hemisphere of most right handers has little independent capacity to generate speech, both the stimulation and cerebral blood flow studies indicate that the right hemisphere may play a quantitatively significant role in the actual motoric production of speech. It may be that lack of this normal right hemisphere motoric component of speech accounts for the speech shadowing deficit in the RL patients of this study and the adult right-sided lesion patients of Lackner and ShattuckHufnagel. It is of note that Marslen-Wilson concluded from the analysis of close shadowing by normal speakers that latency did not depend on speed of comprehension or level of analysis of the material, but on rapidity of initiation and decision-making on the output (motoric) side [7]. The other type of explanation for the finding of RL impairment is that the results arise, not from an impairment of a specific language function, but from a more general impairment. There is good reason to believe that some measures of cerebral function are sensitive to lesions anywhere in the cortex; a number of studies [ 1, 33 have reported that reaction times are increased by lesions of either hemisphere, while TELJBER and WEINSTEIN [ 121 found a test of hidden figure detection to be sensitive to lesions in any of the cerebral quadrants. The

524

BRYAN T. WEEDS

exquisite sensitivity of shadowing performance to rate of presentation in normal controls (Figs 1,2) makes a general speed factor a plausible alternative explanation for the finding. Nevertheless, even though only one of four RL-LL group differences in correlation of shadowing to IQ reaches significance, the LL correlations are all larger and at least suggest a difference in mechanism between the effects of RL and LL lesions on shadowing. Although the data on these patients do not exclude either explanation, the overall results of the study lead to one particular and one general conclusion. First, they indicate in particular that the speech shadowing process includes a functional component that is right-hemisphere dependent, but not closely related to the functions measured by verbal or performance IQ scores or tests for aphasia. More generally they serve as a reminder that language performance is not the product of a single unitary brain function, but rather the resultant of a number of relatively discrete processes that are normally smoothly integrated but may be separately impaired by focal brain lesions. Detection of some of these impairments may only be possible with tests that stress specific components of linguistic performance to their particular limits.

AcknowledgementsThis work was supported in part by NINDS Special Fellowship Grant 2 Fll 2370-02 NSRB, National Institutes of Health; in part by Grant RR-88 from the General Clinical Research Center Program of the Division of Research Resources, National Institutes of Health; in part by Grant 72-4-l from the Alfred P. Sloan Foundation; and in part by NIMH Grant NIH-5-ROl-MH24433 to Dr S. Corkin.

REFERENCES 1. BENTON, A.L. and JOYNT, J.R. Reaction time in unilateral cerebral disease. Con@. Neurologica 19, 247-256, 1959. of rapidly repeated speech sounds. Akusticheskii Zhurnal6, 392-398, 1960. 2. CHISTOVICH, L.A. Classification efficiency of intelligence and vigilance tests in detecting 3. DERENZI, E. and FAGLIONI, P. The comparative hemispheric cerebral damage. Cortex 1, 41c-433, 1965. of cerebral dominance. In S. SEGALOWITZ and F. A. 4. KINSBOURNE, M. and HISCOCK M. The development GKUBER (Editors) Academic Press, New York, 1977. 5. LACKNER, J. R. and SHATTUCK-HUFNAGEL S. R. Alterations in speech shadowing ability after cerebral injury in man. Neuropsychologia 20, 709%714, 1982. 6. LARSEN, B., SKINHOJ, E., SOH, K., ENDO, H. and LASSEN, H. A. The pattern of cortical activity provoked by listening and speech revealed by CBF measurements. In Cerebral Function Metabolism and Circulation, D. H. INCVOR and N. A. LASSEN (Editors) Acta Neural. Stand. Suppl. 64,56, 268-269, 1977. MARSLEN-WILSON, W. D. Linguistic structure and speech shadowing at very short latencies. Nutrtre, Lond. 244, 522-523, 1973. PENFIELD, W. and ROBERTS. L. Speech and Brain Mechanisms. Princeton University Press, Princeton, New Jersey, 1959. RASMUSSEN,T. and MILNER, B. Clinical and surgical studies of the cerebral speech areas in man. In Cerebral Localization, K. J. ZULCH, 0. CREUTZFELDT and G. C. GALBRAITH (Editors), Springer-Verlag, New York/Berlin, 1975. contribution of syntactic structure. Percept. Mot. 10. SHATTUCK, S. R. and LACKNER, J. R. Speech production: Skills 40, 931-936, 1975. hemispherectomy. Science 153, 1280-1282, 1966. 11. SMITH, A. and BURKLAND, C. W. Dominant 12. TEIJBER, H.-L. and WEINSTEIN, S. Ability to discover hidden figures after cerebral lesions. AMA Arch. Neurol. Psychiat. 76, 369.-379. 1956. and familiarity on translating and repeating back a foreign and a 13. TREISMAN, A. M. The effects of redundancy native language. Br. J. Psycho/. 56, 369-379, 1965. effects of right-hemisphere lesions after age one: Wechsler test data. 14. WOODS, B. T. The restricted Neuropsychologia 18, 65-~70, 1980.

EARLY LESIONSAND

SPEECH

SHADOWING

525

15. WOODS, B. T. Dichotic listening ear preference after childhood cerebral lesions. Neuropsychologia 22,3033310, 1984. 16. WOODS, B. T. and CAREY S. Language deficits after apparent clinical recovery from childhood aphasia. Ann. Neural. 6,405409, 1979. 17. WOODS, B. T. and TEUBER, H.-L. Changing patterns of childhood aphasia. Ann. Neural. 3, 2733280, 1978. 18. ZAIDEL E. Unilateral auditory language comprehension on the token test following cerebral commisurotomy and hemispherectomy. Neuropyschologia 15, l-18, 1977. 19. ZANGWILL, 0. L. Speech and the minor hemisphere. Acta Neuropsychiat. 67, 1013-1020, 1967.