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Speech comprehension after unilateral injection of sodium amytal
BRAIN
AND
LANGUAGE
22, 150-157 (1984)
Speech Comprehension after Unilateral Injection of Sodium Amytal JEANNETTE MCGLONE University
Hospital,
London,
Ontario,
Canada
A unilateral cerebral dominance model predicts that speech comprehension will be disrupted after injection of sodium amytal into one hemisphere but not after the other. This model was supported when an auditory receptive task involving relatively nonredundant stimuli similar to that contained in the Token Test (E. DeRenzi & L. Vignolo, 1962, Brain, 85, 665-687) was administered to 17 epileptic patients undergoing bilateral amytal injections.
INTRODUCTION
Earlier reports have suggestedthat language comprehension is unaffected by injection of sodium amytal into the left or right cerebral arteries (Wada & Rasmussen, 1960). Despite muteness or expressive aphasia, injected patients could execute simple body movements to verbal command (e.g., wiggle fingers, squeeze hand, open eyes). These findings contrast with DeRenzi and Faglioni’s report (1978) that 92.5% of aphasic stroke patients showed marked impairment on the Token Test, a well-known measure of speech comprehension whereby the patient is told to point to stimuli that vary according to color, shape, and size. Interestingly, only 60% of the latter patients made errors in executing body movements to verbal command. Data from split brain patients support these observations in so far as the disconnected right cerebral hemisphere responded to simple verbal commands involving gesture (Gazzaniga & Sperry, 1967), but was unable to cope with a test of nonredundant, context-free auditory comprehension such as the Token Test (Zaidel, 1977). I am grateful to Drs. Warren Blume and Alan Fox who aided in the sodium amytal procedures, Nina Manion who collated and analyzed the data, and to Dr. Doreen Kimura for her comments on the manuscript. This project was supported by grants from the Ontario Mental Health Foundation and the Laidlaw Foundation. An earlier version of this paper was presented at the 1982 meetings of BABBLE. Send requests for reprints to the author at: Department of Psychological Services, University Hospital, P.O. Box 5339, Postal Station A, LONDON, Ontario N6A 5A5, Canada. 150 0093-934X/84 $3.00 Copyright All rights
0 1984 by Academic Press, Inc. of reproduction in any form reserved
COMPREHENSION
AFTER AMYTAL
INJECTION
151
This report is concerned with whether some aspects of speech comprehension may be unilaterally organized in the brain. Injection of sodium amytal into the internal carotid artery temporarily disrupts functioning on one side of the brain. If one cerebral hemisphere were dominant for speech comprehension, then its anesthetization would produce marked impairment after one injection but not after the other. A bilateral model predicts that the injection of sodium amytal into each cerebral hemisphere would produce either no comprehension errors due presumedly to the opposite hemisphere’s capacity to produce the information and respond correctly, or a few errors might be made after both left and right injections. The relationship between lateralization of expressive and receptive speech functions was also investigated. METHODS Subjects. From January 1978to December 1982, 29 epileptic patients undergoing bilateral sodium amytal procedures prior to neurosurgery were tested on speech comprehension. From these, 12 were omitted due to preexisting hemiparesis, hearing loss, visual field defects, dysphasia, pre- or postinjection seizure, or prolonged unresponsiveness after one or both injections. The remaining 17 patients are described in Table 1. Hand preference was defined by the demonstrated use of the same side for writing and six of seven other activities. Left-handers and ambidexters were grouped together in the data analyses. The mean age of the sample was 24.7 years (SD 8.7) with an educational level of 11.O grades (SD 2.6). The mean intellectual and memory levels fell within average limits on the Wechsler scales (Full Scale IQ = 98.4, SD 9.3; Memory Quotient = 94.1, SD 11.3). Tasks: expression. Procedures developed at the Montreal Neurological Institute were adapted to assess expressive speech functions (Milner, 1975).Patients were asked to count, TABLE 1 PATIENT
CHARACTERISTICS
N Etiology
7 6 3 1
Tumor No gross pathology Atrophy Agenesis of corpus callosum
EEG focus
15 2 5 10 2
Temporal lobe Frontal lobe Left sided Right sided Bilateral
Onset
7 10
Before age 5 After age 5
Handedness and Sex
12 Right: 3” Pure left: 2” Ambidextrous:
a Data combined.
5 male 1 male 1 male
7 female 2 female 1 female
152
JEANNETTE
MC GLONE
say the days of the week forward, name eight objects (pencil, ring, matches, fork, comb, ashtray, scissors, button), and repeat four phrases (sea shells, many numbers, shrimp fries, ba da pa). Aphasic errors consisted of mispronounciations (other than dysarthria), misnaming, perseverations, or impaired sequencing on the above tasks. Errors were expressed as a percentage of total output over all four subtests. That is, if 10 errors were made in the course of 40 presentations/utterances, the score would be 25%. Comprehension: body commands. Immediately after the injection, each patient was instructed to maneuver the nonparetic hand (e.g., “Stop wiggling the fingers.” “Put your hand down.“). To insure that the patient was alert, other verbal commands were given such as, “Open/close your eyes,” and “Look at me.” A modified version of the Token Test (DeRenzi & Vignolo, 1962)was used to measure auditory speech comprehension. A 12.5 x 20-cm card contained a vertical array of four black shapes: large square, small circle, small square, and large circle (Fig. 1). The examiner held the card within focal and reaching distance of the patient who was lying on a stretcher. With the hand ipsilateral to the injection, the patient was asked to point in turn to (1) the small square, (2) the two circles, (3) the large square and then the large circle. The examiner did not repeat the same command twice. All errors were recorded (maximum = 9). For example, if on the first command, the patient responded by pointing to the small circle, one error was counted. The raw score was converted to a percentage error score (number errors/number items x 100) because some patients were administered fewer than three commands due to uncontrollable variations in the clinical protocol. In the rare instance where it was obvious that a patient could not see the card (postinjection neglect or visual field defect) or misreached beyond the card (past pointing), the items were readministered later, and the initial performance was not counted as a speech comprehension error. Procedure. On separate days a bolus of 175 mg sodium amytal dissolved in 3.5 cc saline was injected transfemorally into the left and right carotid arteries. The side injected first was counterbalanced across patients in a random fashion. Just before the injection the patient’s arms were extended, fingers wiggling, and she/he was asked to count aloud. The receptive and expressive tasks were administered immediately prior to injection (no-drug baseline), after the left and after the right injections. Care was taken to maintain the patient’s full attention before testing comprehension and to present the stimuli in the
FIG. 1. Modified Token Test.
COMPREHENSION
AFTER AMYTAL
INJECTION
153
good visual field. The comprehension task involving body commands was given within the first minute after injection, followed by expressive tests and then the modified Token Test. Expressive testing proceeded immediately following the mute period, but speech comprehension may have been administered earlier if muteness was prolonged. The critical period during which the drug had a unilateral effect was determined by the length of the hemiparesis opposite to the injected hemisphere or by the presence of unilateral delta activity over the injected hemisphere, whichever was longer. Grip strength was measured in pounds per square inch with a bulb dynamometer (Martin Vigorimeter) prior to the injection and every 30 set thereafter. Continuous EEG monitoring (16 channel bipolar montage along the parasagittal and temporal planes) recorded the length of the unilateral delta activity. The time at which strength returned to preinjection levels and the length of the delta activity was recorded (Fig. 2). Detailed scoring of responses and behavior was based on a review of the video tapes and verbatim record of the event.
RESULTS
Critical period. Figure 2 shows that strength returned to baseline levels at 467.9 set after the left injection and 438.9 set after the right (t(16) = 0.70, ns). Unilateral delta activity lasted for 500.6 set on the left and 411.3 set on the right (t(U) = 3.25, p < .005). Expression. Of the 17 patients, 16 made one or more expressive speech errors after a left injection compared to 6/17 patients after right injection (x2 (Yates correction) (1) = 10.43, p < .OOS).The percentage error score was 0% on baseline, 20.5% after the left injection, and 2.6% after the right injection. A one-way ANOVA revealed a significant main effect of condition (F(2, 48) = 17.76, p < .OOOl). The left-injection score was impaired relative to baseline performance (t(49) = 5.47, p < .OOOl)and to the right-injection score ($48) = -4.78, p < .OOOl), but the latter conditions were comparable (t(48) = 0.69, ns). Comprehension. Within 30 to 60 set all patients obeyed commands to * open/close their eyes and rest the arm ipsilateral to the injection on the chest. No left-right comparisons were made on this task. On the modified Token test all 17 patients made one or more speech comprehension errors after the left injection compared to 3/17 after the right injection (x2 (Yates correction) (1) = 19.97, p < .OOl). After the
; --------I t
I 100
’
COMPREHENSION
,
I
I
I
200
300
400
500
I
600 (SEC)
INJEtTlON
FIG.
time.
2. Length of the drug effect in relation to speech comprehension presentation
154
JEANNETTE
MC CLONE
left injection the percentage error score was 61.2% compared with 3.9% after the right injection and 0% during baseline. A one-way ANOVA revealed a main effect of condition (F(2, 48) = 59.3, p < .OOOl). The left injection score was significantly impaired relative to baseline (t(48) = 9.72, p < .OOOl), and relative to the right injection (t(48) = -9.10, p < .OOOl),but the latter conditions were equivalent (f(48) = 0.62, ns). Analysis of covariance taking into account the postinjection time (see Fig. 2) did not alter the above findings. Lateralization of expression versus comprehension. The hemisphere dominant for expressive speech was defined arbitrarily as the presence of two or more aphasic errors after one injection and one or no errors after injection into the opposite hemisphere. The remainder were classified as mixed dominant. Because the range of scores was smaller for the modified Token Test than the expressive tests, the hemisphere dominant for speech comprehension was defined arbitrarily as the presence of 1 or more errors after one injection and no errors after the other, with the remainder classified as mixed. A x2 analyses in Table 2 shows a trend relating the side dominant for expressive and receptive speech functions in this heterogeneous sample. Using the same cut off scores the majority of right-handers (10/12) were classified as left dominant on both tasks (x2 (Yates correction) (1) = 4.86, p < .OS). Hand preference. Table 3 shows that more expressive errors were made after the left than the right injection, however a side by handedness interaction revealed that this asymmetry was not statistically significant in the small left-handed sample (t(4) = 0.89, ns). After the left injection, right-handers made significantly more errors than the left-handers (t( 15)= 2.73, p < .02), but the reverse was not true after right-sided injections (t(15) = -.93, ns). TABLE 2 EXPRESSIVEAND RECEPTIVE SPEECH LATERALIZATION IN TOTAL SAMPLES
Expressive
Receptive Left (13) or right (1) dominant Mixed (3) dominant
Left (3) or right (1) dominant
Mixed (3) dominant
13
1
1
2
a x2 (Yates correction) (1) = 2.95, p < .lO.
COMPREHENSION
AFTER AMYTAL
155
INJECTION
TABLE 3 PERCENTAGE ERRORSCORES ON SPEECHTASKSIN HAND PREFERENCE GROUPS Expression Right injection
Left injection x Right-handers (12) Left-handers (5) Expression Comprehension
-
Comprehension Left injection x
x
Right injection x
(%)
SD
(%)
SD
1%)
SD
(9%)
SD
25.6 8.1
19.3 3.5
1.8 4.5
3.5 6.2
61.1 61.4
30.5 33.3
1.9 8.9
6.4 14.5
Side, F(1, 15) = 7.98, p < .Ol Side x Handedness, F(1, 15) = 4.37, p < .05 Side, F(1, 15) = 40.47, p < .OOOl
On comprehension (Table 3), the laterality effect indicated significantly more errors after left than right injections, regardless of hand preference. Comparisons across tasks are hampered because the expressive and receptive testing took place at different postinjection periods. However, the data for left-handers suggest that degree of left hemisphere control over speech comprehension may be more marked than for expression. Sex differences were not analyzed on these tasks due to inherent bias whereby the same drug dosage resulted in a prolonged disruption of function in the smaller female than male brain (see McGlone & Fox, 1982). DISCUSSION
Auditory speech comprehension is clearly not a unitary phenomenon as evidenced from the pattern of receptive impairments seen after the injection of sodium amytal into the left cerebral hemisphere. In agreement with previous observations (Wada & Rasmussen, 1960), we too found that very quickly the right hemisphere obeyed certain commands such as lowering the arm, directing gaze, and reaching. In contrast, errors were made processing other verbal commands such as the identification of a small square among a choice of four geometric forms. It seems unlikely that the underlying defect was impaired size or shape discrimination because more complex pictorial material was identified correctly during expressive and memory testing. Nor was this defect related to impaired localization or manual apraxia because, if necessary, testing was delayed until the required hand posture and reaching behavior occurred. Attentional deficits were ruled out by the fact that the patient responded promptly though erroneously.
156
JEANNETTE
MC GLONE
Zaidel (1977) has suggested that the right hemisphere’s limited short term memory store (maximum = 3 + 1 items) may account for its failure on the Token Test. In the present study an equal number of errors were made on the two item commands as on the five item command. Length of the sequence may be important but seems not to be sufficient. Zaidel (1976, 1977) also observed that a rich pictorial context improved comprehension of auditory commands. This provided redundancy to the auditory signal, a feature that DeRenzi and Vignolo (1962) purposefully reduced in their construction of the Token Test. The absence of redundancy cues (contextual, pictorial, intonational, motoric, or repetition) in a sequence of commands makes speech comprehension highly dependent upon phoneme discrimination and decoding. The latter processes may indeed be the most critical features underlying hemispheric lateralization of speech comprehension. Although the present study failed to demonstrate a statistically significant relationship between lateralization of expressive and receptive functions in a heterogeneous sample, it was clear that both are closely tied to left hemisphere processes in right-handers. A much larger left-handed sample is needed before any definitive pattern emerges. However, discrepancies between these data and that of Hecaen and Sauget (1971) are worth contrasting. Their study found that comprehension disorders were significantly more frequent in right- than left-handers after left-sided lesions, whereas the current results imply an equally severe comprehension deficit in left- and right-handers after amytal injections. Within their left-handed group, comprehension and expressive disorders occurred equally often regardless of side of lesion. However, in our study a clear laterality effect was found for the receptive task. Methodologies of the two studies differ markedly, nevertheless, our preliminary findings would lead to the conclusion that some speech comprehension skills are as lateralized in lefthanders as in right-handers, and indeed may be more lateralized than expressive skills. The unexpectedly longer drug effect after the left than right injection was not related to the predominance of right-sided lesions in the sample because the asymmetry was of the same magnitude in patients with leftsided EEG foci. Angiograms taken from the hand injection of dye were examined to see whether the drug had a different course after left versus right injection. In all cases the middle cerebral and anterior cerebral arteries filled. The posterior cerebral artery filled in 6/17 left injections compared to 4/17 right injections. Regardless of side, the critical period was longer when the posterior artery filled than when it did not. In part the variation in length of the critical period may be due to asymmetrical filling of the cerebral vessels. However in eight cases where the posterior cerebral artery did not fill after either injection, average length of the drug effect was still longer after left than right injections. There is no
COMPREHENSION
AFTER
AMYTAL
INJECTION
157
clear explanation why the left cerebral hemisphere may be more susceptible to the effects of a depressant medication, but animal studies would determine if this is a uniquely human phenomenon or not. REFERENCES DeRenzi. E.. & Faglioni. P. 197X. Normative data and screening power of a shortened version of the Token Test. Cor/ex. 14, 41-4Y. DcRenzi. E.. & Vignolo. 1.. lY62. The Token Test: A sensitive test to detect rcceptivc disturbances in aphasics. Hrtrin. 85, 665-678. Gazzaniga. M.. & Sperry. R. 1967. Language after section of cerebral commissures. Bruin. 90, 131-14x. Hecaen. H.. & Sauget, J. 1971. Cerebral dominance in left-handed subjects. Corrcx. 7. 194-i. McGlone. J.. & Fox. A. 1982. Evidence from sodium amytal studies of greater asymmetry of verbal representation in men compared to women. In H. Akimoto. H. Kazamatsuri. M. Seino. & A. Ward (Eds.). AdrclnccJs in epilepto1og.v: Xllliir epilepsy intc~rnutioncd s~mposirrm. New York: Raven Press. Pp. 389-391. Mimer. B. 1975. Psychological aspects of focal epilepsy and its neurosurgical management. In D. Purpura, J. Penry. & R. Walter (Eds.). Adtwrrcc.\ in nrrtro/o,qv. New York, Raven Press. Pp. 29!-321. Wada. J., & Rasmussen. T. 1960. lntracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. Jortrrrul of Nwrosur~rry. 17, 266-282. Zaidel. E. 1976. Auditory vocabulary of the right hemisphere following brain bisection or hemidecortication. Corfcx. 12, 191-21 I. Zaidel. E. 1977. Unilateral auditory comprehension on the Token Test following cerebral commissurotomy and hemispherectomy. N~ftrops?choloRio. 15, I-18.
AND
LANGUAGE
22, 150-157 (1984)
Speech Comprehension after Unilateral Injection of Sodium Amytal JEANNETTE MCGLONE University
Hospital,
London,
Ontario,
Canada
A unilateral cerebral dominance model predicts that speech comprehension will be disrupted after injection of sodium amytal into one hemisphere but not after the other. This model was supported when an auditory receptive task involving relatively nonredundant stimuli similar to that contained in the Token Test (E. DeRenzi & L. Vignolo, 1962, Brain, 85, 665-687) was administered to 17 epileptic patients undergoing bilateral amytal injections.
INTRODUCTION
Earlier reports have suggestedthat language comprehension is unaffected by injection of sodium amytal into the left or right cerebral arteries (Wada & Rasmussen, 1960). Despite muteness or expressive aphasia, injected patients could execute simple body movements to verbal command (e.g., wiggle fingers, squeeze hand, open eyes). These findings contrast with DeRenzi and Faglioni’s report (1978) that 92.5% of aphasic stroke patients showed marked impairment on the Token Test, a well-known measure of speech comprehension whereby the patient is told to point to stimuli that vary according to color, shape, and size. Interestingly, only 60% of the latter patients made errors in executing body movements to verbal command. Data from split brain patients support these observations in so far as the disconnected right cerebral hemisphere responded to simple verbal commands involving gesture (Gazzaniga & Sperry, 1967), but was unable to cope with a test of nonredundant, context-free auditory comprehension such as the Token Test (Zaidel, 1977). I am grateful to Drs. Warren Blume and Alan Fox who aided in the sodium amytal procedures, Nina Manion who collated and analyzed the data, and to Dr. Doreen Kimura for her comments on the manuscript. This project was supported by grants from the Ontario Mental Health Foundation and the Laidlaw Foundation. An earlier version of this paper was presented at the 1982 meetings of BABBLE. Send requests for reprints to the author at: Department of Psychological Services, University Hospital, P.O. Box 5339, Postal Station A, LONDON, Ontario N6A 5A5, Canada. 150 0093-934X/84 $3.00 Copyright All rights
0 1984 by Academic Press, Inc. of reproduction in any form reserved
COMPREHENSION
AFTER AMYTAL
INJECTION
151
This report is concerned with whether some aspects of speech comprehension may be unilaterally organized in the brain. Injection of sodium amytal into the internal carotid artery temporarily disrupts functioning on one side of the brain. If one cerebral hemisphere were dominant for speech comprehension, then its anesthetization would produce marked impairment after one injection but not after the other. A bilateral model predicts that the injection of sodium amytal into each cerebral hemisphere would produce either no comprehension errors due presumedly to the opposite hemisphere’s capacity to produce the information and respond correctly, or a few errors might be made after both left and right injections. The relationship between lateralization of expressive and receptive speech functions was also investigated. METHODS Subjects. From January 1978to December 1982, 29 epileptic patients undergoing bilateral sodium amytal procedures prior to neurosurgery were tested on speech comprehension. From these, 12 were omitted due to preexisting hemiparesis, hearing loss, visual field defects, dysphasia, pre- or postinjection seizure, or prolonged unresponsiveness after one or both injections. The remaining 17 patients are described in Table 1. Hand preference was defined by the demonstrated use of the same side for writing and six of seven other activities. Left-handers and ambidexters were grouped together in the data analyses. The mean age of the sample was 24.7 years (SD 8.7) with an educational level of 11.O grades (SD 2.6). The mean intellectual and memory levels fell within average limits on the Wechsler scales (Full Scale IQ = 98.4, SD 9.3; Memory Quotient = 94.1, SD 11.3). Tasks: expression. Procedures developed at the Montreal Neurological Institute were adapted to assess expressive speech functions (Milner, 1975).Patients were asked to count, TABLE 1 PATIENT
CHARACTERISTICS
N Etiology
7 6 3 1
Tumor No gross pathology Atrophy Agenesis of corpus callosum
EEG focus
15 2 5 10 2
Temporal lobe Frontal lobe Left sided Right sided Bilateral
Onset
7 10
Before age 5 After age 5
Handedness and Sex
12 Right: 3” Pure left: 2” Ambidextrous:
a Data combined.
5 male 1 male 1 male
7 female 2 female 1 female
152
JEANNETTE
MC GLONE
say the days of the week forward, name eight objects (pencil, ring, matches, fork, comb, ashtray, scissors, button), and repeat four phrases (sea shells, many numbers, shrimp fries, ba da pa). Aphasic errors consisted of mispronounciations (other than dysarthria), misnaming, perseverations, or impaired sequencing on the above tasks. Errors were expressed as a percentage of total output over all four subtests. That is, if 10 errors were made in the course of 40 presentations/utterances, the score would be 25%. Comprehension: body commands. Immediately after the injection, each patient was instructed to maneuver the nonparetic hand (e.g., “Stop wiggling the fingers.” “Put your hand down.“). To insure that the patient was alert, other verbal commands were given such as, “Open/close your eyes,” and “Look at me.” A modified version of the Token Test (DeRenzi & Vignolo, 1962)was used to measure auditory speech comprehension. A 12.5 x 20-cm card contained a vertical array of four black shapes: large square, small circle, small square, and large circle (Fig. 1). The examiner held the card within focal and reaching distance of the patient who was lying on a stretcher. With the hand ipsilateral to the injection, the patient was asked to point in turn to (1) the small square, (2) the two circles, (3) the large square and then the large circle. The examiner did not repeat the same command twice. All errors were recorded (maximum = 9). For example, if on the first command, the patient responded by pointing to the small circle, one error was counted. The raw score was converted to a percentage error score (number errors/number items x 100) because some patients were administered fewer than three commands due to uncontrollable variations in the clinical protocol. In the rare instance where it was obvious that a patient could not see the card (postinjection neglect or visual field defect) or misreached beyond the card (past pointing), the items were readministered later, and the initial performance was not counted as a speech comprehension error. Procedure. On separate days a bolus of 175 mg sodium amytal dissolved in 3.5 cc saline was injected transfemorally into the left and right carotid arteries. The side injected first was counterbalanced across patients in a random fashion. Just before the injection the patient’s arms were extended, fingers wiggling, and she/he was asked to count aloud. The receptive and expressive tasks were administered immediately prior to injection (no-drug baseline), after the left and after the right injections. Care was taken to maintain the patient’s full attention before testing comprehension and to present the stimuli in the
FIG. 1. Modified Token Test.
COMPREHENSION
AFTER AMYTAL
INJECTION
153
good visual field. The comprehension task involving body commands was given within the first minute after injection, followed by expressive tests and then the modified Token Test. Expressive testing proceeded immediately following the mute period, but speech comprehension may have been administered earlier if muteness was prolonged. The critical period during which the drug had a unilateral effect was determined by the length of the hemiparesis opposite to the injected hemisphere or by the presence of unilateral delta activity over the injected hemisphere, whichever was longer. Grip strength was measured in pounds per square inch with a bulb dynamometer (Martin Vigorimeter) prior to the injection and every 30 set thereafter. Continuous EEG monitoring (16 channel bipolar montage along the parasagittal and temporal planes) recorded the length of the unilateral delta activity. The time at which strength returned to preinjection levels and the length of the delta activity was recorded (Fig. 2). Detailed scoring of responses and behavior was based on a review of the video tapes and verbatim record of the event.
RESULTS
Critical period. Figure 2 shows that strength returned to baseline levels at 467.9 set after the left injection and 438.9 set after the right (t(16) = 0.70, ns). Unilateral delta activity lasted for 500.6 set on the left and 411.3 set on the right (t(U) = 3.25, p < .005). Expression. Of the 17 patients, 16 made one or more expressive speech errors after a left injection compared to 6/17 patients after right injection (x2 (Yates correction) (1) = 10.43, p < .OOS).The percentage error score was 0% on baseline, 20.5% after the left injection, and 2.6% after the right injection. A one-way ANOVA revealed a significant main effect of condition (F(2, 48) = 17.76, p < .OOOl). The left-injection score was impaired relative to baseline performance (t(49) = 5.47, p < .OOOl)and to the right-injection score ($48) = -4.78, p < .OOOl), but the latter conditions were comparable (t(48) = 0.69, ns). Comprehension. Within 30 to 60 set all patients obeyed commands to * open/close their eyes and rest the arm ipsilateral to the injection on the chest. No left-right comparisons were made on this task. On the modified Token test all 17 patients made one or more speech comprehension errors after the left injection compared to 3/17 after the right injection (x2 (Yates correction) (1) = 19.97, p < .OOl). After the
; --------I t
I 100
’
COMPREHENSION
,
I
I
I
200
300
400
500
I
600 (SEC)
INJEtTlON
FIG.
time.
2. Length of the drug effect in relation to speech comprehension presentation
154
JEANNETTE
MC CLONE
left injection the percentage error score was 61.2% compared with 3.9% after the right injection and 0% during baseline. A one-way ANOVA revealed a main effect of condition (F(2, 48) = 59.3, p < .OOOl). The left injection score was significantly impaired relative to baseline (t(48) = 9.72, p < .OOOl), and relative to the right injection (t(48) = -9.10, p < .OOOl),but the latter conditions were equivalent (f(48) = 0.62, ns). Analysis of covariance taking into account the postinjection time (see Fig. 2) did not alter the above findings. Lateralization of expression versus comprehension. The hemisphere dominant for expressive speech was defined arbitrarily as the presence of two or more aphasic errors after one injection and one or no errors after injection into the opposite hemisphere. The remainder were classified as mixed dominant. Because the range of scores was smaller for the modified Token Test than the expressive tests, the hemisphere dominant for speech comprehension was defined arbitrarily as the presence of 1 or more errors after one injection and no errors after the other, with the remainder classified as mixed. A x2 analyses in Table 2 shows a trend relating the side dominant for expressive and receptive speech functions in this heterogeneous sample. Using the same cut off scores the majority of right-handers (10/12) were classified as left dominant on both tasks (x2 (Yates correction) (1) = 4.86, p < .OS). Hand preference. Table 3 shows that more expressive errors were made after the left than the right injection, however a side by handedness interaction revealed that this asymmetry was not statistically significant in the small left-handed sample (t(4) = 0.89, ns). After the left injection, right-handers made significantly more errors than the left-handers (t( 15)= 2.73, p < .02), but the reverse was not true after right-sided injections (t(15) = -.93, ns). TABLE 2 EXPRESSIVEAND RECEPTIVE SPEECH LATERALIZATION IN TOTAL SAMPLES
Expressive
Receptive Left (13) or right (1) dominant Mixed (3) dominant
Left (3) or right (1) dominant
Mixed (3) dominant
13
1
1
2
a x2 (Yates correction) (1) = 2.95, p < .lO.
COMPREHENSION
AFTER AMYTAL
155
INJECTION
TABLE 3 PERCENTAGE ERRORSCORES ON SPEECHTASKSIN HAND PREFERENCE GROUPS Expression Right injection
Left injection x Right-handers (12) Left-handers (5) Expression Comprehension
-
Comprehension Left injection x
x
Right injection x
(%)
SD
(%)
SD
1%)
SD
(9%)
SD
25.6 8.1
19.3 3.5
1.8 4.5
3.5 6.2
61.1 61.4
30.5 33.3
1.9 8.9
6.4 14.5
Side, F(1, 15) = 7.98, p < .Ol Side x Handedness, F(1, 15) = 4.37, p < .05 Side, F(1, 15) = 40.47, p < .OOOl
On comprehension (Table 3), the laterality effect indicated significantly more errors after left than right injections, regardless of hand preference. Comparisons across tasks are hampered because the expressive and receptive testing took place at different postinjection periods. However, the data for left-handers suggest that degree of left hemisphere control over speech comprehension may be more marked than for expression. Sex differences were not analyzed on these tasks due to inherent bias whereby the same drug dosage resulted in a prolonged disruption of function in the smaller female than male brain (see McGlone & Fox, 1982). DISCUSSION
Auditory speech comprehension is clearly not a unitary phenomenon as evidenced from the pattern of receptive impairments seen after the injection of sodium amytal into the left cerebral hemisphere. In agreement with previous observations (Wada & Rasmussen, 1960), we too found that very quickly the right hemisphere obeyed certain commands such as lowering the arm, directing gaze, and reaching. In contrast, errors were made processing other verbal commands such as the identification of a small square among a choice of four geometric forms. It seems unlikely that the underlying defect was impaired size or shape discrimination because more complex pictorial material was identified correctly during expressive and memory testing. Nor was this defect related to impaired localization or manual apraxia because, if necessary, testing was delayed until the required hand posture and reaching behavior occurred. Attentional deficits were ruled out by the fact that the patient responded promptly though erroneously.
156
JEANNETTE
MC GLONE
Zaidel (1977) has suggested that the right hemisphere’s limited short term memory store (maximum = 3 + 1 items) may account for its failure on the Token Test. In the present study an equal number of errors were made on the two item commands as on the five item command. Length of the sequence may be important but seems not to be sufficient. Zaidel (1976, 1977) also observed that a rich pictorial context improved comprehension of auditory commands. This provided redundancy to the auditory signal, a feature that DeRenzi and Vignolo (1962) purposefully reduced in their construction of the Token Test. The absence of redundancy cues (contextual, pictorial, intonational, motoric, or repetition) in a sequence of commands makes speech comprehension highly dependent upon phoneme discrimination and decoding. The latter processes may indeed be the most critical features underlying hemispheric lateralization of speech comprehension. Although the present study failed to demonstrate a statistically significant relationship between lateralization of expressive and receptive functions in a heterogeneous sample, it was clear that both are closely tied to left hemisphere processes in right-handers. A much larger left-handed sample is needed before any definitive pattern emerges. However, discrepancies between these data and that of Hecaen and Sauget (1971) are worth contrasting. Their study found that comprehension disorders were significantly more frequent in right- than left-handers after left-sided lesions, whereas the current results imply an equally severe comprehension deficit in left- and right-handers after amytal injections. Within their left-handed group, comprehension and expressive disorders occurred equally often regardless of side of lesion. However, in our study a clear laterality effect was found for the receptive task. Methodologies of the two studies differ markedly, nevertheless, our preliminary findings would lead to the conclusion that some speech comprehension skills are as lateralized in lefthanders as in right-handers, and indeed may be more lateralized than expressive skills. The unexpectedly longer drug effect after the left than right injection was not related to the predominance of right-sided lesions in the sample because the asymmetry was of the same magnitude in patients with leftsided EEG foci. Angiograms taken from the hand injection of dye were examined to see whether the drug had a different course after left versus right injection. In all cases the middle cerebral and anterior cerebral arteries filled. The posterior cerebral artery filled in 6/17 left injections compared to 4/17 right injections. Regardless of side, the critical period was longer when the posterior artery filled than when it did not. In part the variation in length of the critical period may be due to asymmetrical filling of the cerebral vessels. However in eight cases where the posterior cerebral artery did not fill after either injection, average length of the drug effect was still longer after left than right injections. There is no
COMPREHENSION
AFTER
AMYTAL
INJECTION
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clear explanation why the left cerebral hemisphere may be more susceptible to the effects of a depressant medication, but animal studies would determine if this is a uniquely human phenomenon or not. REFERENCES DeRenzi. E.. & Faglioni. P. 197X. Normative data and screening power of a shortened version of the Token Test. Cor/ex. 14, 41-4Y. DcRenzi. E.. & Vignolo. 1.. lY62. The Token Test: A sensitive test to detect rcceptivc disturbances in aphasics. Hrtrin. 85, 665-678. Gazzaniga. M.. & Sperry. R. 1967. Language after section of cerebral commissures. Bruin. 90, 131-14x. Hecaen. H.. & Sauget, J. 1971. Cerebral dominance in left-handed subjects. Corrcx. 7. 194-i. McGlone. J.. & Fox. A. 1982. Evidence from sodium amytal studies of greater asymmetry of verbal representation in men compared to women. In H. Akimoto. H. Kazamatsuri. M. Seino. & A. Ward (Eds.). AdrclnccJs in epilepto1og.v: Xllliir epilepsy intc~rnutioncd s~mposirrm. New York: Raven Press. Pp. 389-391. Mimer. B. 1975. Psychological aspects of focal epilepsy and its neurosurgical management. In D. Purpura, J. Penry. & R. Walter (Eds.). Adtwrrcc.\ in nrrtro/o,qv. New York, Raven Press. Pp. 29!-321. Wada. J., & Rasmussen. T. 1960. lntracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. Jortrrrul of Nwrosur~rry. 17, 266-282. Zaidel. E. 1976. Auditory vocabulary of the right hemisphere following brain bisection or hemidecortication. Corfcx. 12, 191-21 I. Zaidel. E. 1977. Unilateral auditory comprehension on the Token Test following cerebral commissurotomy and hemispherectomy. N~ftrops?choloRio. 15, I-18.