Thirty years of research on developmental neurolinguistics

Review Article

Thirty Years. of Research on Developmental Neurolinguistics

John L. Locke, PhD

A body of medically important work has accumulated in the field of developmental neurolinguistics in the 30 years since Lenneberg set forth a research agenda for that field, consisting of the following: (1) the physiologic specialization or endowment for speech; (2) the genetic origin or natural history of vocalization and speech; (3) the nature of prelinguistic behavior, making possible the detection of any environmental (social) influences; (4) the development of motor-speech orgau- ization from birth; and (5) the limiting effects of deficient intelligence, hearing, and environmental stimulation. Subsequent study of these questions has estab- lished a genetic, neuroanatomic, and functional basis for such outwardly disparate disorders as dyslexia, stuttering, autism, and delayed language. Studies of emergent motor behavior suggest that babbling may index a state of neural maturation favoring expression of spoken languages. Based on studies of the congenitally deaf, mentally retarded, and other clinical populations it is now considered possible to detect early warn- ing signs of developmental language disorders during the first year of life based on analyses of vocal turn- taking, gesturing, and utterance complexity.

Locke JL. Thirty years of research on developmental neu- roiinguistics. Pediatr Neurol 1992;8:245-50.

. Introduction

Thirty years ago, Eric Lenneberg described the promise of a new domain of biomedical inquiry and the hope of- fered by emerging analytic methods [l]. Although it was never named specifically, that domain may well be called “developmental neurolinguistics” because it involves the scientific investigation of human speech and language within a neurobiologic framework.

In 1962, Lenneberg argued that basic research in developmental neurolinguistics eventually would produce implications for medical diagnosis and treatment. In hind- sight, it appears that Lenneberg’s optimism was not unwar- ranted, and in this review I consider the 5 central issues

raised by Lenneberg, reporting progress in the medical aspects of developmental neurolinguistics over the last 3 decades. Because there has been a great deal of relevant research in the last 30 years, my review will be selective.

Issues Raised by Lenneberg

In the target article, Lenneberg described his own ongo- ing research and set forth the following topics for future investigation [ 11:

(1) The physiologic specialization or endowment for speech;

(2) The genetic origin or natural history of vocalization and speech;

(3) The nature of prelinguistic behavior, making possible the detection of any environmental (social) influences;

(4) The development of motor-speech organization from birth; and,

(5) The limiting effects of deficient intelligence, hearing, and environmental stimulation.

In his own career, Lenneberg studied each of these questions, but the inquiry was cut short by his untimely death in 1975. His studies of vocalization and spoken language, described in 1962 and later presented in detail elsewhere [2-51, were based on various populations, including normally developing infants raised in normal environments, children with Down syndrome and other genetic abnor- malities, congenitally deaf and hearing infants being raised by hearing or deaf parents, an anarthric child, and at least one tracheostomized infant.

A Thirty-year Report: Clinical Progress

In this report, I review the critical findings affecting each of the areas above, in some cases expanding the original issue slightly to include unforeseen questions of a related nature. The interpretations presented are relevant to clinical issues in pediatric neurology and several other medical specialties.

Critical Period for Language and Cerebral Plasticity

LeMeberg believed there was a critical developmental period in which the brain could assume linguistic functions

From the Neurolinguistics Laboratory; Massachusetts General Hospital Institute of Health Professions and Harvard Medical School; Boston, Massachusetts.

Communications should be addressed to: Dr. Locke; Neurolinguistics Laboratory; MGH Institute of Health Professions; 101 Menimac StreeS Boston, MA 021 M-4707. Received March 9, 1992; accepted May 19,1992

Locke: DevelopmentalNeucolingui&% %I5

if the child were exposed to appropriate stimulation, after which language acquisition would be extraordinarily dif- ficult. This period is now more commonly regarded as a sensitive period because language has a fairly broad temporal envelope with a gradual offset. Certainly this applies to theacquisition of languages encountered after one’s first language has been mastered.

There now appear to be several -age periods in which language learning is especially efficient. Languages encountered between birth and about 7 years of age are likely to be expressed with a native-sounding accent [6]. This also is the period in which the bulk of one’s native language is mastered. Following this initial period there is a second interval that extends until or through adolescence, after which there may be a further decline in language learning ability.

Studies of unilateral brain damage occurring during the first year or two of life revealed that neither left nor right hemisphere lesions necessarily produced lasting effects on language development [7]. The plasticity of the developing system is such that cerebral reorganization evidently takes place, sometimes producing subtle differences in language processing but not necessarily a measurable in- adequacy. This fmding is not surprising because much of the brain develops competitively, with active inputs secur- ing larger processing domains in the cortex than inactive ones. Surgical de- and re-afferentation causes the development of new pathways and reorganization of the cortex in animals [8,9]. Naturalistic studies of congenitally deaf adults suggest that the “auditory cortex” may be comman- deered by the visual system [lO,ll].

Recovery from Aphasia. Since Lenueberg’s time it has been believed that cortical plasticity declines with neural maturation, accounting for the lack of recovery from aphasia in older adults. In the aging human brain, there is evidently little adaptive capability in whatever alternate structures would normally be able to assume responsibility for spoken language in younger persons; however, in regard to nonlinguistic processing at least, primate brain appears to be exceedingly plastic for sensory processing well into adulthood [9]; with additional research it may become possible to restore some level of cortical plasticity in mechanisms capable of assuming linguistic operations.

Neuroanatomy and Physiology of Language

Communicative Factors. The human genome provides each neurologically normal infant with a developmental path which will lead to spoken language when there also is opportunity for appropriate social interaction. To a degree, the linguistic adequacy of social interactions depends upon each infant’s interest in, and capacity to process facial and vocal cues which convey affect. These cues are demonstrated during the act of speaking; therefore, mechanisms encouraging attention to these cues lure infants into the stream of information which carries language [12].

These facts, along with other behavioral data, suggest that congenial faces may attract infants to the human voice

and, perforce, spoken language. What, then, of the linguistic development of children who are blind? Research indi- cates that blind children do not necessarily develop language more slowly than their sighted counterparts, but there are qualitative differences in their initial lexicon. Specifically, the first 50 words in the expressive vocabulary of blind children may include a lower than normal proportion of words having a visible mode of articulation (e.g., words beginning with a labial consonant, such as ball) and their words may be deployed in less creative ways than is the case with sighted children [13]. In autism, where there frequently is a documentable indifference to the human face, and an inability to interpret facial affect [ 141, there tends to be rather severe language and cognitive deficits.

Neural specializations for social interaction are important pieces of the larger neural mechanisms which sub- serve language. In primates, there are neurons dedicated to face recognition and other brain cells that appear to respond only to facial activity [15,16]. Less is known about any vocal or bimodal (face-voice) neurons that may exist, although infants are capable of bimodal matching operations within the first month of life [17,18].

In humans, there are interesting neurophysiologic connections between voices and faces both in receptive and expressive processing. In reception, lesions can impair either the identification of familiar faces (prosopagnosia) or the interpretation of emotional facial activity [ 191; damage in and around the same parts of the brain can impair either the identification of .familiar voices (phonagnosia) or the interpretation of emotional vocal activity (dyspro- sodia) [20,21]. In expression, it is not unusual for the same lesion to impair both facial and vocal affect [22,23], imply- ing a common biologic substrate for both modes of emotional expression.

Language Mechanisms. From neuropathologic analyses of Broca aphasia and Wernicke aphasia, it was well known in Lenneberg’s time that important oral-motor control centers for language are located in the posterior portion of the left inferior frontal gyms and that language undergoes auditory analysis in the posterior portion of the left superior temporal gyrus [24]. Postmortem studies revealed that structures in this area typically are larger in the left hemisphere than in the right [25]. This asymmetry is congruent with studies of function which reported that spoken and written language are processed grossly by the left ‘cerebral hemisphere primarily in nearly all right- handed individuals and in the majority of left-handed individuals.

Language lateralization does not appear to develop later in childhood or gradually over the first few years of life, as was believed by Lenneberg and his contemporaries. Rather, speech disproportionately activates mechanisms in the left hemisphere as early as the third month postnatally [26]; congruently, the left planum is already larger than the right in the final trimester of fetal life [27]; however, there are many different components of spoken language and

.m# P~LURIC NEUROLOGY Vol. 8 No. 4

vocal communication and some are processed primarily in the right hemisphere. Among these components are vocal prosody (variations of vocal pitch, tempo, and loudness) and vocal affect (expression of mood, emotion, and atti- tude) which are interpreted mainly in the right hemisphere.

In a second type of prosody, linguistic prosody, stress variations distinguish noun and verb forms of two-syllable words (e.g., conflict, conjkt), and differentiate lexical compounds from adjective-noun combinations (e.g., greerzhouse, green house). The interpretation of linguistic prosody and the identification of spoken and written words typically are conducted in the left cerebral hemisphere. Consequently, a patient who cannot understand or express linguistic messages is likely to have a disturbance of the left hemisphere, while a patient who speaks in a monotone or with a lifeless facial expression, or misses the emotional force of a message, may have a lesion in the right hemisphere, particularly in the basal ganglia [28].

Signed Languages. The human capability for spoken languages extends completely to languages that are signed. Such languages appear to be as rule-governed, efficiently transmitted, flexible, and semantically rich as spoken ones. Infants raised by signing parents acquire manual languages just as readily as spoken ones, and use them with equiva- lent degrees of creativity and complexity [29].

The language control centers of profoundly hearing-impaired individuals who communicate with manual signs also are lateralized to the left [30]. Consequently, a stroke on that side of the brain may produce aphasia for sign. This phenomenon suggests that whatever sensorimotor links to communication control centers may have existed in prelinguistic history [3 11, the brain mechanisms responsible for language are amodal.

As is now well known, efforts have been made to teach manual languages to primates. These studies reported that primates had some capability for signing (arguably with less than a human degree of flexibility and naturalness) and also had some capability to follow fairly complex spoken commands [32].

Structural Causes of Developmental Language Disorders

At the time of Lenneberg’s studies, there was little evidence of structural deficiencies in most children who were slow to develop language, although he suspected that genetic and neurologic factors may be involved in such patients. There now is evidence of a family history and abnormal brain development in dyslexia, language delay, autism, and stuttering.

Dyslexia. Family history studies revealed an elevated incidence of reading and writing problems in families of dyslexic children [33] and linkage studies suggested a polygenic mode of transmission. Postmortem and imaging studies demonstrated that in dyslexics the planum tem- poralis usually is the same size in both cerebral hemispheres [34,35].

Language Delay. Because many dyslexic individuals have subtle difftculties with spoken language, it is not surprising that speech-delayed children also have neurologic findings similar to those of reading-delayed children. This population includes a higher than normal proportion of males [36]. Recent studies indicate that first-degree relatives of children with delayed language report diicul- ties in learning to speak at greater than normal levels [37-391. Because in most cases the parents’ own speech has not been substandard, the assumption is that these intrafarnilial difficulties are due to genetic rather than to environmental factors. This assumption needs to be con- firmed with more precise methods (e.g., twin studies). As for brain structure, studies using magnetic resonance imaging recently reported symmetric plana in children with delayed language and normal, asymmetric plana in normally developing peers [40,41].

Autism. Autistic children are preponderantly male [42] and are more likely than nonautistic children to be right- or weakly left-hemisphere dominant for language [43]. Twin studies revealed a significantly higher concordance for autism in monozygotic than in dizygotic twins [44]. Neuropathologic studies identified a number of abnormal- ities in the nuclei of the forebrain, the amygdala and the cerebellum [45].

Stuttering. Lie autism, stuttering is more prevalent in males. There are high familial concentrations of stuttering and higher concordance in monozygotic than in dizygotic twins [46]. Morphometric studies revealed a greater incidence of interhemispheric symmetry among language-related structures [47]; function studies (e.g., dichotic listen- ing studies) disclosed higher rates of atypical hemispheric lateralization in stuttering individuals [48].

An ontogenetic picture emerges, then, in which development of language varies with symmetry of neural structure and hemispheric processing of speech, in association with genetic factors. As neurogenetic effects, anomalous or delayed developmental linguistic processes may, in princi- ple, be detected long before the age at which words would normally be expected.

Precursors to Spoken Language

Research subsequent to Lenneberg’s era has demonstrated continuity between infants’ prelinguistic vocal behavior and the form of their early words. Consequently, it is now possible to predict developmental language disorders from the quality of early vocal and communicative behaviors.

The first steps in the development of spoken language are taken by the fetus. Fetal hearing develops ,and can be tested in the final trimester [49]. Intrauterine vocal leam- ing has been documented [50]. In the first few days:of Ii@, neonates react selectively to their mother’s voiceand the language spoken by the mother duringpregnanoy l&52$ Capabilities that are “present at birth” should not,, the&,be believed to be “innate.”

Locke: Developmental Newolbg!@$ie& >I$$$

Even in infants who have not yet begun to speak it is possible to evaluate progress toward that milestone. This evaluation should take into account vocal turn-taking, gesturing, and babbling.

Vocal Turn-t.aki~g

If infants are to perceive and reproduce speech, it is imperative that they vocalize in turn with caretakers. After an initial period of vocal clashing, the tendency for infants to take turns becomes evident at 12-18 weeks, and may continue to increase thereafter [53]. It is not surprising that Down syndrome infants, who are at considerable risk for language delay, also tend to be delayed in the development of vocal turn-taking [54,55].

Gesturing

Pointing. When infants noticeably look at something, their ocular behavior isolates that object or event from local alternatives. Pointing has the same effect. The context in which pointing occurs helps observers to surmise the infant’s reasons for isolating a particular object or action. Infants normally begin to refer to objects and people by pointing, frequently at 9-12 months of age [56]. This piece of emergent communication is correlated with later language and develops atypically in infants who are autistic [57].

Mutual Gaze. Much lexical learning is facilitated by the mother’s desire and ability to determine what her child is looking at. Typically, a mother tends to name a toy at the moment she sees her child looking at it [58]. In this way, verbal labels become correlated with the objects of a child’s attention, which stimulates development of a lexical reference. Infants with Down syndrome tend to be delayed in the development of these mutual gaze pat- terns [59].

Babbling

In Lenneberg’s day, “babbling” was believed to be any kind of vocal play by infants. Now this term is restricted to the production of well-formed syllables, which normal infants suddenly begin to produce at 6-10 months of age, regardless of which language is spoken around them [60]. These syllables are the audible result of alternated man- dibular closures with relatively passive positioning of the lips and tongue. The resulting vocalizations resemble syllables, usually of the consonant-vowel type. They occur singly (e.g., %a”) or in reduplicated strings (e.g., “dada- da”) and sound very much like speech [61].

As infants develop, there is an increase in the number, phonetic range, and complexity of their vocal maneuvers. At 9 months of age, the majority of an infant’s noncrying vocalizations are vowels and consonant-vowel syllables in which the consonant is released explosively from an oral closure (e.g., “ba” or “da”), nasally emitted (e.g, “ma” or

“na”), or glided into the vowel (e.g., “wa” or “ya”). In a 30-min play session, one would expect to hear at least 15 different consonant sounds at this age. By 12 months of age, there usually are more sounds that are made with complete oral closures and a richer mixture of consonants and vowels within an utterance [62,63].

Role of Audition. In infants who are born with severe hearing impairments, babbling is delayed, most not beginning until the second year of life [64]. When they do babble, the range of sounds is greatly constricted and their nature qualitatively different [62] which suggests that hearing others speak is importantly related to the timing and complexity of babbling; however, the frequency and complexity of babbling also may depend on the infant’s hearing of his or her own vocalizations. This possibility is suggested by the recent observation that repetitive hand- and object-banging tends to begin just prior to babbling (unpublished data) and by a clinical case study revealing primitive levels of vocalization in an infant previously denied the experience of self-hearing [65].

Motor Factors. The onset of babbling is timed with several other motoric factors, usually beginning within one week of the onset of one-handed (often right-handed) reaching and the onset of rhythmic hand activity. This synchrony and the normally close relationship between vocal and manual activity suggest that babbling may signal the development of mechanisms in the left hemisphere which control repetitive motor activities [60]. Studies by Locke et al. suggested that these mechanisms may be more specifically concerned with stereotyped activities that are associated with sound [66]. If accurate, the onset of babbling should be viewed as a linguistically favorable event, a sign that the brain has undergone an adaptation that is associated with, and perhaps required for, speech.

Down syndrome infants, who typically are late to begin speaking, may not begin to babble, on average, until 36 weeks of age [64]. Because Down syndrome infants typically are delayed both motorically and cognitively, the specific cause of their babbling delay is not well under- stood. Reduced dendritic arborization in infants with Down syndrome [67] may be a factor. Interestingly, damage to the brain of normally developing neonates does not necessarily delay onset of babbling or skew its articulatory content in any systematic way [68].

Role of Health. If babbling were a form of play, we should expect it to be correlated with the general state of the infant’s health because play (including stereotyped motor activities) is more frequent in animals who are heal- thy, rested, and psychologically secure [69]. In humans, there is less play in children who are undernourished; they also are late in reaching cognitive milestones and language [70]. There also is direct evidence that socially neglected infants engage in vocal play less frequently and with less variety than other infants [71].

Diagnostic Signs. There are several reasons why delayed babbling may forecast language delay. It can indicate that the infant’s brain may not have matured to a state

248 PEDIATRIC NEUROLOGY Vol. 8 No. 4

of readiness for speaking. Infants who do not babble are denied the experience of hearing sounds made by their own oral-motor activity. Infants who are aphonic during the babbling period do not begin to babble immediately after phonatory capability is instated [65] and they do not learn to speak as quickly thereafter [72]. As indicated, failure to babble also may index internal conditions that do not favor complex learning (e.g., poor health, discom- fort, fatigue).

True words may not have appeared in the normally developing child by 12 months of age. When the non- speaking child of this age also produces no consonant- vowel syllables or produces only a few sounds recurrently, he or she should be referred to a speech-language patholo- gist for more formal evaluation of vocal, cognitive, motor, and social development. When there is any suggestion of hearing loss, an audiologist should be consulted.

Conclusions

Lenneberg gave developmental neurolinguistics im- petus. The five questions he raised have been pursued by a multitude of researchers from several disciplines. In my view, the best way to recognize his efforts would be to generate a neurolinguistic research agenda for the next 30 years which may include:

(1) Studies of the emergent capacity for social cognition and its neural specialization, matters of critical importance to the development of spoken language. We need to know more about neural responses to facial and vocal expres- sions of emotion and the nature of language acquisition by children lacking normal access to or interest in facial information;

(2) Structure-function correlations in normally developing children and each of the neurolinguistic pathologies, and in brain variations associated with subtypes of spoken language disorders and dyslexia;

(3) Interactions between the genetic factors that deposit SJl normally constituted infants on a path leading to spoken language and the sensory and linguistic experiences that stimulate appropriate brain development and keep infants on that path;

(4) Studies of the degree to which brain development is influenced by experiences provided by the infant’s own actions, whether set in motion by environmental or endo- genous factors; and,

(5) Studies of induced or preserved plasticity in neural systems capable of taking over in case of damage to the phylogenetically preadapted brain mechanisms normally used for language.

This work was partially supported by a grant from the James S. McDonnell Foundation. An earlier draft of the manuscript was read by Leslie Brothers, MD.

References

[l] Lenneberg EH. A laboratory.for speech research at the Chil- dren’s Hospital Medical Center. N Engl J Med 1962;266:385-92.

[2] Lenneberg EH. Understanding language without ability to speak: A case report. J Abnorm Sot Psycho1 1962;6:419-25.

[3] Lenneberg EH, Rebelsky FCi, Nichols IA. The vocalizations of infants born to deaf and to hearing parents. Hum Dev 1965;8:23-37.

[4] Lenneberg EH. Speech as a motor skill with special reference to nonaphasic disorders. In: Bellugi U, Brown R, eds. The acquisition of language. Monogr Sot Res Child Dev 1964;29:115-91.

151 Lenneberg EH. Biological foundations of language. New York: Wiley, 1968.

[6] Asher J. Garcia R. The optimal age to learn a foreign language. Mod Lang J 1969;38:334-4 1.

[7] Aram DM, Ekelman BL, Whitaker HA. Lexical retrieval in left and right brain lesioned children. Brain Lang 1986;27:75-100.

[El Frost DO, Innocenti GM. Effects of sensory experience on the development of visual callosal connections. In: Lepore F, Petit0 M. Jasper HH, eds. Two hemispheres-one brain: Functions of the corpus callosum. New York: Liss, 1986;255-66.

191 Menenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM. Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neural 1984;224: 591-605.

[lo] Neville HJ. Schmidt A, Kutas M. Altered visual-evoked poten- tials in congenitally deaf adults. Brain Res 1983;266:127-32.

[Ill Wolff AB, Thatcher RW. Cortical reorganization in deaf children. J Clin Exp Neuropsychol 1990;12:209-21.

[12] Locke JL. The child’s path to spoken language. Cambridge: Harvard University Press, in press.

[13] Mulford R. First words of the blind child. In: Smith MD, Locke JL, eds. The emergent lexicon: The child’s development of a linguistic vocabulary. New York: Academic Press, 1988;293-338.

[14] Weeks SJ, Hobson RP. The salience of facial expression for autistic children. J Child Psycho1 Psychiatry 1987;28:137-52.

[15] Desimone R. Face-selective cells in the temporal cortex of monkeys. J Cog Neurosci 1991;3:1-8.

[16] Brothers L, Ring B. A neuroethological framework for the representation of minds. J Cog Neurosci, in press.

[17] Meltzoff AN, Moore MK. Imitation of facial and manual ges- tures by human neonates. Science 1977;198:75-8.

[18] Meltzoff AN, Barton RW. Intermodal matching by human neonates. Nature 1979:282:403-4.

[19] Tranel D, Damasio AR, Damasio H. Intact recognition of facial expression, gender, and age in patients with impaired recognition of face identity. Neurology 1988;38:690-6.

[20] Van Lancker DR. Cummings JL, Kreiman J, Dobkin BH. Phonagnosia: A dissociation between familiar and unfamiliar voices. Cortex 1988;24: 195-209.

[21] Ross ED. The aprosodias: Functional-anatomic organization of the affective components of language in the right hemisphere. Arch Neural 1981;38:561-9.

[22] Van Laocker DR, Canter GJ. Impairment of voice and face recognition in patients with hemispheric damage. Brain Cogn 1982;l: 185-95.

[23] Borod JC, Koff E, Larch MP, Micholas M. Channels of em* tional expression in patients with unilateral brain damage. Arch Neurol 1985;42:345-8.

[24] Nolte J. Cerebral cortex. In: The human brain: An introduction to its functional anatomy, 2nd ed. St. Louis: CV Mosby, 1988;335-65.

[251 Geschwind N, Levitsky W. Human brain: Left-right asymmetries in temporal speech region. Science 1%8;161:186-7.

[26] Glanville B, Best C, Levenson R. A cardiac measure of cerebral asymmetries in infant auditory perception. Dev Psycho1 1977;13: 54-9.

[27] Chi JG, Dooling EC, Gilles FH. Left-right asymmetries of the temporal speech areas of the human fetus. Arch Neural 1977;34:346-8.

1281 Cancellierr ABB, Kertesz A. Lesion localization in acquired deficits of emotional expression and comprehension. Brain Cogn 1990; 13:133-47.

[29] Meier RP, Newport EL. Out of the hands of babes: On a pas-

sible sign advantage in language acquisition. Language 1990;66:1-23.

Locke: DevelopmentalNeumlin8uistics 249

[30] Poizner H, Klima ES, Bellugi U. Language across left-lesioned signers. In: What the hands reveal about the brain. Cambridge: MIT Press, 1987;109-32.

1311 Ojemann GA. Common cortical and thalamic mechanisms for language and motor functions. Am J Physiol 1984;246:R901-3.

[32] Savage-Rumbaugh ES. Language acquisition in a nonhuman species: Implications for the innateness debate. Dev Psychobiol 1990; 2x599-620.

1331 Volger GP, deFries JC, Decker SN. Family history as an indi- cator of risk for reading disability. J Learn Disabil 1984;17:616-8.

[34] Galaburda AM, Sherman GF, Rosen GD. Aboitiz F, Geschwind N. Developmental dyslexia: Four consecutive patients with cortical anomalies. Ann Neural 198.5;18:222-33.

[35] Larsen J, Heoien T, Lunderberg I. Odegaard H. Evaluation of the size and symmetry of the plana temporale in adolescents with developmental dyslexia. Brain Lang 1990;39:289-30 I.

[36] Neills JR, Aram DM. Handedness and sex of children with developmental language disorders. Brain Lang 1986;28:53-65.

[371 Lewis BA, Ekelman BL, Aram DM. A familial study of Severe phonological disorders. J Speech Hear Res 1989;32:713-24.

[38] Tallal P, Ross R, Curtiss S. Familial aggregation in specific language impairment. J Speech Hear Dis 1989;54:167-73.

[39] Tomblin JB. Familial concentration of developmental language impairment. J Speech Hear Res 1989;54:287-95.

[40] Plante E, Swisher L, Vance R. Anatomical correlates of normal and impaired‘language in a set of dizygotic twins. Brain Lang 1989;37:643-55.

[41] Plante E, Swisher L, Vance R, Rapcsak S. MRI findings in boys with specific language impairment. Brain Lang 1991;41:52-66.

1421 Mason-Brothers A, Ritvo ER, Guze B, et al. Pm-, peri-, and postnatal factors in 181 autistic patients from single and multiple incidence families. J Am Acad Child Adolesc Psychiatry 1987;26:39-42.

[43] Dawson G, Finley C, Phillips S, Galpert L. Hemispheric specialization and the language abilities of autistic children. Child Dev 1986;57:1440-53.

[44] Steffeberg S, Gillberg C, Hellgren L, et al. A twin study of autism in Denmark, Finland, Iceland, Norway and Sweden. J Child Psycho1 Psychiatry 1989;30:405-16.

[451 Bauman M, Kemper TL. Histoanatomic observations of the brain in early infantile autism. Neurology 1985;35:866-74.

[4q Kidd KH. Recent progress on the genetics of stuttering. In: Ludlow CL, Cooper JA, eds. Genetic aspects of speech and language disorders. New York: Academic Press, 1983;197-213.

[473 Strub RL, Black FW, Naeser MA. Anomalous dominance in sibling stutterers: Evidence from CT scan asymmetries, dichotic listen- ing, neuropsychological testing, and handedness. Brain Lang 1987;32: 338-50.

[48] Sussman HM, MacNeilage PF. Hemispheric specialization for speech production and perception in stutterers. Neuropsychologia 1975; 1319-26.

[49] Biruholz JC, Benacemaf BR. The development of human fetal hearing. Science 1983;222:516-8.

[50] Lecanuet J-P, Granier-Deferre C, Busnel M-C. Differential fetal auditory reactiveness as a function of stimulus characteristics and state. Semin Perinatol 1989;13:421-9.

[Sl] DeCasper A, Hfer WP. On human bonding: Newborns prefer their mothers’ voices. Science 1980;208:1174-6.

[52] Mehler J. Jusczyk P, Lambertz G, H&ted N, Bertoncini J, Amiel-Tison C. A precursor of language acquisition in young infants. Cognition 1988;29: 143-78.

[53] Ginsburg GP. Kilboume BK. Emergence of vocal alternation in mother-infant interchanges. J Child Lang 1988;15:221-35.

[54] Berger J, Cunningham CC. Development of early vocal behaviors and interactions in Down’s syndrome and nonhandicapped infant-mother pairs. Dev Psycho1 1983; I9:322-3 I.

[55] Jones OHM. Mother-child communication with pre-linguistic Down’s syndrome and normal infants. In: Schaffer HR. ed. Studies in mother-infant interaction. New York: Academic Press, I977;379-40 I.

[56] Murphy CM. Pointing in the context of a shared activity. Child Dev 1978;49:37 I-SO.

[57] Mundy P, Sigma M. The theoretical implications of joint-attention deficits in autism. Dev Psychopathol 1989;l: 173-83.

[SS] Collis GM. Visual co-orientation and maternal speech. In: Schaffer HR. ed. Studies in mother-infant interaction. New York: Academic Press, 1977;355-75.

1591 Berger J, Cunningham CC. The development of eye contact between mothers and normal versus Down’s syndrome infants. Dev Psycho1 1981;17:678-89.

[60] Locke JL. Structure and stimulation in the ontogeny of spoken language. Dev Psychobiol 1990;23:621-43.

[61] Oiler DK. The emergence of sounds of speech in infancy: In: Yeni-Komshian GH, Kavanagh JF, Ferguson CA, eds. Child phonology. vol I. Production. New York: Academic Press, 1980;93- I 12.

[62] Steel-Gammon C, Otomo, K. Babbling development of hearing-impaired and normally hearing subjects. J Speech Hear Dis 1986; 51:33-41.

[63] Steel-Gammon C. Prespeech and early speech development of two late talkers. First Lang 1989,9:207-24.

[64] OUer DK. Eilers RE. The role of audition in infant babbling. Child Dev 1988;59:441-9.

[65] Locke JL, Pearson DM. Linguistic significance of babbling: Evidence from a tracheostomized infant. J Child Lang 1990; 17: I - 16.

[66] Locke JL, Bekken KE, Wein D, McMinn-Larson L. Emergent control of manual and vocal-molor activity in reference to human language. Sot Neurosci Abstr 1991;17:177.

[67] Takashima S, Becker L, Armstrong D, Chan F. Abnormal neu- ronal development in the visual cortex of the human fetus and infant with Down’s syndrome: A quantitative and qualitative Golgi study. Brain Res 1981;225:1-21.

[68] Marchman VA, Miller R, Bates EA. Babble and first words in children with focal brain injury. Appl Psycholing 1991;12:1-22.

[69] Bekoff M. The development of social interaction, play, and metacommunication in mammals: An ethological perspective. Q Rev Biol 1972;47:412-34.

[70] Chavez A, Martinez C, Yaschine T. Nutrition, behavioral development, and mother-child interaction in young rural children. Fed Proc 1975;34:1574-82.

[71] Brodheck AJ, Irwin OC. The speech behaviour of infants without families. Child Dev 194617: 145-56.

[72] Simon BM, Fowler SM. Handler SD. Communication development in young children with long-term tracheostomies: Preliminary report. Int J Pediatr Otorhinolaryngol 1983;6:37-50.

250 PEDIATRIC NEUROLOGY Vol. 8 No. 4

Documents

Thirty years of research on developmental neurolinguistics