International Journal of Pediatric Otorhinolaryngology, @ Elsevier/North-Holland Biomedical Press
1 (1979) 13-24
13
Review Articles BRAIN FUNCTION
AND LANGUAGE
DISABILITIES
*
PEGGY C. FERRY, JAN L. CULBERTSON, PATRICIA M. FITZGIBBONS MARTIN G. NETSKY
and
Department of Pediatrics and Neurology, University of Arizona Health Sciences Center, Tucson, Ark. 85724 and Departments of Pediatrics and Pathology, Vanderbilt Uniuersity School of Medicine, Nashville, Tenn. 37232 (U.S.A.) (Received December 8th, 1978) (Accepted May lst, 1979)
INTRODUCTION
Children with normal intelligence, but with specific learning disabilities, are being recognized with increasing frequency. In a survey in 1976, there were almost 2 million children with learning disabilities in the United States, 87% of them not receiving special educational services [ 61. A recent survey by the American Academy of Pediatrics showed that 15% of mothers reported some type of learning difficulty in their children, and that almost half sought advice from their physician about the problem [9]. Recent federal legislation, Public Law 94-142, mandates that learning-disabled children receive free appropriate public education designed for their specific needs [ 51. This law has resulted in identification and referral of increased numbers of such children. In the past decade, studies on neurologic, cognitive, and linguistic development in children have shown increasing evidence of cerebral hemispheric specialization, and differential rates of brain maturation between sexes. In this review, information will be provided about: (1) normal brain development, and (2) the neurologic substrates of language and learning disabilities, to enable the physician to participate in planning rational educational programs. NORMAL BRAIN DEVELOPMENT
(1) Anatomic
and physiologic
development
During intrauterine life, the brain is the largest organ in the body. It constitutes 15% of body weight during most of the 40 weeks of gestation. This fact highlights a major feature to be emphasized: the brain is precocious, its * Presented in part at the SENTAC Annual Meeting, Santa Barbara, Calif., December 7th, 1978.
14
major anatomic structures being well formed by the tenth week of fetal life [3]. This observation is often overlooked in consideration of critical periods, plasticity, and later developmental events. The first gross evidence of the nervous system arises about 3 weeks after conception with the formation of the neural groove. This structure evolves into the neural tube, closure occurring between 21 and 25 days. By the end of the third week, the CNS has divided into 3 major subdivisions: prosencephalon, mesencephalon, and rhombencephalon. Reflex physiologic circuits are active after 5.5 weeks [25]. The circle of Willis is completed by 6.5 weeks. At 7 weeks, the principle aural structures are formed, and spontaneous electroencephalographic (EEG) activity can be recorded. Five subdivisions are delineated by 8 weeks, with the cerebral hemispheres clearly evident. Rapid telencephalic growth is characteristic of the period from 8 to 12 weeks. Externally, the fetus at this stage resembles the human infant. An eye-blink reflex can be obtained at 10 weeks, and patellar reflexes have been observed in a 12-week fetus [ 191. The sylvian fissure develops at 14 weeks gestation, and additional fissures and gyri develop in predictable sequence until birth. The gyral configuration of the brain is a reliable guide to gestational age [ 41. Myelination begins around 20 weeks. The visual pathway is structurally complete by 28 weeks, from the optic disc to the occipital lobe. After this time, the cortex forms into 6 distinct layers. Pupillary reflexes can be obtained at 27-29 weeks [ 251. Different parts of the brain grow at different rates. The medulla-pons region is largest up to 7 weeks, then becomes proportionately smaller at 18 weeks. The telencephalon is smaller at 4 weeks, but by 8 weeks it is growing more rapidly than all other parts of the brain. It stabilizes at about 90% of total brain weight in the 16th week of gestation. The cerebellum has two spurts in growth, one at about 8 weeks of intrauterine life, and the other in the first year after birth. The majority of neurons in the adult brain are formed early, perhaps by 18 weeks gestation [ 171. The onset of synaptogenesis differs regionally, but has been noted as early as 8.5 weeks gestation. Radioautography has shown that “waves” of neuroblasts migrate through pre-existing layers of the brain to form the final 6 layers of the cortex. Evidence suggests that specific spatial and temporal sequencing of synaptic development occurs from 8.5 to 24 weeks. After 23 weeks, the number of synaptic connections increases from lo- to 80-fold [3]. Myelination begins in the fourth month of gestation and continues in an orderly sequence into the fifth and sixth decades of postnatal life [3]. Yakovlev has shown that specific pathways in the brain myelinate at widely different times, following phylogeneticaIly logical temporal and spatial patterns. In general, the older systems myelinate first, proceeding in a caudo-cephalic direction, then the pyramidal tracts (completed during the second year of life), and association fibers (continuing well into adult life).
15
(2) “Critical” periods The concept of various critical periods in neurologic development has been proposed to indicate finite times in which specific events must occur to provide the substrate for subsequent developmental achievements [ 231. This “now-or-never” hypothesis is based upon imprinting studies in animals and psychologic studies of sensorimotor development leading to cognitive skills in children. More recently, however, the concept has been challenged. Wolff, in 1970, suggested that child behavior depends upon the complex interaction of many biologic and environmental factors. The concept of “sensitive” periods has been proposed as an alternative, referring to periods when a child may learn particular skills more easily than others [ 381. Based on the early precocity of brain development and the highly complex interaction between neurogenesis, synaptogenesis, and myelination as described, all phases of early brain development are critical. The most important (if not critical) period of neurologic development is the first 10 weeks of intrauterine life, when the anatomic, physiologic, and biochemical substrates of future developmental progress are being formed. HEMISPHERIC ASYMMETRY
AND SPECIALIZATION
During the past century, increasing evidence has accumulated of a division of labor between the two sides of the brain. The cerebral hemispheres are asymmetric and clearly specialized for different cognitive and linguistic functions [34]. In gross anatomic appearance, the left and right halves of the brain are not identical. The left sylvian fissure is significantly longer than the right in most adult and infant human brains [26]. The superior surface of the posterior temporal lobe is longer on the left. The angular gyms is smaller on the left. The left planum tempo&e, the portion of the temporal lobe involved in language comprehension, is distinctly larger than the right. This asymmetry is clearly evident at birth as well as in fetuses as early as 29 weeks gestation, and suggests that the substrate for language development in the left cerebral hemisphere is present well before birth [32]. Evoked response and dichotic listening studies in newborn infants have shown left hemisphere specialization for speech sounds [ 71. Infants in the first week of life keep their heads turned preferentially to the right 90% of the time [30]. This head-right bias increases with conceptual age, from 64% at 33-35 weeks to 96% at 39 weeks. The right hemisphere is specialized for musical notes in the first week of life [14]. Hemispheric specialization continues to develop throughout childhood. Motor performance tests in children as young as 3 years of age indicate right hemisphere specialization for non-sequential, spatial control of hand movements [ 201. Bight hemisphere specialization for visually presented stimuli is
16
evident in normal children by the age of 6 years [ 111. Development of left hemisphere specialization for mediating language functions is complete by about 5 years of age [18]. Witelson has summarized the current evidence about hemispheric specialization: (1) the left hemisphere processes stimuli in a linguistic, sequential, analytic manner to form the basis of receptive and expressive language; and (2) the right hemisphere uses a synthetic or holistic approach [34]. These differences are not absolute, in that each side is able to execute some functions of the other to some extent, SEX DIFFERENCES
IN BRAIN FUNCTION
Along with the differences in functional capabilities between the two hemispheres, there are sex differences in cerebral organization and function. Sexual differentiation of the brain is similar to the reproductive system: the brain is inherently female, and, if not exposed to androgenic hormones during development, it remains so [35]. Exposure to testicular androgen converts the ontogenetically female brain into a “male” brain, with differing functional neuronal mechanisms. In general, girls acquire language earlier than boys, have lower touch and pain thresholds, and have better sound discrimination abilities. Boys have better visuospatial abilities, greater muscular development, and more precision in aiming and throwing [ 161. Boys show right hemisphere specialization for spatial processing as early as age 6 years, but girls maintain bilateral representation until age 13 1351. Morphologic asymmetry between left and right temporal lobes is more evident in females earlier in ontogeny than males, suggesting again a preprogrammed neural substrate for earlier language development in girls [ 361. Epidemiologic evidence shows that certain neurologic disorders are far more common in boys than girls: autistic behavior, some forms of cerebral palsy, reading disabilities, and language disorders are 2-8 times more frequent in boys than in girls [lo]. Primate studies have shown that brain lesions in infant monkeys produced significantly more sequelae in males than females. Male and female rats responded in opposite manner to psychotropic drugs given in the neonatal period; early drug administration abolished the expected normal sexual differences in behavior [ 81. Studies on adults with unilateral brain damage showed that 3 times more men than women with left hemisphere lesions became aphasic [22]. Only men continued to show the expected pattern of depressed verbal intelligence and verbal memory after left hemisphere damage as compared to men with right hemisphere damage. Women, as a group, had a more heterogenous pattern of cerebral speech representation than did men. Studies of children with temporal lobe epilepsy showed differences between the left and right hemispheres, and between sexes [29]. Left-sided
17
seizures occurred more frequently before age 2, but right-sided lesions were equally prevalent during the first 4 years of life. The inception rate of seizures in boys fell away smoothly with increasing age, but girls had a more precipitate fall. LANGUAGE DEVELOPMENT,
READING ABILITY, AND DYSLEXIA
Increasing evidence has accumulated in the past decade that language impairment forms the substrate for many reading problems [28]. A study of 113 dyslexic children has shown that 39% had poor receptive and expressive language abilities [ 211. A study of 30 learning-disabled adolescents revealed that they had significantly more difficulty with linguistic processing, cognitive-semantic processing, and retrieval of verbal labels, verbal associations, and syntactic structures than a matched control group [33]. Studies of hemispheric specialization have been performed in a large group of dyslexic children [ 371. The left hemisphere was the major hemisphere for speech and language functions in dyslexic children of both sexes, as it is in normal children. However, significant evidence of left hemisphere dysfunction was found in dyslexic children. Dyslexic boys showed bilateral representation of spatial form perception (in contrast to the usual right brain dominance found in normal boys), and evidence of impaired left-hemisphere processing of language functions. Dyslexic girls had only one deficiency, impaired left hemisphere function. These findings suggest that the neural substrate of dyslexia in boys may be bilateral representation of spatial perception, and impaired left hemisphere processing of language functions. In girls, it may involve only deficient function of the left hemisphere. Review of birth records of the dyslexic group showed that a “large majority” had subclinical or clinical jaundice as compared with normal controls, suggesting that hyperbilirubinemia may predispose to left hemisphere injury at birth. Computed brain tomograms (CT) of 24 patients with developmental dyslexia showed a pattern of reversed cerebral asymmetry in 10, with widening of the right parieto-occipital region as compared to the left [14]. Because functional asymmetry generally corresponds to structural asymmetry, these findings suggest that some compromise in the left hemisphere language functions may have occurred. BRAIN DYSFUNCTION
AND OTHER DEVELOPMENTAL
DISABILITIES
Additional evidence of impaired left hemisphere function has been noted in children with other developmental disabilities. Left temporal lobe atrophy has been observed in young boys with delayed language development and autistic behavior [ 121. Pneumoencephalograms in children with developmental language retardation showed structural damage of the left hemisphere more frequently than in a control group [ 21. In CT scans in 9 mentally retarded children with autistic behavior and
18
severe delay in language development, enlargement of the right parietooccipital region was found more often than in non-autistic retarded children or normal cases [ 151. This finding of reversed cerebral asymmetry suggests a mechanism for left hemisphere dysfunction underlying autistic behavior. The auditory system is selectively vulnerable to brief episodes of asphyxia at birth [27]. The inferior colliculus has a high oxygen requirement,’ and is one of the few brain structures myelinated at birth. Early injury to brain stem auditory pathways could interfere with development of normal auditory processing and cause impaired language development, as in autism or developmental dysphasia. Acquired aphasic disorders in children occur more often in boys than girls. Acquired auditory verbal agnosia, presumably related to left temporal lobe dysfunction, occurs more frequently in boys than in girls [ 11. Acquired aphasia in 19 children was associated with left-sided lesions in 88% of cases, and right-sided lesions in 12% of cases [ 131. DIAGNOSTIC AND EDUCATIONAL
IMPLICATIONS
Using a variety of tests, brain function can be examined as it relates to learning and behavior in children, drawing from both standard and informal psychologic tests. The pediatric neuropsychologist looks specifically at cognitive, linguistic, perceptual, and memory skills as they relate to specific academic tasks. Rather than using one specific test to diagnose learning disabilities, a typical neuropsychologic battery might assess: (1) significant differences in verbal and non-verbal IQ scores, from a test such as the Wechsler Intelligence Scale for Children; (2) strengths and deficits in the primary sensory areas: auditory, visual, and tactile; (3) spatial orientation and coordination in visual motor and handwriting tasks; (4) memory functions, in both verbal and non-verbal tasks; (5) language ability, including both speech production and language processing; (6) abstract reasoning, in both verbal and non-verbal tasks; and (7) academic achievement in reading, arithmetic, and spelling. Using the information obtained from the test battery, a profile of the child’s strengths and deficits may be derived *. From this profile, which assesses both auditory-verbal (“left-brain”) skills and visuo-spatial (“rightbrain”) skills, educational programming appropriate to the child’s needs is feasible.
* This approach is based on techniques developed by Barbara C. Wilson, Director, Neuropsychology Section, Department of Neurology, North Shore University Hospital, Manhasset, New York, U.S.A.
19
Case example No. 1 Fig. 1 illustrates a hypothetic profile of a 7-year-old, second grade boy with academic difficulties in spelling and hand-writing. In this profile, the individual subtest scores are converted to a “centile” score; with the 50th centile representing the average level of function of most children. He also reverses the direction of letters such as b-d and p-q when reading and writing. Despite the difficulty with letter reversals, he generally reads and comprehends well, and has good use of language. This profile illustrates primary strengths in the auditory-linguistic areas such that the child has a high verbal IQ, has an excellent memory for oral instructions presented, and is well able to verbalize abstract concepts. These skills are mediated primarily by the left hemisphere [ 241. The child displayed deficits in visuo-spatial skills in that his non-verbal IQ was significantly lower than his verbal IQ, and he had difficulty remembering and discriminating material presented visually. On the hand-writing task, which involved reproducing geometric designs, he displayed distortion and improper orientation of the designs as well as poor coordination. These visuo-spatial skills are mediated primarily by the right cerebral hemisphere [ 241. The deficits in this child, of these skills, suggest right hemisphere dysfunction. This profile also illustrates that presentation of tasks involving auditory and visual skills simultaneously enabled him to complete the tasks well.
AudItory
vlsuol
Motor
Acchlwement
Fig. 1. Profile of a 7-year-old boy with auditory-linguistic spatial and hand-writing skills.
strengths and deficits in
visuo-
20
Apparently his strengths in the auditory area helped him compensate for deficits in the visual area. This finding suggests that educational planning should involve pairing these two modalities. Finally, the profile indicates that this youngster was reading and comprehending well, but had difficulty when asked to spell words to dictation or do written arithmetic problems. Thus his academic difficulty occurred most often when writing and visuo-spatial skills (i.e. remembering the direction and spacing of letters and numbers) were requested. A sample educational program might include the following activities. (1) Teaching spelling by pairing the auditory input (i.e. the sound of letters) with the visual symbol (i.e. the printed letter). The child could also be asked to say the sound of the letter or word as he writes it, using his strong auditory modality to reinforce his weak writing skills. (2) To improve his visual discrimination skills, he could be asked to underline a word such as “do” each time it occurred on a page of simple words. (3) To improve his visual memory skills for words, he could be asked to write the words “in the air”, using large muscle movements, before being asked to write them on paper. Case example No. 2 Fig. 2 illustrates a 7-year-old boy with academic difficulties in reading and spelling. His arithmetic computation skills were at appropriate grade level, but he had difficulty in both reading comprehension and word attack skills. His spelling was poor, both oral and written. The profile illustrates primary strengths in visual and motor areas. The non-verbal IQ was slightly above average, as was his performance on tasks of visual memory and discrimination. Graphomotor skills, as measured in a task which involved reproducing geometric designs, were above average. Writing skills in the classroom were also reported to be good, as when he was asked to copy written material from the blackboard. These visual-spatial-motor skills are primarily mediated by the right cerebral hemisphere [ 241. The profile illustrates the primary deficits of this child in the auditory linguistic, or left hemisphere, areas of functioning. The verbal IQ, containing measures of general information, verbal abstract reasoning, social judgement, and ability to recall definitions or words, was below average. In Fig. 2, Auditory Memory I shows his ability to recall non-linguistic information, such as a series of digits, in the correct sequence. Auditory Memory II refers to ability to repeat sentences and recall the significant ideas in a paragraph read to him. Although both memory tasks were below the average level, this youngster had greater difficulty recalling verbal material presented orally. Thus, he would probably have difficulty remembering and performing directions presented orally in the classroom. Finally, auditory discrimination abilities were deficient, in that he was unable to discriminate speec!_ sounds in words or to discriminate between
21
AudItory
Motor
Visual
Fig. 2. Profile of a 7-year-old auditory-linguistic skills.
boy
with
Achievement
visuo-spatial-motor
strengths
and
deficits
in
similar sounding words. When attempting to read or spell, he had difficulty associating the sound of a letter or group of letters with the printed letters because of auditory association and auditory discrimination deficits, Attempts had been made to teach reading to him by use of phonic sounds but, not surprisingly, this method was unsuccessful. A sample educational program for this child might include the following. (1) Teaching through visual and motor areas to augment the auditorylinguistic deficits. When auditory-verbal material must be presented, it should be given in small steps and where possible, paired with another modality. (2) Additional practice on auditory discrimination of sounds by: (a) rhyming games (e.g. “It rhymes with floor. When you leave the room you walk through the _.“); (b) asking the child to think of several words that begin with the same first letter as “top”. (3) Work on auditory memory, by giving the child simple instructions, gradually increasing the number of steps involved. (4) Giving verbal instructions in the classroom in which the teacher would repeat the instructions to the child individually, having him repeat them step by step. (5) Working on his expressive language ability, the teacher might ask him to label, describe, and tell stories about events or things in his environment. (6) Teaching him by the “whole word” approach, pairing words with pic-
22
tures of the object, or using word groups which are similar except for one letter (i.e. tap, lap, nap, sap). (7) Allowing him visual cues (practicing with concrete objects such as matchsticks), or tactile cues (such as tapping on the table) may help reinforce the arithmetic concepts. Although this youngster performs well on arithmetic computation skills, he may have increasing difficulty as arithmetic problems become more abstract and verbal. Although the two profiles used for illustrative purposes presented rather clear-cut strengths and deficits, it should be stated that the problems of children are rarely so circumscribed. Each child is different, but this approach is valuable in planning individualized education programs for language- and learningdisabled children. Children can be taught to spell, for example, while listening to music, perhaps by suppressing right hemisphere functions. Serial, color-coded, systematic “phonics” can be used to emphasize word structure in reading instruction. Such “lateralizing” techniques have been used successfully with leamingdisabled children, producing significant gains in oral reading scores as compared with conventional teaching techniques [ 311. CONCLUSIONS
The human brain is precocious in its development, the major structural landmarks being formed by 10-12 weeks gestation. Subsequent develop ment proceeds sequentially and asynchronously, and continues well into adult life. The two sides of the brain are specialized anatomically and physiologically. The left hemisphere serves language, reading, and mathematical skills; the right, visual-spatial, musical, and mechanical abilities. Maturation of these specialized activities is different in boys and girls, girls having greater functional efficiency of the left hemisphere. Boys are superior in visuospatial abilities, but girls are superior in language acquisition. The left temporal lobe in boys appears to be especially vulnerable to early insult; this feature may, in part, explain the higher incidence of language and learning disabilities in boys. Rational classroom instruction is based upon careful assessment of right and left cerebral functions. Sound knowledge of the neurologic substrates of normal and abnormal brain development will enable the physician to better diagnose and manage the increasing numbers of children seen for evaluation of learning, language, and reading disabilities. REFERENCES 1 Cooper, J.A. and Ferry, P.C., Acquired auditory verbal agnosia and seizures in childhood, J. Speech Dis., 43 (1978) 176-184. 2 Dalby, M., Airstudies of speech-retarded children: evidence of early lateralization of
23
3
4 5 6 7
8
9 10
11 12
13 14
15 16 17 18 19
20 21
22 23 24
language function. Presented at the Int. Congr. Child Neurology, Toronto, Ontario, October 10, 1975. Dodge, P.R., Prensky, A.L. and Feigin, R.D., Morphologic development. In P.R. Dodge, A.L. Prensky and R.D. Feigin (Eds.), Nutrition and the Developing Nervous System, Mosby Co., St. Louis, 1975, Chap. 1. Dorovini-Zis, K. and Dolman, C.L., Gestational development of the brain, Arch. Path. Lab. Med., 101 (1975) 192-195. Education for All Handicapped Children Act of 1975, Public Law 94-142, November 29, 1975. Education of the Handicapped Today. Am Ed 1-3, 12, 1976. Available from Superintendent of Documents, Government Printing Office, Washington, D.C. 20402. Entus, A.K., Hemispheric asymmetry in processing of dichstically presented speech and nonspeech stimuli by infants. In S.J. Segalowitz and F.A. Gruber (Eds.), Language Development and Neurological Theory, Academic Press, New York, 1977, Chap. 6. Fonseca, N.M., Sell, A.B. and Carlini, A.A., Differential behavioral responses of male and female adult rats treated with five psychotic drugs in the neonatal state, Psychopharmacologia (Bed.), (1976) 263-268. The Future of Pediatric Education. Report by the Task Force on Pediatric Education, American Academy of Pediatrics, Evanston, Ill. 60204. Goldman, P.S., Age, sex, and experience as related to the neural basis of cognitive development. In N.A. Buchwald and M.A. Brazier (Eds.), Brain Mechanisms in Mental Retardation, Academic Press, New York, 1975, Chap. 13. Gorski, R.A., Sexual differentiation of the brain. Hosp. Pratt., 10 (1978) 55-62. Hauser, S.L., De Long, G.R. and Rosman, N.P., Pneumographic findings in the infantile autism syndrome - a correlation with temporal lobe disease, Brain, 98 (1975) 367-442. Hecaen, H., Acquired aphasia in children and the ontogenesis of hemispheric functional specialization, Brain Lang., 3 (1976) 114-134. Hier, D.B., Le May, M., Rosenberger, P.B. and Perlo, V.P., Developmental dyslexia: evidence for a subgroup with a reversal of cerebral asymmetry, Arch. Neurol. (Chic.), 35 (1975) 90-92. Hier, D.B., Le May, M. and Rosenberger, P.B., Autism: association with reversed cerebral asymmetry, Neurology (Minneap.), 28 (1978) 348-349. Hutt, C., Biological bases of psychological sex differences, Amer. J. Dis. Child., 132 (1978) 170-177. Jones, D.G., Synapses and Synaptosomes: Morphological Aspects, Chapman and Hall, London, 1975. Krasher, S.D., The critical period for language acquisition and its possible bases, Ann. N.Y. Acad. Sci., 263 (1975) 211-224. Langworthy, O., Development of behaviour patterns and myelination of the nervous system in the human fetus and infant, Contr. Embryol. Carneg. Instn, 139 (1933) l-57. Levy, J., The mammalian brain and the adaptive advantage of cerebral asymmetry, Ann. N.Y. Acad. Sci., 299 (1977) 264-272. Mattis, S., French, J. and Rapin, I., Dyslexia in children and young adults: three independent neuropsychological syndromes, Develop. Med. Child. Neurol., 17 (1975) 150-163. McGlone, J., Sex differences in the cerebral organization of verbal functions in patients with unilateral brain lesions, Brain, 100 (1977) 775-793. Moltz, H., Some implications of the critical period hypothesis, Ann. N.Y. Acad. Sci., 223 (1973) 144-146. Reitan, R.M., A research program on the psychological effects of brain lesions in in human beings. In N.R. Ellis (Ed.), International Review of Research in Mental Retardation, 1, Academic Press, New York, 1966.
24 25 Robinson, R.J. (Ed.), Brain and Early Behavior: Development in the Fetus and Infant, Academic Press, London, 1969. 26 Rubens, A.B., Anatomical asymmetries of human cerebral cortex. In S. Harnad et al. (Eds.), Lateralization in the Nervous System, Academic Press, New York, 1977, Chap. 26. 27 Simon, N., Echolalic speech in childhood autism: consideration of possible underlying loci of brain damage, Arch. gen. Psychiat., 32 (1975) 1439-1446. 28 Stark, J., Reading failure: a language-based problem. ASHA, 17 (1975) 832-834. 29 Taylor, D.C., Differential rates of cerebral maturation between sexes and between hemispheres, Lancet, 2 (1969) 140-142. 30 Turkewitz, G., The development of lateral differentiation in the human infant, Ann. N.Y. Acad. Sci., 299 (1977) 309-317. 31 van den Honert, D., A neuropsychological technique for training dyslexics, J. Learn. Disabil., 1(1977) 15-21. 32 Wada, J.A., Clarke, R. and Hamm, A., Cerebral hemispheric asymmetry in humans: cortical speech zones in 100 adult and 100 infant brains, Arch. Neurol. (Chic.), 32 (1975) 239-246. 33 Wiig, E., Language disabilities of adolescents: implications for diagnosis and remediation, Brit. J. Disord. Commun., 11 (1976) 3-17. 34 Witelson, S.F., Early hemispheric specialization and interhemispheric plasticity: an empirical and theoretical review. In S.J. Segalowitz and F.A. Gruber (Eds.), Language Development and Neurological Theory, Academic Press, New York, 1977, Chap. 16. 35 Witelson, S.F., Sex and the single hemisphere: right hemisphere specialization for spatial processing, Science, 193 (1976) 425-427. 36 Witelson, S.J. and Pallie, W., Left hemisphere specialization for language in the newborn: neuroanatomical evidence of asymmetry, Brain, 96 (1973) 641-647. 37 Witelson, S.F., Neural and cognitive correlates of developmental dyslexia: age and sex differences. In C. Shagass, S. Gershon and A.J. Friedhoff (Eds.), Psychopathology and Brain Dysfunction, Raven Press, New York, 1977. 38 Wolff, P.H., ‘Critical periods’ in human cognitive development, Hosp. Pratt., 5 (1970) 77-87.
1 (1979) 13-24
13
Review Articles BRAIN FUNCTION
AND LANGUAGE
DISABILITIES
*
PEGGY C. FERRY, JAN L. CULBERTSON, PATRICIA M. FITZGIBBONS MARTIN G. NETSKY
and
Department of Pediatrics and Neurology, University of Arizona Health Sciences Center, Tucson, Ark. 85724 and Departments of Pediatrics and Pathology, Vanderbilt Uniuersity School of Medicine, Nashville, Tenn. 37232 (U.S.A.) (Received December 8th, 1978) (Accepted May lst, 1979)
INTRODUCTION
Children with normal intelligence, but with specific learning disabilities, are being recognized with increasing frequency. In a survey in 1976, there were almost 2 million children with learning disabilities in the United States, 87% of them not receiving special educational services [ 61. A recent survey by the American Academy of Pediatrics showed that 15% of mothers reported some type of learning difficulty in their children, and that almost half sought advice from their physician about the problem [9]. Recent federal legislation, Public Law 94-142, mandates that learning-disabled children receive free appropriate public education designed for their specific needs [ 51. This law has resulted in identification and referral of increased numbers of such children. In the past decade, studies on neurologic, cognitive, and linguistic development in children have shown increasing evidence of cerebral hemispheric specialization, and differential rates of brain maturation between sexes. In this review, information will be provided about: (1) normal brain development, and (2) the neurologic substrates of language and learning disabilities, to enable the physician to participate in planning rational educational programs. NORMAL BRAIN DEVELOPMENT
(1) Anatomic
and physiologic
development
During intrauterine life, the brain is the largest organ in the body. It constitutes 15% of body weight during most of the 40 weeks of gestation. This fact highlights a major feature to be emphasized: the brain is precocious, its * Presented in part at the SENTAC Annual Meeting, Santa Barbara, Calif., December 7th, 1978.
14
major anatomic structures being well formed by the tenth week of fetal life [3]. This observation is often overlooked in consideration of critical periods, plasticity, and later developmental events. The first gross evidence of the nervous system arises about 3 weeks after conception with the formation of the neural groove. This structure evolves into the neural tube, closure occurring between 21 and 25 days. By the end of the third week, the CNS has divided into 3 major subdivisions: prosencephalon, mesencephalon, and rhombencephalon. Reflex physiologic circuits are active after 5.5 weeks [25]. The circle of Willis is completed by 6.5 weeks. At 7 weeks, the principle aural structures are formed, and spontaneous electroencephalographic (EEG) activity can be recorded. Five subdivisions are delineated by 8 weeks, with the cerebral hemispheres clearly evident. Rapid telencephalic growth is characteristic of the period from 8 to 12 weeks. Externally, the fetus at this stage resembles the human infant. An eye-blink reflex can be obtained at 10 weeks, and patellar reflexes have been observed in a 12-week fetus [ 191. The sylvian fissure develops at 14 weeks gestation, and additional fissures and gyri develop in predictable sequence until birth. The gyral configuration of the brain is a reliable guide to gestational age [ 41. Myelination begins around 20 weeks. The visual pathway is structurally complete by 28 weeks, from the optic disc to the occipital lobe. After this time, the cortex forms into 6 distinct layers. Pupillary reflexes can be obtained at 27-29 weeks [ 251. Different parts of the brain grow at different rates. The medulla-pons region is largest up to 7 weeks, then becomes proportionately smaller at 18 weeks. The telencephalon is smaller at 4 weeks, but by 8 weeks it is growing more rapidly than all other parts of the brain. It stabilizes at about 90% of total brain weight in the 16th week of gestation. The cerebellum has two spurts in growth, one at about 8 weeks of intrauterine life, and the other in the first year after birth. The majority of neurons in the adult brain are formed early, perhaps by 18 weeks gestation [ 171. The onset of synaptogenesis differs regionally, but has been noted as early as 8.5 weeks gestation. Radioautography has shown that “waves” of neuroblasts migrate through pre-existing layers of the brain to form the final 6 layers of the cortex. Evidence suggests that specific spatial and temporal sequencing of synaptic development occurs from 8.5 to 24 weeks. After 23 weeks, the number of synaptic connections increases from lo- to 80-fold [3]. Myelination begins in the fourth month of gestation and continues in an orderly sequence into the fifth and sixth decades of postnatal life [3]. Yakovlev has shown that specific pathways in the brain myelinate at widely different times, following phylogeneticaIly logical temporal and spatial patterns. In general, the older systems myelinate first, proceeding in a caudo-cephalic direction, then the pyramidal tracts (completed during the second year of life), and association fibers (continuing well into adult life).
15
(2) “Critical” periods The concept of various critical periods in neurologic development has been proposed to indicate finite times in which specific events must occur to provide the substrate for subsequent developmental achievements [ 231. This “now-or-never” hypothesis is based upon imprinting studies in animals and psychologic studies of sensorimotor development leading to cognitive skills in children. More recently, however, the concept has been challenged. Wolff, in 1970, suggested that child behavior depends upon the complex interaction of many biologic and environmental factors. The concept of “sensitive” periods has been proposed as an alternative, referring to periods when a child may learn particular skills more easily than others [ 381. Based on the early precocity of brain development and the highly complex interaction between neurogenesis, synaptogenesis, and myelination as described, all phases of early brain development are critical. The most important (if not critical) period of neurologic development is the first 10 weeks of intrauterine life, when the anatomic, physiologic, and biochemical substrates of future developmental progress are being formed. HEMISPHERIC ASYMMETRY
AND SPECIALIZATION
During the past century, increasing evidence has accumulated of a division of labor between the two sides of the brain. The cerebral hemispheres are asymmetric and clearly specialized for different cognitive and linguistic functions [34]. In gross anatomic appearance, the left and right halves of the brain are not identical. The left sylvian fissure is significantly longer than the right in most adult and infant human brains [26]. The superior surface of the posterior temporal lobe is longer on the left. The angular gyms is smaller on the left. The left planum tempo&e, the portion of the temporal lobe involved in language comprehension, is distinctly larger than the right. This asymmetry is clearly evident at birth as well as in fetuses as early as 29 weeks gestation, and suggests that the substrate for language development in the left cerebral hemisphere is present well before birth [32]. Evoked response and dichotic listening studies in newborn infants have shown left hemisphere specialization for speech sounds [ 71. Infants in the first week of life keep their heads turned preferentially to the right 90% of the time [30]. This head-right bias increases with conceptual age, from 64% at 33-35 weeks to 96% at 39 weeks. The right hemisphere is specialized for musical notes in the first week of life [14]. Hemispheric specialization continues to develop throughout childhood. Motor performance tests in children as young as 3 years of age indicate right hemisphere specialization for non-sequential, spatial control of hand movements [ 201. Bight hemisphere specialization for visually presented stimuli is
16
evident in normal children by the age of 6 years [ 111. Development of left hemisphere specialization for mediating language functions is complete by about 5 years of age [18]. Witelson has summarized the current evidence about hemispheric specialization: (1) the left hemisphere processes stimuli in a linguistic, sequential, analytic manner to form the basis of receptive and expressive language; and (2) the right hemisphere uses a synthetic or holistic approach [34]. These differences are not absolute, in that each side is able to execute some functions of the other to some extent, SEX DIFFERENCES
IN BRAIN FUNCTION
Along with the differences in functional capabilities between the two hemispheres, there are sex differences in cerebral organization and function. Sexual differentiation of the brain is similar to the reproductive system: the brain is inherently female, and, if not exposed to androgenic hormones during development, it remains so [35]. Exposure to testicular androgen converts the ontogenetically female brain into a “male” brain, with differing functional neuronal mechanisms. In general, girls acquire language earlier than boys, have lower touch and pain thresholds, and have better sound discrimination abilities. Boys have better visuospatial abilities, greater muscular development, and more precision in aiming and throwing [ 161. Boys show right hemisphere specialization for spatial processing as early as age 6 years, but girls maintain bilateral representation until age 13 1351. Morphologic asymmetry between left and right temporal lobes is more evident in females earlier in ontogeny than males, suggesting again a preprogrammed neural substrate for earlier language development in girls [ 361. Epidemiologic evidence shows that certain neurologic disorders are far more common in boys than girls: autistic behavior, some forms of cerebral palsy, reading disabilities, and language disorders are 2-8 times more frequent in boys than in girls [lo]. Primate studies have shown that brain lesions in infant monkeys produced significantly more sequelae in males than females. Male and female rats responded in opposite manner to psychotropic drugs given in the neonatal period; early drug administration abolished the expected normal sexual differences in behavior [ 81. Studies on adults with unilateral brain damage showed that 3 times more men than women with left hemisphere lesions became aphasic [22]. Only men continued to show the expected pattern of depressed verbal intelligence and verbal memory after left hemisphere damage as compared to men with right hemisphere damage. Women, as a group, had a more heterogenous pattern of cerebral speech representation than did men. Studies of children with temporal lobe epilepsy showed differences between the left and right hemispheres, and between sexes [29]. Left-sided
17
seizures occurred more frequently before age 2, but right-sided lesions were equally prevalent during the first 4 years of life. The inception rate of seizures in boys fell away smoothly with increasing age, but girls had a more precipitate fall. LANGUAGE DEVELOPMENT,
READING ABILITY, AND DYSLEXIA
Increasing evidence has accumulated in the past decade that language impairment forms the substrate for many reading problems [28]. A study of 113 dyslexic children has shown that 39% had poor receptive and expressive language abilities [ 211. A study of 30 learning-disabled adolescents revealed that they had significantly more difficulty with linguistic processing, cognitive-semantic processing, and retrieval of verbal labels, verbal associations, and syntactic structures than a matched control group [33]. Studies of hemispheric specialization have been performed in a large group of dyslexic children [ 371. The left hemisphere was the major hemisphere for speech and language functions in dyslexic children of both sexes, as it is in normal children. However, significant evidence of left hemisphere dysfunction was found in dyslexic children. Dyslexic boys showed bilateral representation of spatial form perception (in contrast to the usual right brain dominance found in normal boys), and evidence of impaired left-hemisphere processing of language functions. Dyslexic girls had only one deficiency, impaired left hemisphere function. These findings suggest that the neural substrate of dyslexia in boys may be bilateral representation of spatial perception, and impaired left hemisphere processing of language functions. In girls, it may involve only deficient function of the left hemisphere. Review of birth records of the dyslexic group showed that a “large majority” had subclinical or clinical jaundice as compared with normal controls, suggesting that hyperbilirubinemia may predispose to left hemisphere injury at birth. Computed brain tomograms (CT) of 24 patients with developmental dyslexia showed a pattern of reversed cerebral asymmetry in 10, with widening of the right parieto-occipital region as compared to the left [14]. Because functional asymmetry generally corresponds to structural asymmetry, these findings suggest that some compromise in the left hemisphere language functions may have occurred. BRAIN DYSFUNCTION
AND OTHER DEVELOPMENTAL
DISABILITIES
Additional evidence of impaired left hemisphere function has been noted in children with other developmental disabilities. Left temporal lobe atrophy has been observed in young boys with delayed language development and autistic behavior [ 121. Pneumoencephalograms in children with developmental language retardation showed structural damage of the left hemisphere more frequently than in a control group [ 21. In CT scans in 9 mentally retarded children with autistic behavior and
18
severe delay in language development, enlargement of the right parietooccipital region was found more often than in non-autistic retarded children or normal cases [ 151. This finding of reversed cerebral asymmetry suggests a mechanism for left hemisphere dysfunction underlying autistic behavior. The auditory system is selectively vulnerable to brief episodes of asphyxia at birth [27]. The inferior colliculus has a high oxygen requirement,’ and is one of the few brain structures myelinated at birth. Early injury to brain stem auditory pathways could interfere with development of normal auditory processing and cause impaired language development, as in autism or developmental dysphasia. Acquired aphasic disorders in children occur more often in boys than girls. Acquired auditory verbal agnosia, presumably related to left temporal lobe dysfunction, occurs more frequently in boys than in girls [ 11. Acquired aphasia in 19 children was associated with left-sided lesions in 88% of cases, and right-sided lesions in 12% of cases [ 131. DIAGNOSTIC AND EDUCATIONAL
IMPLICATIONS
Using a variety of tests, brain function can be examined as it relates to learning and behavior in children, drawing from both standard and informal psychologic tests. The pediatric neuropsychologist looks specifically at cognitive, linguistic, perceptual, and memory skills as they relate to specific academic tasks. Rather than using one specific test to diagnose learning disabilities, a typical neuropsychologic battery might assess: (1) significant differences in verbal and non-verbal IQ scores, from a test such as the Wechsler Intelligence Scale for Children; (2) strengths and deficits in the primary sensory areas: auditory, visual, and tactile; (3) spatial orientation and coordination in visual motor and handwriting tasks; (4) memory functions, in both verbal and non-verbal tasks; (5) language ability, including both speech production and language processing; (6) abstract reasoning, in both verbal and non-verbal tasks; and (7) academic achievement in reading, arithmetic, and spelling. Using the information obtained from the test battery, a profile of the child’s strengths and deficits may be derived *. From this profile, which assesses both auditory-verbal (“left-brain”) skills and visuo-spatial (“rightbrain”) skills, educational programming appropriate to the child’s needs is feasible.
* This approach is based on techniques developed by Barbara C. Wilson, Director, Neuropsychology Section, Department of Neurology, North Shore University Hospital, Manhasset, New York, U.S.A.
19
Case example No. 1 Fig. 1 illustrates a hypothetic profile of a 7-year-old, second grade boy with academic difficulties in spelling and hand-writing. In this profile, the individual subtest scores are converted to a “centile” score; with the 50th centile representing the average level of function of most children. He also reverses the direction of letters such as b-d and p-q when reading and writing. Despite the difficulty with letter reversals, he generally reads and comprehends well, and has good use of language. This profile illustrates primary strengths in the auditory-linguistic areas such that the child has a high verbal IQ, has an excellent memory for oral instructions presented, and is well able to verbalize abstract concepts. These skills are mediated primarily by the left hemisphere [ 241. The child displayed deficits in visuo-spatial skills in that his non-verbal IQ was significantly lower than his verbal IQ, and he had difficulty remembering and discriminating material presented visually. On the hand-writing task, which involved reproducing geometric designs, he displayed distortion and improper orientation of the designs as well as poor coordination. These visuo-spatial skills are mediated primarily by the right cerebral hemisphere [ 241. The deficits in this child, of these skills, suggest right hemisphere dysfunction. This profile also illustrates that presentation of tasks involving auditory and visual skills simultaneously enabled him to complete the tasks well.
AudItory
vlsuol
Motor
Acchlwement
Fig. 1. Profile of a 7-year-old boy with auditory-linguistic spatial and hand-writing skills.
strengths and deficits in
visuo-
20
Apparently his strengths in the auditory area helped him compensate for deficits in the visual area. This finding suggests that educational planning should involve pairing these two modalities. Finally, the profile indicates that this youngster was reading and comprehending well, but had difficulty when asked to spell words to dictation or do written arithmetic problems. Thus his academic difficulty occurred most often when writing and visuo-spatial skills (i.e. remembering the direction and spacing of letters and numbers) were requested. A sample educational program might include the following activities. (1) Teaching spelling by pairing the auditory input (i.e. the sound of letters) with the visual symbol (i.e. the printed letter). The child could also be asked to say the sound of the letter or word as he writes it, using his strong auditory modality to reinforce his weak writing skills. (2) To improve his visual discrimination skills, he could be asked to underline a word such as “do” each time it occurred on a page of simple words. (3) To improve his visual memory skills for words, he could be asked to write the words “in the air”, using large muscle movements, before being asked to write them on paper. Case example No. 2 Fig. 2 illustrates a 7-year-old boy with academic difficulties in reading and spelling. His arithmetic computation skills were at appropriate grade level, but he had difficulty in both reading comprehension and word attack skills. His spelling was poor, both oral and written. The profile illustrates primary strengths in visual and motor areas. The non-verbal IQ was slightly above average, as was his performance on tasks of visual memory and discrimination. Graphomotor skills, as measured in a task which involved reproducing geometric designs, were above average. Writing skills in the classroom were also reported to be good, as when he was asked to copy written material from the blackboard. These visual-spatial-motor skills are primarily mediated by the right cerebral hemisphere [ 241. The profile illustrates the primary deficits of this child in the auditory linguistic, or left hemisphere, areas of functioning. The verbal IQ, containing measures of general information, verbal abstract reasoning, social judgement, and ability to recall definitions or words, was below average. In Fig. 2, Auditory Memory I shows his ability to recall non-linguistic information, such as a series of digits, in the correct sequence. Auditory Memory II refers to ability to repeat sentences and recall the significant ideas in a paragraph read to him. Although both memory tasks were below the average level, this youngster had greater difficulty recalling verbal material presented orally. Thus, he would probably have difficulty remembering and performing directions presented orally in the classroom. Finally, auditory discrimination abilities were deficient, in that he was unable to discriminate speec!_ sounds in words or to discriminate between
21
AudItory
Motor
Visual
Fig. 2. Profile of a 7-year-old auditory-linguistic skills.
boy
with
Achievement
visuo-spatial-motor
strengths
and
deficits
in
similar sounding words. When attempting to read or spell, he had difficulty associating the sound of a letter or group of letters with the printed letters because of auditory association and auditory discrimination deficits, Attempts had been made to teach reading to him by use of phonic sounds but, not surprisingly, this method was unsuccessful. A sample educational program for this child might include the following. (1) Teaching through visual and motor areas to augment the auditorylinguistic deficits. When auditory-verbal material must be presented, it should be given in small steps and where possible, paired with another modality. (2) Additional practice on auditory discrimination of sounds by: (a) rhyming games (e.g. “It rhymes with floor. When you leave the room you walk through the _.“); (b) asking the child to think of several words that begin with the same first letter as “top”. (3) Work on auditory memory, by giving the child simple instructions, gradually increasing the number of steps involved. (4) Giving verbal instructions in the classroom in which the teacher would repeat the instructions to the child individually, having him repeat them step by step. (5) Working on his expressive language ability, the teacher might ask him to label, describe, and tell stories about events or things in his environment. (6) Teaching him by the “whole word” approach, pairing words with pic-
22
tures of the object, or using word groups which are similar except for one letter (i.e. tap, lap, nap, sap). (7) Allowing him visual cues (practicing with concrete objects such as matchsticks), or tactile cues (such as tapping on the table) may help reinforce the arithmetic concepts. Although this youngster performs well on arithmetic computation skills, he may have increasing difficulty as arithmetic problems become more abstract and verbal. Although the two profiles used for illustrative purposes presented rather clear-cut strengths and deficits, it should be stated that the problems of children are rarely so circumscribed. Each child is different, but this approach is valuable in planning individualized education programs for language- and learningdisabled children. Children can be taught to spell, for example, while listening to music, perhaps by suppressing right hemisphere functions. Serial, color-coded, systematic “phonics” can be used to emphasize word structure in reading instruction. Such “lateralizing” techniques have been used successfully with leamingdisabled children, producing significant gains in oral reading scores as compared with conventional teaching techniques [ 311. CONCLUSIONS
The human brain is precocious in its development, the major structural landmarks being formed by 10-12 weeks gestation. Subsequent develop ment proceeds sequentially and asynchronously, and continues well into adult life. The two sides of the brain are specialized anatomically and physiologically. The left hemisphere serves language, reading, and mathematical skills; the right, visual-spatial, musical, and mechanical abilities. Maturation of these specialized activities is different in boys and girls, girls having greater functional efficiency of the left hemisphere. Boys are superior in visuospatial abilities, but girls are superior in language acquisition. The left temporal lobe in boys appears to be especially vulnerable to early insult; this feature may, in part, explain the higher incidence of language and learning disabilities in boys. Rational classroom instruction is based upon careful assessment of right and left cerebral functions. Sound knowledge of the neurologic substrates of normal and abnormal brain development will enable the physician to better diagnose and manage the increasing numbers of children seen for evaluation of learning, language, and reading disabilities. REFERENCES 1 Cooper, J.A. and Ferry, P.C., Acquired auditory verbal agnosia and seizures in childhood, J. Speech Dis., 43 (1978) 176-184. 2 Dalby, M., Airstudies of speech-retarded children: evidence of early lateralization of
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24 25 Robinson, R.J. (Ed.), Brain and Early Behavior: Development in the Fetus and Infant, Academic Press, London, 1969. 26 Rubens, A.B., Anatomical asymmetries of human cerebral cortex. In S. Harnad et al. (Eds.), Lateralization in the Nervous System, Academic Press, New York, 1977, Chap. 26. 27 Simon, N., Echolalic speech in childhood autism: consideration of possible underlying loci of brain damage, Arch. gen. Psychiat., 32 (1975) 1439-1446. 28 Stark, J., Reading failure: a language-based problem. ASHA, 17 (1975) 832-834. 29 Taylor, D.C., Differential rates of cerebral maturation between sexes and between hemispheres, Lancet, 2 (1969) 140-142. 30 Turkewitz, G., The development of lateral differentiation in the human infant, Ann. N.Y. Acad. Sci., 299 (1977) 309-317. 31 van den Honert, D., A neuropsychological technique for training dyslexics, J. Learn. Disabil., 1(1977) 15-21. 32 Wada, J.A., Clarke, R. and Hamm, A., Cerebral hemispheric asymmetry in humans: cortical speech zones in 100 adult and 100 infant brains, Arch. Neurol. (Chic.), 32 (1975) 239-246. 33 Wiig, E., Language disabilities of adolescents: implications for diagnosis and remediation, Brit. J. Disord. Commun., 11 (1976) 3-17. 34 Witelson, S.F., Early hemispheric specialization and interhemispheric plasticity: an empirical and theoretical review. In S.J. Segalowitz and F.A. Gruber (Eds.), Language Development and Neurological Theory, Academic Press, New York, 1977, Chap. 16. 35 Witelson, S.F., Sex and the single hemisphere: right hemisphere specialization for spatial processing, Science, 193 (1976) 425-427. 36 Witelson, S.J. and Pallie, W., Left hemisphere specialization for language in the newborn: neuroanatomical evidence of asymmetry, Brain, 96 (1973) 641-647. 37 Witelson, S.F., Neural and cognitive correlates of developmental dyslexia: age and sex differences. In C. Shagass, S. Gershon and A.J. Friedhoff (Eds.), Psychopathology and Brain Dysfunction, Raven Press, New York, 1977. 38 Wolff, P.H., ‘Critical periods’ in human cognitive development, Hosp. Pratt., 5 (1970) 77-87.
