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1. The Neurobiology Of Language Processing In Adults
The classic theory of the neural basis of language function was based on observations of adults with acquired brain injuries. Approximately 95 percent of adults who develop aphasia after stroke have damage to the left hemisphere (LH). The LH was, therefore, assumed to play a crucial role in mediating expressive and receptive language. Within the LH, Broca’s area (the inferior frontal operculum) was thought to be the neural substrate for speech production and Wernicke’s area (the posterior superior temporal area and supramarginal gyrus of the parietal lobe) the neural substrate for speech comprehension (Caplan 1987).
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New experimental methods that assess the neural substrate of language in awake and processing individuals have revolutionized the classic theory. Language areas are not well circumscribed and are not homogeneous. Researchers have proposed that Wernicke’s area is involved in phonological processing (Petersen and Fiez 1993) and may include the neurocognitive network for the written and spoken word lexicon (Howard et al. 1992). Posterior inferior temporal cortex has also been implicated in lexical and semantic aspects of language comprehension and production (Alexander 1997). Broca’s area has been implicated in syntactic processing (Zurif and Swinney 1994), in verbal short-term memory (Braver et al. 1997), and in phonological processing (Demonet et al. 1992, Zatorre et al. 1992). Other areas of the brain seem to participate in language functioning. The middlesuperior temporal region has been implicated in semantic processing and anterior-superior temporal area in syntactic processing (Mazoyer et al. 1993, Price et al. 1996). Moreover, the dorso-lateral prefrontal cortex (DLPFC) is active during language and reading tasks. The DLPFC may be responsible for modulation of processing in posterior semantic regions, such as Wernicke’s area (Frith et al. 1991, Raichle et al. 1994) or for maintaining verbal information in memory during comprehension of complex sentences (Jonides et al. 1997).
Three lines of evidence suggest that language processing in the normal state may involve bilateral representation, at least under some circumstances. The superior temporal areas in both the LH and right hemisphere (RH) are specialized for processing auditory information (Heﬀner and Heﬀner 1984). Adult stroke patients undergo a period of recovery that leads to increased activation bilaterally during auditory and language tasks (Weiller et al. 1995, Engelien et al. 1995). Finally, fMRI studies with normal adults show that increasing task diﬃculty increases the magnitude of bilateral activation. Homologous areas of the RH become active as the intensity and volume of the neural response within the LH increases. This pattern has been documented for language and working memory (Braver et al. 1997, Just et al. 1996). If bilateral activation emerges during diﬃcult cognitive tasks, these ﬁndings suggest that the relevant neural wiring for language processing may be in place in both hemispheres and utilized when a single hemisphere is unable to complete the task or complete it in a timely manner.
Though research over the last several years has documented the neural systems involved in language processing, very little is known about the processing at more molecular levels of analysis. Obviously, animal models cannot be used to consider these questions. New methods such as Magnetic Resonance Spectroscopy may provide information into energy metabolism in language processing and expand our current knowledge.
2. Challenges In Studying The Neural Basis Of Language Development
The main question that researchers have focused on regarding the neural basis of language development has been to what extent are neural systems organized in advance of language learning? Are the involved areas of brain, even if they are widespread and nonhomogeneous, nonetheless committed prior to language development? Or is the system organized by the very act of learning language? A secondary issue of interest has been whether the dramatic changes in language during the ﬁrst few years of life are stimulated by changes in brain development, such as myelination, or whether the behavioral changes can be accounted for as the outcome of learning. At the present time this second question is addressed only by correlational studies of brain and behavioral developments and is thus highly speculative in terms of causality. This research paper will not address that issue.
Currently, our knowledge about the neural basis of language development is extremely limited. A major impediment to the development of the ﬁeld is the paucity of methods appropriate for use in human infants and young children. In adults, neural mechanisms are investigated through a variety of diﬀerent noninvasive functional imaging techniques, such as event-related potentials (ERP), positron emissions tomography (PET), and functional magnetic resonance imaging (fMRI). Each of these methods has advantages and limitations; considering them together assists in piecing together a full account of the neural basis of language function. In children, PET scanning has been avoided—except in children with clinical indications for its use—because the tests require exposure to ionizing radiation. Functional MRI involves no exposure to ionizing radiation but requires an awake and responding subject to hold still. Even minimal movement by a young child renders it impossible to detect the minimal diﬀerences in activation between baseline and experimental conditions. Children less than 7 years of age cannot usually comply with the stringent requirements of the scanning. Therefore, for infants and young children, the only direct method of functional imaging that has been used successfully is ERP.
An indirect method for addressing the neural underpinnings of language development has been to study children with early lesions impinging on classical language areas of the cortex. If, the argument goes, children with damage to the usual language areas have serious delays and disabilities in aspects of language functioning, then the implication is that the neural mechanisms for those aspects of language development were probably present prior to the injury. If the damage occurred around the time of birth and language performance is impaired, then the inference is that specialization is congenital, and possibly determined or initiated by genetic mechanisms. If children with early brain injuries successfully master language, then the implication is that, at least under extreme circumstances, alternative organizations within the human brain for language are possible.
This experimental strategy also has serious limitations. Early focal brain injury in childhood is rare and, unlike the situation in adults, the causes are diverse. Studies in the 1970s and 1980s enrolled children with hemidecortication for intractable seizures in Sturge– Weber syndrome, a vascular malformation of the brain and overlying skin (Dennis and Kohn 1975, Dennis and Whitaker 1976), and children with embolic strokes sustained during cardiac procedures to treat congenital cardiac disorders (Aram et al. 1986, Aram and Ekelman 1987). In these populations, the age of onset and extent of injury both vary. More recently, studies have enrolled children with strokes that occurred in utero or in the perinatal period. Though the age of onset of this population is narrow and the injury preceded any language development, the locations of injury still vary substantially. Furthermore, the study of children with early focal lesions is challenging because the language capabilities of the young infant had no injury occurred are uncertain, whereas the capacities of adults can be inferred from their previous functioning and occupation. Other variables and coexisting conditions such as seizure disorder and use of anticonvulsant medications appear to mediate outcome (Dall’Oglio et al. 1994).
3. Evidence From Behavioral Data
Behavioral data suggest that language development has a strong biological basis. Language development begins when a child approaches one year of age and reaches almost adult levels of competence by the time that the child enters school. The rapidity of that development, at a time when other skills—basic adding and substracting, playing chess or riding bikes—are rudimentary suggests a strong biological predisposition or preparedness. Prelinguistic infants demonstrate processing biases before they have had much exposure to language. For example, they categorically discriminate phonetic contrasts, even those that are not found in the native language and therefore not part of the linguistic environment (Eimas et al. 1971, Best et al. 1988). They become tuned to the phonetic contrasts in their native language in the second half of the ﬁrst year, as their babbling approaches the sound patterns of the adult language (Best et al. 1988). These processing biases may provide the mechanisms that infants use to begin to segment and/organize the sound stream to which they are exposed. Though it is tempting to assume that the mechanisms are innate, neonates also show preferences for their mother’s voice, though they do not recognize their mother’s face (Burnham 1993). Thus, prenatal exposure to the mother’s voice in utero, rather than some innate bias, is likely responsible for the early preference. Interestingly, when infants start learning to map words to meaning, they confuse similar sounding words, suggesting that they are not able to capitalize immediately on their speech discrimination skills when they begin to acquire verbal language. The neural basis of language development may involve forming connections between the neural substrates involved in speech perception and language production.
Behavioral data also suggests a strong environmental component to language development. In the area of vocabulary development, the rate of vocabulary growth is a function of the amount of maternal input the child hears (Huttenlocher et al. 1991). In the realm of syntax, children ﬁrst learn features that are highly regular and prosodically prominent. Diﬀerences in the features of the adult language seem to explain some diﬀerences in the order of acquisition across languages.
4. Evidence From ERP And fMRI
Using ERP techniques on normal children learning language, a picture emerges that initial development of language requires a wide and bilateral neural network and that progressive neural specialization and lateralization occurs in association with language experience rather than strictly with age. Speciﬁc ERP components in toddlers 13 to 20 months of age demonstrate diﬀerences between words that the child understands and words that are incomprehensible. Word comprehension shows both age and experience components. At 13 months of age, the comprehension eﬀects can be found over both the right and left hemisphere and over anterior and posterior regions. By 20 months of age, the eﬀects are detectable only over the posterior left hemisphere. However, younger toddlers who are more advanced in language development show this laterality eﬀect at a younger age than do less advanced children (Mills et al. 1997).
Data from children with early focal brain injury corroborate the view of initial bilateral involvement in language development. Children with focal injury to either hemisphere experience developmental delays in prelinguistic skills, including the onset of babbling and communicative gestures (Marchman et al. 1991) and in the onset of vocabulary development and use of word combinations in parent–child conversations (Feldman et al. 1992, Thal et al. 1991). Once the children with focal injury begin to acquire functional vocabulary and syntactic skills, their rate of developmental progress as measured by vocabulary use and mean length of utterance is comparable to each other and to children developing typically (Feldman et al. 1992). By age 4, children with focal LH damage can even master the complex morphosyntactic structures of a language like Hebrew (Levy et al. 1994). However, at school age, children with damage to either the LH or RH show delays compared with children developing typically in the creation of narrative discourse (Reilly et al. 1998). These ﬁndings are suggestive that both hemispheres participate in advanced language skills such as narrative discourse in school aged children.
Research also indicates that individual diﬀerences in developmental rate relate to the location of injury. Children ages 10 to 17 months of age with RH damage have been shown to have greater initial delays in word comprehension and production than do children with LH damage. However, at the point of word and syntax development children with LH temporal lobe injury demonstrate slower development than do those with damage to other areas of the RH or LH (Thal et al. 1991). These data are compatible with a view of increasing specialization during language development. However, it is important to note that individual diﬀerences also relate to other variables besides the size and site of the lesion, such as the presence of seizures and the use of anticonvulsant medications (Dall’Oglio et al. 1994).
Studies using fMRI in children developing typically demonstrate that predominant LH activation during language tasks is present by about age 7 to 9 years, and as with adults, bilateral activation occurs under some circumstances. The activation of neural networks on fMRI was studied during sentence processing in adults, normal school aged children and also children with perinatal focal brain injury (Booth et al. 1999, 2000). In a relatively natural linguistic task, children listened to sentences and then responded true or false to a statement about each sentence. Adults and children show lower accuracy levels to diﬃcult objectrelative sentences, such as ‘The pig that the dog jumped ate the trash in the street,’ intermediate accuracy to moderate subject-relative sentences, such as ‘The principal that tripped the janitor used the phone to call home,’ and highest accuracy levels to relatively easy conjoined-verb-phrase sentences, such as ‘The cat chased the rabbit and enjoyed the hunt in the yard.’ However, children are less accurate than are adults. Children, as well as adults, are more accurate when true–false statements test for the subject of the ﬁrst verb, for example, ‘The dog jumped the pig,’ than for the subject of the second verb, for example, ‘The principal used the phone.’
In adults, the fMRI showed that the sentence comprehension task produced more activation in the LH than in the RH. The greatest activation was found in the superior temporal, middle temporal, and inferior frontal areas, the traditional language areas but also in prefrontal areas, the brain region associated with working memory. Healthy children activated similar neurocognitive networks as did the adults with LH predominance. However, the distribution of activity across these networks was related to response accuracy, strategy use, and task diﬃculty. Greater activation was associated with higher response accuracy and with consistent use of a comprehension strategy, whether correct or incorrect. Improved performance was also associated with more activation in the anterior middle temporal area suggesting that this area was important in the syntactic processing demanded by the task. Activation of occipital regions was greater in children who were less accurate in the task. These ﬁndings suggest that some children may have been using a diﬀerent and immature strategy in complex sentence processing, possibly trying to visualize the sentence as an aid to comprehension. In both normal adults and children, the number of areas activated correlated with the diﬃculty of the sentences. The RH was recruited for diﬃcult sentences (Booth et al. 2000).
Children with LH damage showed patterns of activation consistent with organization of cognitive processing into homologous areas of the contralateral hemisphere. The size of their lesion was associated with the degree of their cognitive deﬁcit. These results conﬁrmed earlier ﬁndings of RH language in many individuals with left hemisphere damage undergoing a carotid amytal infusion (Rasmussen and Milner 1977).
Studies of children with LH damage indicate that though the RH can participate in language processing, the LH has a more central role in language tasks at school age. Dennis and co-workers found that despite comparable intelligence, children with LH hemide-cortication were inferior to children with RH hemi-decortication on the ease and speed of syntactic discrimination, interpretation of passive negative sentences, and repetition of syntactically complex sentences (Dennis and Kohn 1975, Dennis and Whitaker 1976, Dennis 1987). Aram and co-workers similarly found expressive and receptive syntactic diﬃculties in children with LH focal damage from embolic events (Aram et al. 1986, Aram and Ekelman 1987). However, it is important to note that children with LH damage acquired in early infancy or child- hood have only subtle deﬁcits, and are not frankly aphasic as are adults with comparable lesions.
It is diﬃcult to assess if syntax is particularly vulnerable in children with these lesions acquired later in life. An alternative hypothesis is that subjects with LH damage had greatest diﬃculty with the most developmentally advanced items on the assessment (Bishop 1983). Children with LH injuries and LH perinatal damage also show diﬃculty in tests of comprehension of diﬃcult verbal material, formulating sentences, and lexical retrieval (MacWhinney et al. 2000).
To determine the speciﬁcity of underlying information-processing deﬁcits after early injury, MacWhinney et al. (2000) used on-line reaction time methodology. School-aged children underwent visual and auditory tasks of signal detection, recognition, and choice as well as rapid naming to visual and auditory stimuli. The results showed that children with LH, RH, and with mixed lesions generally were as accurate as age- matched controls but consistently had slower reaction times. The reaction times of normal learners lawfully decreased as the children went from 5 to 10 years of age. Similarly, in the subjects with early lesions, the reaction times became shorter as the children got older and the slopes suggested that by adulthood the reaction times might converge. The two tasks that best distinguished children with LH injuries from children with other lesions were verbally repeating numbers presented in the auditory mode and naming numbers presented in the visual mode, though there was considerable overlap across groups. Interestingly, both these tasks required phonological access and verbal output.
Taken together, these ﬁndings on school-aged children suggest that despite adequate functional communication skills, children with LH injuries may have more diﬃculty than do children with other lesions performing precise, constrained, high-level language tasks, particularly in tasks that require speed. The areas of greatest diﬃculty seem to be developmentally challenging syntactic skills, comprehension of diﬃcult oral directions, and formulating sentences with a constrained vocabulary. Phonological access, as evidenced in naming and repeating verbal items, also diﬀerentiates subjects with damage to the LH from other children without injuries.
Study of the neural basis of language function is advancing rapidly in the era of neural imaging and related methods. Study of the neural basis of language development is lagging behind because many of the techniques are not appropriate for children. The early emerging picture is that sensory processing mechanisms that are called on for initial segmentation and/organization of the linguistic stream are present at or even before birth. However, these processing biases are not immediately available to true verbal development. Language development seems to use a broad and bilateral neural network at each stage. That network becomes more constrained and specialized to the LH as a function of language experience. However, bilateral activation remains possible in normal functioning, for example, when tasks are diﬃcult and in circumstances of brain injury. Adult patterns of neural activation are present by school age and show LH predominance. However, children with LH damage may use homologous regions of the RH for sentence processing. Hopefully, in the near future new experimental techniques will allow greater detail and understanding of these processes and will begin to explain individual diﬀerences in children developing typically and children with a variety of developmental disorders.
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