Speech lateralization in deaf populations: Evidence for a developmental critical period

JOURNAL

OF BRAIN

AND

LANGUAGE

39, 134-152 (I!%))

Speech Lateralization in Deaf Populations: Evidence for a Developmental Critical Period ANN C. MARCOTTE Department

of Psychiatry and Human Behavior, Brown University Program in Medicine, and Department of Pediatrics, Memorial Hospital of Rhode Island

AND DONNA Department

of Psychiatry,

A. MORERE

University

of Rochester

Medical

Center

Cerebral lateralization for speech in right-handed normal hearing and deaf adolescents was assessed using the dual-task paradigm. Subjects with normal hearing and deafness acquired after 3 years of age displayed left hemispheric dominance for speech production, whereas both congenitally deaf and those with an early acquired deafness (onset 6-36 months) showed atypical, anomalous cerebral representation. These results suggest the presence of a developmental critical period for cerebral lateralization during which exposure to adequate environmental stimulation may be needed to activate left hemispheric dominance for speech. 0 1990 Academic Press, Inc.

INTRODUCTION

During the past decade, evidence from converging neurological and neuropsychological research has strengthened the notion that the left cerebral hemisphere is specialized at birth for the regulation and control of speech and language processes. Evidence has come from neuroanatomical studies of neonatal brains, infant behavioral research, and from differential electrophysiological arousal studies in day-old neonates as This project was funded in part by a University of Alabama at Birmingham Graduate School Faculty Research Grant (1986-1987). Preliminary findings reported in this article were presented at the 96th Annual Convention of the American Psychological Association in August, 1988. Special thanks to Drs. Frieda Meacham, Phillip Wade, and Jack Hawkins of the Alabama Institute for the Deaf and Blind for their support and assistance in this project. Requests for reprints should be sent to Ann C. Marcotte, Department of Pediatrics, Memorial Hospital of Rhode Island, 111 Brewster Street, Pawtucket, RI 02860. 134 0093-934x190 $3.00 Copyright All rights

0 1990 by Academic Press. Inc. of reproduction in any form reserved.

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well as in premature infants (see Kinsbourne & Hiscock, 1983 and Molfese & Betz, 1988 for comprehensive reviews). Results of numerous neuropsychological studies examining auditory or visual asymmetries in speech perception, coupled with investigations of asymmetries in the control and regulation of speech production (e.g., concurrent dual-task paradigm), further converge in demonstrating left hemispheric laterality for language in children as young as 3 years old (see Kinsbourne & Hiscock, 1983; Witelson, 1987; and Hiscock, 1988 for reviews). Furthermore, these studies suggest that the magnitude of functional cerebral asymmetry remains unchanged over development. While the research in neuroanatomy, psychophysiology, and behavioral asymmetries each have methodological limitations, the consistency in the finding of early left hemispheric specialization for language processes is compelling. What remains less clearly addressed in this area of research is the issue of whether there is a critical period in brain development during which environmental factors may impact and possibly alter the left cortical specialization for language regulation. The effects of sensory environmental stimulation on brain development have been studied more extensively in the visual as compared to the auditory sensory system. Animal research has suggested that there are visual cortex cells that do not develop without visual stimulation (Cummins, Livesey, Evans, & Walsh, 1979). Others have noted abnormal development of orientationspecific cells in the visual cortex of cats under conditions of visual deprivation (Hubel & Wiesel, 1963). While some investigators have examined the impact of auditory/linguistic deprivation at the cellular level on the growth of language-specific areas in the brain, others have examined the pattern of normal cortical maturation in Broca’s area. Mimer (1976) found that Broca’s area undergoes remarkable growth in neural connections and myelinization in the six cortical layers at different times during the first 3 years of life which parallels the period of rapid language acquisition and growth. Kesner and Baker (I 980) have noted a dramatic increase in dendritic arborization in Broca area neurons between 12 and 24 months, a period again noted for rapid language growth. Kyle (1978) has also suggested that there is a critical period for the development of the auditory cortex during which auditory stimulation is needed for normal cortical development to unfold. The interesting case study of Genie (Curtiss, 1977), a right-handed adolescent who endured 1I+ years of extreme social and experiential deprivation has also been cited as supporting evidence that environmental experience plays a role in functional brain organization. Neuropsychological tests administered upon her discovery revealed deviant brain organization, with right hemispheric lateralization of language skills and an apparent functional left hemispherectomy. One way to examine the hypothesis of a critical period in brain de-

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velopment during which environmental deprivation leads to atypical cerebral representation for language functions is to investigate cerebral lateralization patterns in profoundly deaf populations. Such studies serve not only to assist in the search for a possible critical period in brain development but also to potentially add to our limited knowledge about cognitive processes in the hearing impaired (Ross, 1983). Observation of atypical brain organization for speech in deaf populations would lend support to the critical period hypothesis. Furthermore, by examining patterns of cerebral specialization for speech in deaf populations that vary in age of onset of profound hearing loss, the precise time frame of the critical period of development may be delineated. Research investigating cerebral laterahzation patterns for language in deaf populations has followed two main paths. One area of research has examined brain organization for language in neurologically abnormal deaf individuals who have become sign aphasic. The other body of research has employed neuropsychological behavioral asymmetry paradigms to investigate cerebral laterahzation patterns in neurologically normal deaf subjects. The results and interpretations generated from both lines of research have produced quite contradictory findings. Both groups of researchers have often erred in viewing the deaf population as being homogeneous in nature, and in doing so have been limited by failing to examine for all potentially critical factors that may influence brain lateralization. Important contributing variables that have been investigated in educational and cognitive research, such as early linguistic experience and severity of hearing loss, have not always been adequately controlled or examined in these neuropsychological studies (Gibson, 1988). Rare clinical case studies of deaf aphasics have consistently reported disruption in signing abilities associated with left hemispheric damage in a way similar to the effect of such damage on speaking and language comprehension in hearing patients (see Bellugi, Poizner, & Klima, 1983 and Poizner, Klima, & Bellugi, 1987 for reviews). There are notable limitations to using the clinical case method to generalize about brainbehavioral relationships in neurologically intact populations based on the in-depth examination of a few neurologically abnormal patients (Kinsbourne & Hiscock, 1983). In addition, these reported cases cover a wide variety of deaf individuals who vary significantly in terms of age at hearing loss onset, etiology, severity of deafness, linguistic (auditory and/or signing) experiences in early development, as well as pretrauma signing fluency and the nature of their signing system. As a result, it is possible that different patients may have come to have their sign language controlled by the left hemisphere due to very different important processes or mechanisms. In contrast to the consistent finding of left hemispheric dominance for sign language in the case studies of aphasic deaf patients, the behavioral

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neuropsychological research has produced diverse and mixed findings, with the majority of studies reporting atypical lateralization patterns for neurologically intact deaf subjects (see Gibson, 1988 and Marcotte & LaBarba, 1987 for reviews). Most of these studies have involved tachistoscopic presentation to the left and right visual hemifields with a confounding variety of stimuli, including English words and numbers and static and nonstatic pictorial representations of American Sign Language. While hearing subjects consistently display left hemispheric advantages in t-scope studies using English stimuli, the deaf subjects have been reported to display bilateral representation (Manning, Goble, Markman, & LaBreche, 1977; Neville, Kutas, & Schmidt, 1982; Phippard, 1977; Poizner & Lane, 1979; Vargha-Khadem, 1983), a slight left hemispheric advantage (McKeever, Hoemann, Florian, VanDeventer, 1976; Panou & Sewell, 1984; Poizner, Battison, & Lane, 1979), as well as right hemispheric advantage (Kelly & Tomlinson-Keasey , 1977, I98 I ; Phippard, 1977) in different studies. Similarly varying laterality patterns have been reported using t-scope-presented sign language stimuli. The deaf have been reported to display no cerebral dominance for moving signs (Poizner et al., 1979; Vargha-Khadem, 1983). In contrast, the results with static sign include results suggestive of right hemispheric dominance (Poizner & Lane, 1979; Poizner et al., 1979), no asymmetry (Manning et al., 1977; McKeever et al., 1976), and left hemispheric lateralization (Panou & Sewell, 1984). Hearing subjects fluent in ASL have been reported to display right hemispheric processing of static signs (McKeever et al., 1976; Poizner & Lane, 1979). In addition to methodological variability, Gibson (1988) aptly points out that the subjects used in these r-scope studies varied greatly in terms of severity and etiology of hearing loss. She concludes that the variability in the results may be due to uncontrolled and unexamined critical variables, and by the fact that many deaf children have abnormal eye movement patterns, thus raising questions about the appropriateness of this technique with this population. Electrophysiological research with deaf subjects has been more limited than behavioral asymmetry research. Using a t-scope paradigm involving recognizing English words in visual hemifields with concurrent eventrelated potential recordings being measured, Neville et al. (1982) reported that the congenitally deaf adults did not display visual field asymmetries, and had ERPs that differed from those observed in hearing adults. In particular, the deaf subjects did not display the negative (410 msec)positive shift prominent in the left hemisphere of hearing subjects, suggesting that the deaf have different patterns of cerebral organization for language-related activities. Tactile behavioral asymmetry studies (see Gibson, 1988 for review) and the dual-task paradigm avoid some of the problems associated with tachistoscopic research, and the majority of these limited number of

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studies have suggested that the deaf perform differently from hearing subjects on these tasks and have atypical brain organization for language processes. To date, three studies have been reported in the literature utilizing the concurrent dual-task paradigm to determine speech production lateralization patterns in deaf populations (Ashton & Beasley, 1982; Marcotte & LaBarba, 1985, 1987). While sign language is primarily used by the deaf to communicate, speech nevertheless is a component of Total Communication (signing, speech, and lip reading), the system of communication emphasized in almost all educational settings for the hearing impaired. The dual-task method requires minimal speech performance, and in two studies (Marcotte & LaBarba, 1985, 1987) the speech stimuli were specifically selected by educators of the deaf for ease of production in 5- to 6-year-old hearing-impaired children. All three of these studies reported atypical, anomalous brain representation for speech production, with relatively more right hemispheric involvement among congenitally deaf subjects with profound bilateral hearing loss. These findings suggest that environmental deprivation throughout development associated with profound hearing loss can lead to cortical reorganization of certain language-specific functions. Only one study to date has attempted to isolate a critical period in development when environmental stimulation is essential to actualize the left hemispheric bias for regulating speech. Using the dual-task method, Marcotte and LaBarba (1987) examined lateralization patterns in deaf individuals who had acquired a severe to profound bilateral hearing loss between 2 and 36 months of age. As a group, the acquired hearing loss subjects displayed atypical lateralization patterns. Hearing loss onset from birth to 24 months of age resulted in the same anomalous, more bilateral cerebral representation for speech comparable to that reported for congenitally deaf populations. Those subjects with hearing loss incurred during the third year of life displayed mixed cerebral dominance dependent on the linguistic complexity of the speech task. As such, this study suggested that environmental deprivation associated with hearing loss at any point in the first three years of life can result in cerebral reorganization of speech functions. This study failed, however, to isolate the endpoint of such a critical period after which interruption of environmental stimulation does not alter left cerebral specialization for speech. The present study was designed as an attempt to isolate a critical period in development during which environmental deprivation associated with profound hearing loss leads to cortical reorganization and alteration of the typical pattern of left hemispheric specialization for speech production. The approach used to examine this problem involved a comparative analysis of laterality patterns for speech production among a population of congenitally deaf and one with profound acquired hearing

SPEECH

LATERALITY

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TABLE SUMMARY

OF SUBJECTS’ CHARACTERISTICS:

Group

Group n

139

I

GENDER AND AGE BY HEARING

No. of males

No. of females

Normal hearing Congenitally deaf Acquired hearing loss

16 22 I9

IO II I4

6 II 5

Total

57

35

22

STATUS GROUP

Average age in years 16.18 16.73 16.89

losses incurred in the first 5 years of life, and therefore with histories of differential linguistic/auditory exposure and experience. This study further served to examine the reliability of the findings of Marcotte and LaBarba (1987), the first reported study examining cerebral laterality patterns in acquired hearing loss subjects using the time-sharing paradigm. Based upon previous neurological research in the development of Broca’s area in the left cerebral hemisphere (e.g., Milner, 1976; Kesner & Baker, 1980), it was hypothesized that environmental deprivation associated with deafness incurred during the first 3 years of life would result in alteration of the typical pattern of brain organization for speech control. Specifically, it was hypothesized that subjects with profound congenital deafness or deafness with onset between birth to 36 months of age would display atypical anomalous cerebral representation for speech as compared to normal hearing controls. Likewise, it was hypothesized that deafness acquired after 36 months of age would not alter left hemispheric dominance for speech, and that these subjects would resemble normal hearing controls in brain organization. Thus, a critical period in which environmental deprivation would disrupt normal left cerebral lateralization for speech was hypothesized to span the early developmental period up to approximately 36 months of age. METHOD Subjects Fifty-seven adolescents between the ages of 13 and 20 served as subjects in this study. Subjects were assigned to one of three groups on the basis of hearing status: normal hearing (n = l6), congenitally deaf (n = 22), and deafness acquired after birth up to 5 years of age (n = 19). This latter group was further divided into early and later childhood hearing losses on the basis of documented age at onset of hearing loss. Distribution of subject sex and average age by group is summarized in Table I. All subjects were right-handed as behaviorally assessed by the Edinburgh Handedness Inventory (Oldfield, 1971). To qualify for participation, all subjects had to write with their right hand and perform no more than two other behavioral tasks (use scissors, draw a circle, use a spoon, throw a ball, sweep, open a box, or use a toothbrush) with their left

140

MARCO’I-TE AND MORERE TABLE 2 ETIOLOGICAL FACTORSOF HEARING Loss FOR ALL CONGENITALLY DEAF SUBJECTS

Identified etiology Hereditary deafness Maternal rubella Maternal measles

No. of subjects

Percentage of group

12 7 3

55% 32% 13%

hand. Adolescents with multiple handicaps and/or neurological impairment beyond sensorineural hearing loss as determined by review of medical and academic records were excluded from this study. All hearing-impaired subjects were students at the Alabama Institute for the Deaf and Blind, and used a Total Communication system (finger spelling, gestural signing, and oral speech). These deaf subjects all had documented hearing losses in the profound range in both ears (hearing loss of 90 dB or greater). Congenital deafness was defined as medically diagnosed deafness present at birth. Only congenitally deaf adolescents with documented causes for deafness were used in this study; this etiological information is summarized in Table 2. Similarly, only those subjects with acquired hearing losses of known etiology and age at onset were used in this experiment. Subjects with hearing loss due to head injury or exposure to explosions were excluded from this study because of suspected neurological complications. Descriptive data for the acquired hearing loss subjects are summarized in Table 3.

Apparatus Finger tapping was recorded using a standard telegraphic key mounted on a wooden base and connected to a BSR Foeringer Counter (Model CP-901), which was activated by a Tenor timer (Model TI-902) set for I5 sec. The counter was read at the end of each trial and reset. Each subject’s utterances in all dual-task and vocalization-only trials were tape recorded for later independent analysis.

Design The independent variables examined in this study were as follows: one between-subjects variable, hearing status (normal hearing, congenitally deaf, acquired deafness with early developmental onset, acquired deafness with later developmental onset), and two withinsubjects variables, task condition (no verbal task, Verbal Task I, Verbal Task 2, Verbal Task 3) and hand used (right, left, or no hand). In the first phase of the study, the dependent variable was the number of utterances/words produced in 15 set, whereas in the second phase of the study the dependent variable was the number of taps provided in a l5-set time interval. Each subject participated in II experimental trials, yielding repeated measures along both dependent variables. The overall study design was therefore a 4 x 4 x 3 mixed model, repeated measures analysis of variance (ANOVA). Individual hypotheses were tested using variables of this design.

Procedure The procedures used in this study were similar to those reported by Marcotte and LaBarba (1987). Each subject was tested individually by an adult experimenter. Deaf

SPEECH

LATERALITY TABLE

ETIOLOGY,

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IN THE DEAF 3

AGE AT HEARING Loss ONSET, AND GENDER FOR ALL ACQUIRED HEARING Loss SUBJECTS

Assigned subject No.

Gender

43 44 45 4x 53 54 57 61 62 63 67 69 70 71 76 81 82 x3 84

M M M M M M M F F M M M M F F M M M M

Age at onset (months) 6 6 6 9.5 10

12 15 16 17 19 24 24 24 36 39 40 50 60

Identified

etiology

High fever Meningitis Ear infection Meningitis Measles/High fever Meningitis Meningitis Pneumonia High fever Meningitis Meningitis Meningitis Meningitis Meningitis Measles Dehydration High fever Meningitis Meningitis

subjects were also signed to by a certified American Sign Language interpreter. Subjects were first screened for handedness, and only those identified as right-handed by the Edinburgh Handedness Inventory (Oldfield, 1971) were selected for participation in the study. Subjects were told that the purpose of the test was to “see how fast you can tap” and “to see how fast you can do two things at once.” The experimenter then sat down next to the subject and demonstrated how to tap on the telegraph key with an index finger. Each subject was then given approximately 5 set to practice tapping with each index finger. During this initial practice session, the experimenter made certain that the subject was applying only the index finger to the key, and that sufficient pressure was applied to record the taps on the automatic counter. There were I I experimental conditions involving tapping and/or vocalizations. Each subject performed one 15.set trial of each of these conditions. The experimental conditions were as follows: I. Right-hand control (RC): tapping without verbalization 2. Left-hand control (LC) 3. RH tapping with verbal condition I: “ba-ba” (RVI) 4. LH tapping with verbal condition I: (LVI) 5. RH tapping with verbal condition 2: “cat-dog-horse” (RV2) 6. LH tapping with verbal condition 2 (LV2) 7. RH tapping with verbal condition 3: “how are you” (RV3) 8. LH tapping with verbal condition 3 (LV3) 9. Verbal Condition I without tapping (VI) IO. Verbal Condition 2 without tapping (V2) I I. Verbal Condition 3 without tapping (V3)

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Half of the subjects in each group performed the tasks in the order LC, RVl, RV2, RV3, V3, V2, VI, LV3, LV2, LVI, and RC. The other half performed the tasks in the reverse order to counterbalance for possible task order effects. Before each trial, subjects were told what the forthcoming task involved. Subjects were then permitted to practice this task to ensure that the instructions were understood, and that the subject was able to perform the task. Once the experimenter was assured that the subject could perform the task, the experimental trial was run. Subjects were then asked to tap and/or repeat the verbal material as rapidly as possible from the time the experimenter said “Go,” and tapped the subject on the arm not involved in tapping, until the experimenter said “Stop,” and tapped the subject on the arm again. The subject’s index finger was positioned on the telegraphic key prior to those trials involving tapping. This series of task presentation and practice, followed by the running of the experimental trial, were repeated until all I I experimental conditions were completed for each subject. The average time to completion of all experimental conditions for each subject was approximately I5 min.

RESULTS Because of possible violation of the assumption of homogeneity of covariance given the repeated measures design of this study, conservative Greenhouse-Geisser-adjusted degrees of freedom (Greenhouse & Geisser, 1959) were used in ANOVA data analyses as suggested by Myers (1979). All post hoc tests employed Tukey’s (1953) Honestly Significance Difference (HSD) procedure ((Y = .05). Analysis of Utterance Data Four judges independently counted the number of utterances emitted in each of the experimental trials involving speech production for each subject. Two judges counted the utterances of the hearing subjects, while two other judges counted the utterances of all hearing-impaired subjects. Based on these ratings, the mean number of words emitted in each verbal trial was calculated for each subject. These utterance means are reported in Table 4. A 3 (hearing status: normal, congenitally deaf, and acquired hearing loss) x 3 (task: Vl, V2, V3) x 3 (hand employed: R, L, no hand) ANOVA was performed across all subjects using the mean number of utterances produced in 15 set as the dependent variable in order to determine possible speech production interference in this dual-task paradigm. There was a main effect for hearing status (F(2, 52) = 8.47, p < .OOl) and task (F(2, 86) = 134.12, p < .OOOl).Post hoc Tukey tests revealed that hearing subjects produced more mean utterances (X = 67.1) than did the congenitally deaf (a = 50.3) and acquired deaf groups (X = 54.2). In the task conditions, subjects overall produced significantly fewer utterances (HSD = 1.98) in the V2 condition, “cat-dog-horse” (X = 44.9), than in the VI condition, “ba-ba” (I%= 6&O), and V3 condition, “how are you” (X = 56.6). The two-way interaction between hearing

Hearing Congenitally deaf Acquired deaf

Hearing Congenitally deaf Acquired deaf

71.9 62.7 68.7

71.1

65.5

68.4

72.2

66.0

67.9

L

41.2

37.0

57. I

-

44.1

38.4

57.2

R

V2: “Cat-dog-horse”

42.4

36.5

58. I

No hand

52.2

50.4

71.2

L

R

81.3 69.3 68. I

L

73.6 60.1 63.9

VI: “Ba-ba”

70.1 49.8 52.9

L

V2: “Cat-doghorse”

81.3 54.7 60.4

R

71.5 56.6 56.7

L

V3: “How you”

R

-

83.1 60.8 64.8

are

TABLE 5 MEAN NUMRER OF TAPS PRODUCEDIN I5 SEC AS A FUNCTION OF GROUP, TASK, AND HAND

No hand

L

R

V I : “Ba-ha”

50.8

50.4

72.4

97.8 79.1 83.6

R

No hand

No vocal task

are you”

75.8 72.2 71.4

L

52.4

41.4

12.1

R

V3: “How

TABLE 4 MEAN NUMBER OF UIWRANO.S PRODLKED IN 15 S.W AS A FUNCTION OF GROUP. TASK, AND HAND

6

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status and task was also significant (F(3, 86) = 8.32, p < .OOl). Of importance in interpreting results generated by the dual-task paradigm, there was no main effect for hand (F(2, 94) = 0.29, p > .05) indicating no significant changes in the rate of utterance production when the concurrent tapping component was added. Furthermore, there were no significant interactions between hearing status and hand employed (F(4, 94) = 0.67, p > .05), or between hearing status, hand, and task (F(6, 153) = 1.0, p > .05). As these results suggest that utterance production was not selectively interfered with in this dual-task study for any of the subject groups, all subsequent analyses of the dual-task data and lateralization interpretations used the mean number of taps produced in 15 set as the dependent variable. Analysis

of Tapping Data: Lateralization

Patterns

To determine the cerebral lateralization patterns for speech control and regulation across subjects, a 3 (hearing status: normal, congenitally deaf, acquired deafness) x 4 (task: no verbal task, VI, V2, V3) x 2 (hand: right, left) repeated measures ANOVA was performed using the mean number of taps produced in 15 set as the dependent variable. These means are reported in Table 5. In this initial analysis, all acquired hearing loss subjects remained grouped together. This analysis yielded significant main effects for hand (F(1, 54) = 55.22, p < .OOl), task (F(3, 144) = 113.15, p < .OOl), and group (F(2, 54) = 15.19, p < .OOl). Across subjects, right-hand tapping (Z = 72.63) was, as would be expected, significantly faster than lefthand tapping (X = 63.86). Among groups (HSD = 2.5), hearing subjects (X = 79.3) tapped faster overall than did the congenitally deaf group (X = 62.8) and the acquired hearing loss group (X = 65.2). There were significant declines in tapping (HSD = 2.5) from baseline tapping without vocalization (X = 79.4) with all three concurrent vocalization tasks (VI 55 = 68.7; V2 K = 60.3; V3 x = 64.6). A series of significant two-way interactions was also found: task by group (F(5, 144) = 5.07, p < .OOl), and task by hand (F(3, 154) = 6.99, p < .Ol). Of importance for interpreting patterns of lateralization, the three-way interaction effect between group, task, and hand reached significance (F(6, 154) = 2.3, p < .05). For the hearing subjects, there were significant drops in the rate of right-hand tapping with all three concurrent vocalization tasks (HSD = 6.62). There was, however, no significant difference in the rate of left-hand tapping under dual-task conditions. This pattern of right but not left-hand declines in the rate of tapping in dual-task trials is interpreted as evidence of left cerebral hemispheric control of speech in the hearing group. These findings are consistent with earlier reports. The congenitally deaf group demonstrated significant declines from

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base rate in both left- and right-hand tapping during concurrent vocalization (HSD = 6.08), suggesting more anomalous brain organization with greater right cerebral hemispheric involvement in speech regulation than seen in the normal hearing group. The observation of atypical, anomalous, more bilateral representation among the congenitally deaf replicates previous findings (Marcotte & LaBarba, 1985, 1987), lending further support to the hypothesis that early exposure to environmental stimulation may play a critical role in how the brain ultimately becomes organized for speech regulation. The patterns of tapping suppression across all acquired hearing loss subjects were identical to those reported for the congenitally deaf. That is, this group also displayed significant suppression (HSD = 5.65) of both right- and left-hand tapping from baseline in the three dual-task conditions, again suggesting atypical brain organization for speech production for this acquired hearing loss group. These results replicate those reported by Marcotte and LaBarba (1987). Anulysis

of Tapping Data: Effect of Age of Onset

In addition to validating previously reported findings of an atypical, more symmetrical brain organization for speech among the prelingually hearing impaired, this study further hypothesized a critical period in development from birth up to 36 months of age during which environmental stimulation is required to “actualize” the left hemispheric potential for the control of speech production. Previous attempts failed to isolate such a critical period of development when cerebral lateralization patterns were examined in adolescents with hearing loss incurred between birth and 3 years of age (Marcotte & LaBarba, 1987). The current study examined brain control for speech production in adolescents with deafness incurred over a wider span of development, namely postbirth to 5 years of age. A subsequent ANOVA test was performed in which this acquired hearing loss group was subdivided into an early age of onset (onset birth to 36 months) and later onset (37 to 60 months) in order to examine for the hypothesized critical period. While this later onset acquired hearing loss group comprised only four male subjects, it was believed that this analysis might reveal preliminary evidence for a critical period in brain development. Given this small sample size and all male constitution of this group, the following results should be tempered by these facts. This ANOVA yielded significant main effects for hearing status (F(3, 53) = 9.95, p < .OOl), task (F(3, 142) = 73.57, p < .OOl), and hand (F(1, 53) = 26.58, p < .OOl), and significant two-way interactions, task x hearing status (F(8, 142) = 3.7, p < .OOl) and hand x task (F(3, 150) = 4.86, p < .05). The task x hand x hearing status interaction also reached significance (F(8, 150) = 2.77, p < .05). In this analysis, subjects with

146

MARCOTTEANDMORERE

hearing losses incurred between birth and 36 months of age displayed significant suppressions in both right- and left-hand tapping across all concurrent tasks (HSD = 6.7). Those subjects with acquired hearing loss onset after 3 years of age had cerebral lateralization patterns for speech regulation that were the same as those observed in the normal hearing group. That is, subjects with acquired deafness incurred after 3 years of age demonstrated left cerebral dominance for speech as witnessed by their pattern of significant suppression in only right-hand tapping from base rate across all verbal tasks (HSD = 12.95). Despite the limitations of this analysis due to the small sample size of the later acquired hearing loss group, these findings begin to support the suggestion that there is a critical period of development during which environmental exposure plays a key role in the ultimate brain organization for speech control and regulation. Namely, these data suggest that this critical period spans the first 3 years of life. Interruption of environmental stimulation associated with hearing during this period will lead to an alteration in the “prewired” left cerebral dominance for speech, resulting in greater right hemispheric involvement in this process than would be normally expected. Frequency

Analysis

of Lateralization

Data for Deaf Groups

Hiscock and Kinsbourne (1978) have proposed that frequency analyses of group data are a useful alternative to ANOVA analyses in observing laterality trends. This approach involves calculating the proportion of subjects in various groups displaying different lateralization patterns. Such a process first involves the determination of lateralization based on suppression in tapping rate patterns for each subject. Various researchers (e.g., Hiscock & Kinsbourne, 1978; Orsini, Satz, Soper, & Light, 1985) have proposed interpretation rules for determining whether a subject’s dual-task performance is indicative of right or left cerebral dominance. These decision rules are limited in that they allow only for two possible laterality outcomes. This and other studies have suggested there is a possible third brain organizational pattern for speech, namely, an anomalous, more bilateral representation. As such, the frequency data analysis of lateralization patterns in this study followed interpretative guidelines described by Marcotte and LaBarba (1987) that provide rules for determining left, right, or atypical/symmetrical patterns of lateralization. First, the average percentage amount of tapping suppression in each hand for every subject during concurrent vocalization tasks is calculated. If the difference score in tapping suppression (percentage reduction in righthand tapping minus percentage reduction in left-hand tapping) is equal to or falls between - 6 and + 6, the subject is classified as less completely lateralized or more bilaterally represented for speech production. A dif-

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IN THE DEAF

TABLE 6 SUMMARY OF THE NUMBER AND PERCENTAGEOF SUBJECTSDISPLAYING LEFT, RIGHT, OR BILATERAL REPRESENTATIONBASED ON FREQUENCY DATA FOR EACH HEARING STATUS GROUP Interpreted Left

Normal

hearing

(n = 16) Congenitally

deaf

(n = 22) Acquired deaf onset

hemispheric dominance

lateralization Right hemispheric dominance

pattern Bilateral representation

14 (88%)

0 ( 0%)

2 (12%)

7 (32%)

7 (32%)

8 (36%)

5 (33%)

4 (27%)

6 (40%)

4 (100%)

0 ( 0%)

0 (

6-36 months (n = Acquired 39-60

IS) deaf onset

0%)

months

(t1 = 4)

ference score of less than -6 is interpreted as right hemispheric dominance, and greater than + 6, left hemispheric dominance. The percentage of subjects in each hearing status group displaying right, left, or atypical representation for speech regulation as interpreted by difference scores is shown in Table 6. x2 analysis and subsequent examination of trends in the frequency data analysis of the various hearing status groups lends support to the previously reported ANOVA findings, and to the critical period hypothesis. A xZ test of association (x2 = 16.81, u” = 6, p < .Ol) revealed a significant relationship between hearing status and lateralization patterns. The frequency data suggest that age at hearing loss onset is a critical factor in determining ultimate brain organization for speech observed in this population. Generally, earlier developmental environmental deprivation due to profound bilateral hearing loss is associated with atypical, more symmetrical brain representation for speech, involving more of the right cerebral hemisphere than is observed in the normal hearing. Sixtyeight percent of the congenitally deaf subjects displayed atypical [either right cerebral dominance (32%) or bilateral representation (36%)] brain organization for speech regulation. Similarly, 67% of subjects with hearing loss onset between 6 and 36 months of age displayed comparable atypical [right cerebral dominance (27%), bilateral representation (400/o)] brain organization for speech. In contrast, all subjects with deafness incurred at or after 36 months of age displayed left cerebral hemispheric lateralization for speech, and resembled the normal hearing group (88% left hemispheric dominant) more so than either of the two other hearing impaired groups.

148

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DISCUSSION

The results of this study, using both analysis of variance and frequency data approaches, begin to lend support to the hypothesis that a critical developmental period may exist during which environmental deprivation is associated with cortical reorganization of the normal left hemispheric specialization for speech regulation. Specifically, this study suggests that this critical period may span the period between birth to approximately 36 months of age. A profound bilateral hearing loss at birth and one incurred between birth and 36 months of age were observed in this experiment to be associated with atypical, anomalous, more bilateral pattern of cerebral representation for speech, with greater right hemispheric involvement than is observed in hearing populations. A profound hearing impairment incurred after 36 months of age, however, was found not to be related to deviation from the typical pattern of left cerebral dominance for speech. Thus, while there is compelling research evidence to suggest a bias for left cerebral specialization for speech processes at birth, the results of this study nevertheless suggest that there appears to be a crucial span of time in early development during which this cortical representation can be altered; specifically, under conditions of environmental deprivation. Given our small limited sample of adolescents with acquired hearing loss incurred after 36 months of age who met all of the study’s inclusion criteria, these findings should be viewed as being preliminary in nature. Further study of individuals with later life onset of profound deafness is needed to verify the existence of a critical period in brain development as suggested in this study. The question remains to be answered, however, as to what specific aspect of environmental experience in early development is the causative factor leading to altered cortical organization in select deaf populations. Phrased another way, is it auditory sensory stimulation or linguistic exposure and experience that is critical in actualizing the left hemisphere’s dominance for the control and regulation of language functions? In their work with sign aphasic deaf adults, all of whom suffered left hemisphere strokes, Poizner et al. (1987) conclude that it is early linguistic experience rather than hearing and oral speech that is necessary for the left hemispheric specialization of language to unfold. While all three of their patients were profoundly deaf, had attended deaf residential schools, and were members of the deaf community, they varied in the nature of the acquisition of their deafness. One parent (G.D.) was born deaf and had deaf siblings while a second (K.L.) had acquired profound deafness at 6 months of age, but had used sign language throughout most of her life. The third patient (P.D.), however, had hearing and presumably normal oral language experiences and exposure until 5 years of age. At that age, he subsequently acquired profound hearing loss and has used

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sign language as his major form of communication from that time on. Despite the differences in the form of their early linguistic experiences (e.g., sign versus oral speech) all three patients nevertheless had, according to Poizner et al. (1987), adequate linguistic experiences to actualize the left hemisphere’s potential for language regulation. Most of the other case studies reported in the literature of sign aphasic deaf individuals with left hemispheric damage also represent individuals either who were congenitally deaf but who signed throughout their lives, or who had adequate hearing and thus auditory language experiences in the early critical years of brain development. The major focus of this study, as is true of most neuropsychological behavior research with deaf populations, was on auditory sensory experiences rather than linguistic experiences per se. When examined for age at hearing loss onset, subjects in this study showed patterns of atypical brain organization for speech associated with deafness incurred at birth up to 3 years of age, but left hemispheric dominance for speech with hearing loss incurred after 3 years of age. Confounded in this approach, however, are the varying linguistic experiences each subject had both prior to and after the onset of deafness. Related to this, it is important to note that there was variability in the patterns of laterality observed within each of the deaf subgroups examined in this study as highlighted by review of Table 6. Might this variability reflect varying linguistic experiences during this apparent critical period reflected in the findings of this study? Post hoc examination of this study’s data lends only partial support to this hypothesis. For example, all I2 of the congenitally deaf subjects with hereditary deafness had been raised in deaf households and had been exposed to a signing linguistic environment throughout their lives. Examination of each subject’s patterns of brain organization for speech regulation, however, reveals that only 42% of these subjects had left hemispheric dominance for speech. If, as Poizner et al. (1987) conclude, it is linguistic experience that actualizes the left hemisphere’s control of language functions, one would have expected 100% of this group to show this normal pattern of lateralization. On the other hand, all of the subjects who acquired deafness at or after 36 months of age, who had had adequate exposure and experience with, in this case, an auditory linguistic environment, displayed typical left hemispheric lateralization for speech. To better address this issue, well-designed, behavioral neuropsychological research designed to dissociate the influences of auditory sensory from linguistic experience in deaf populations is needed. This could be accomplished, for example, using the dual-task paradigm with comparison groups of congenital profoundly deaf subjects who vary in linguistic experiences (e.g., compare lateralization patterns for subjects who had linguistic experiences in the first 3 years of life to those deaf children

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who lacked these experiences). Such a study would allow for examination of the effects of linguistic experience on brain organization independent of auditory sensory stimulation. Careful dissociation of auditory and linguistic experiences might further reveal that each of these components of early developmental stimulation may impact neuropsychological functioning in different ways. While Poizner et al. (1987) contend that linguistic experiences are critical in determining lateralization patterns for language, others have proposed that early auditory experiences, particularly experience with the temporal sequential nature of an oral speech environment, influences cognitive information processing abilities. Craig and Gordon (1988) report that congenital profoundly deaf adolescents display relative impairments in sequential information-processing skills, but above average simultaneous information-processing abilities compared to hearing peers. They contend that it is these deaf children’s lack of auditory experiences coupled with the more simultaneous nature of ASL (as compared to the more sequential nature of spoken language) that accounts for these findings. In a similar vein, normal hearing adults raised in deaf households who learned sign language as their first language had equivalent performance on sequential information-processing tasks as nonsigning hearing adults, while congenitally deaf adults displayed impaired sequential performance (McKee & Gordon, 1987). This finding suggests that early auditory experiences may play a role in the development of adequate sequentialprocessing skills. In summary, the results of this study suggest the presence of a sensitive period in the first 3 years of life that parallels the myelinization of Broca’s area (Mimer, 1976) during which environmental deprivation associated with profound hearing loss alters the normal left hemispheric lateralization of speech. Whether the precise component of this early environmental deprivation leading to cortical reorganization is auditory or linguistic in nature remains unsolved. Carefully designed studies in which auditory and linguistic experiences can be dissociated will be required to resolve this issue, and to further clarify the nature of the critical period in brain development. The limited number of hearing-impaired subjects in this study, particularly those with hearing loss incurred postlingually, speaks to the challenge of conducting well-controlled investigations with this population. REFERENCES Ashton,

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