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Behavioral assessment of language brain processing in the first year of life
Accepted Manuscript Behavioural assessment of language brain processing in the first year of life Francesco Guzzetta PII:
S1090-3798(14)00079-8
DOI:
10.1016/j.ejpn.2014.04.015
Reference:
YEJPN 1786
To appear in:
European Journal of Paediatric Neurology
Received Date: 28 December 2013 Revised Date:
16 April 2014
Accepted Date: 27 April 2014
Please cite this article as: Guzzetta F, Behavioural assessment of language brain processing in the first year of life , European Journal of Paediatric Neurology (2014), doi: 10.1016/j.ejpn.2014.04.015. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Behavioural assessment of language brain processing in the first year of life Francesco Guzzetta (Child Neurology and Psychiatry, Catholic University, Rome (Italy) Prof. Francesco Guzzetta Via Boezio 2 I-00193 Roma Tel. 3473316159 e-mail: [email protected] Review Key words; early language assessment; language brain processing; early development; early language disorder; newborns at risk Running title: auditory brain processing in the first year of life Abstract An up-to-date review of the behavioural assessments of language development in the first year of life is reported. After recalling the anatomical bases of the early development of the auditory system, the different stages of language development during the first year of life are considered: discrimination, transition and perception. The different kinds of behavioural assessment during the course of the first year are then described by stressing their indications and limitations. Human newborns are extraordinarily competent in the world of sounds and speech. They are able to cortically process acoustic features of language: rhythm (1, 2), stress and prosody (3), voice timber (4). speech (5-7) or native language (8). On the contrary, vocal production appears extremely poor. Such apparent physiological asymmetry might depend on different levels of maturation. The first sign indicating the ability to discriminate between the spectro-temporal features of sounds is demonstrated by neurophysiology: an electrophysiological response to changes of auditory inputs (deviant stimulus) after a repetitive stimulation with the same sound (standard stimulus) is revealed as a modification of the evoked potential, called mismatch negativity (MMN). MMN can be recordable even without attention (which makes possible the assessment in the neonate), and testify the ability of discrimination and recognition memory, capturing the first manifestations of cognition at birth. However, a number of other techniques are used to assess speech perception skills in infants during the first year of life, including those based on psychophysical responses (changes in gross movements or sucking; neuro-vegetative reflexes) or on intentional motor behavior. Anatomical and physiological bases of early auditory development There is an evident correlation between the maturation of acoustic cerebral pathways and the development of auditory function. I refer to the review of Eggermont & Moore (9) for a detailed analysis of the anatomical and physiological development of auditory cerebral structures, while I summarize here the main features of this development during the third trimester of gestation and the first year of life. During this period two stages of the auditory function maturation can be distinguished. The first one refers to the ability to discriminate, i.e. to recognize the differences between simple sounds or any speech phonemes. The second one refers to the ability to perceive, i.e. to recognize speech structure up to link the stimulus to its meaning. Discriminative abilities of acoustic stimuli are already present in the last trimester of gestation at a time when only brain stem and cortical marginal layers seem to have reached the early steps of maturation. At that time there was the emergence and initial growth from the cochlear nerve to thalami of axonal neurofilaments (first apparent in histochemical studies at about the 16th week of gestational life), followed by myelination visible by 27-29 weeks of fetal life, with increasing dendritic arborization and synapse formation. All that corresponds to the function of one subsystem underlying discrimination, responsible for the first analysis of stimulus features.
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The second important subsystem expressing the parallel cortical maturation essentially consists of the temporary organization of the marginal layer This layer is mainly made of intrinsic transitory neurons, Cajal Retzius (CR) cells whose main role is attracting migrating neurons to form cortical layers, and of cell processes consisting of axons and dendrites, in particular coming from the peripheral pathways through the reticular ascendant system (RAS). Brainstem with its peripheral afferents and the marginal layer are thus the anatomical substrates for the discrimination processing in this first period of life. The second stage of auditory function starts at the beginning of the second semester of life and consists of the anatomical maturation of the cortex and its connections. Axonal neuro-filaments and myelination progressively involve auditory radiation, while cortex lamination is achieved. At this stage, the role of marginal layer is changing, going through the apoptosis of CR cells and the development of new transcortical connections. New connections with medial geniculate body will eventually substitute RAS. Maturing cortex thus becomes the substrate of perception. Cortical maturation is obviously dependent on sensory inputs as demonstrated by the negative effects of hearing loss and conversely by the positive consequences of deprivation correction by early cochlear implants. Pre-cognitive abilities In the very first months of life the reception of the auditory stimulus is mediated by several abilities usually considered as pre-cognitive because of the absence of an operational awareness. Information processing model gives an useful frame to explain the first steps of development through the individuation of individual basal abilities including auditory function [10]. There are several tools based on the information processing model to asses cognitive competence of young infants [11]. Similarly to MMN, they generally assess the ability to discriminate a novel stimulus from an old one that has left a memory trace. Among these tests, the Fagan test of infant intelligence (FTII) [12] has shown its good predictive ability as to subsequent cognitive development [13], definitely higher than that of traditional developmental scales [14]. There is an increasing body of literature investigating the role of pre-cognitive abilities on language development [15-19]. Some basic functions were particularly studied to predict later capacity of language development: visual recognition memory, speed of information processing, attention, and representation ability. Visual recognition memory is based on the child's preference for novel stimuli using the paradigm of comparison between two paired stimuli [20], and is expressed by a score of novelty given by the percentage of time spent by infants in looking at the novel stimulus in relation to the total time spent in looking at both stimuli (familiar and new). Stimulus familiarity has foundation so in the phenomenon of habituation, expressing the progressive loss of interest for repeated stimuli which leave a memory trace. As a result, the new interest of the infant observed when the stimulus changes (dishabituation), can be seen as a measure of discrimination ability. A better visual recognition memory in the first months of life correlates with better understanding of language in the following months, [21] and better ability of expression (lexicon and morpho-syntactic rules) in the following years [19, 22]. The speed of information processing in infants is tested as a measure of response time in a paradigm of "violation of expectation" (orientation towards foreseeable or unforeseeable events) [23] or as a measure of the time to encode information using familiarization (familiarization time) [24]. Although this approach showed some predictive value for later cognitive development [25], little is known on its predictive
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value for language development [26]. However, it appears convincing that the processing speed can influence positively the development of language, as shown by tests for RAP (rapid auditory processing) performed in early ages. They demonstrate how language development is based on the ability to process efficiently and accurately short auditory stimuli presented in rapid sequences [27] (see below). Measuring the evolution of visual attention in the first few months of life can provide some useful information about the maturation of the attentive function, from the subcortical visual skills up to selective attention [28]. Looking at times and rate of displacement (shift) of gaze, as visual indicators of ability to direct the gaze towards objects of interest, was useful in predicting cognitive development [29, 30]. Shared attention and eye contact are certainly at the basis of language, although specific contributions about the influence of attention on language development are scarce and contradictory [31, 32]. Representation competence is defined as "the ability to extract common points from the experiences and to draw an abstract or symbolic representation " [19], all skills necessary to the development of language. To detect such skills in infants, a number of assessment techniques were proposed with various targets: tactual-visual cross-modal transfer, where information about shape is extracted from one modality and applied to another [33], anticipation of events that requires rule abstraction in placement of details in a series of images [34], object permanence which concerns the ability of keeping in mind a hidden object [35] and symbolic game which consists of using one object to represent another one [36]. All these tests, particularly the last two, gave results useful to predict language development [37, 38]. The examinations of the so-called pre-cognitive functions, detected by techniques inspired by the model of information processing provides therefore reliable information about the development of language. The phase of discrimination Auditory discriminative abilities are acquired in the first phase of development, from 28 weeks of gestational age to six months of life. Such kind of discrimination between two sounds belonging to speech or not (universal discrimination) does not need attention, at least conscious attention; it belongs to the pre-attentive stage of auditory processing, consistent with age-specific anatomical-physiological features (see above), auditory inputs coming from the bottom (sensory peripheral structures) without a higher control [39]. The way to investigate discrimination abilities when motility is not yet intentional (pre-praxic stage) consists of examining rudimentary motor responses, non nutritive sucking, orienting reflex, or neurovegetative behaviours (e.g., heart rate changes). Also visual fixation times, when visual targets are associated with speech stimuli may express discrimination abilities and looking time may show the preference towards a kind of linguistic or non-linguistic sounds [40]. Similarly, habituation with specific audio-visual targets allows to check discrimination in infants that prefer new stimuli instead of habituated standard stimuli [41]. At this stage, especially in the first weeks factors more linked to “musical” features of speech (rhythm, prosody) than to phonetic components are predominant, as shown by adaptive changes of the mother speech in order to favor the baby comprehension: high tone exaggeration, slowing of verbal flux, inserting long pauses and stressing the rhythm (motherese is the name to indicate this kind of speech). This particular speech is clearly preferred by infants [40], which in a first stage prefer the maternal source of speech compared to the style of elocution. The attraction towards motherese however ,decreases with time [42], paralleling the progressive loss of ability to discriminate contrasts of non-native language. The relevance of the relational dimension at this early stage of language
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development has led to stress its emotional aspect (vocal emotion) [43]. The preference for the exaggerated characteristics of motherese could come from sensitivity to its emotional value more than to its intrinsic characteristics [44]. But, even more, the maturation of first language appears to depend on a dynamic and mutual relationship between the child and the mother [45]. The reduction of abilities to discriminate between hundreds of possibilities to a few tens of phonetic sounds belonging to native language is particularly characteristic of the last part of this stage. The gradual approach to a selection of only the speech contrasts of the native language is mainly the result of a learning activity relating to phonetic contrasts, to which the child is usually exposed (statistical learning of distributional frequency). Assessment techniques in the discrimination phase. Most assessment techniques in the discrimination phase are experimental and have had a fundamental value in the advancement of knowledge on the processing of auditory stimuli in this stage of development. Early assessment studies inclusive of a more or less prolonged follow up to highlight any predictive capability in language development or, more generally in cognitive development, although not yet commonly used in clinical practice, have a true clinical significance. This type of study, which provides tools for early treatment and prevention of language developmental disorders may give useful information for understanding some mechanisms of speech development [46]. Although there are controversial data on the role of the auditory processing of acoustic non-linguistic stimuli in respect to the phonological structure of speech [47], observer-based methods during the discriminative stage are generally used to measure the ability to respond to novel acoustic stimuli (linguistic or not). Babies on the caregiver’s lap inside a soundproof booth undergo repeated acoustic stimulations alternating with a novel one. An observer outside the booth starts stimulation trials blindly and checks psychophysic behavioural response (see above) to stimulus change. An experimenter inside the booth helps the observer to keep baby’s attention alert [48]. Another protocol to measure the auditory processing abilities in this period takes advantage of visual fixation during acoustic stimulation. The comparison between looking times after presentation of repeated visual target generating two kinds of acoustic stimuli allows the evaluation of stimulus preference. The preference may be also assessed after the habituation to a standard stimulus to test the discrimination with a novel stimulus [49]. This preferential looking intermodal paradigm is widely used in research and now extended to the clinical-diagnostic use [50]. A different kind of evaluation in these first months of life, based always on habituation and recognition memory, may concern suprasegmental (not referring to phonetic features) parameters, e.g. to measure a skill to accurately process repetitive, short and rapid (RAP, rapid auditory processing) auditory stimuli, linguistic or not [51]. The ability to perform the analysis of stimuli sequences (in the range of tens of milliseconds) will allow the construction of maps of phonetic language [52], and its difficulty can predict a disorder of language development [53] Transition from discrimination to perception Around the sixth month, discrimination stage based on sub-cortical mechanisms ends and perception induced by the experience of native phonetic contrasts becomes operational, with always higher involvement of cortical activity. Indeed, transition in auditory processing is progressive, grossly around between 4th and 6th month; however, what is the direction of the maturation process in the other various developmental parameters?
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If another relevant sensory processing, the visual one is considered, at about the 4th month specific tests such as fixation shift under competition shows the achievement of cortical involvement in visual function [28]. In the same way the transition from the pre-praxic stage to that of intentional motility occurs around the 4th .month. The acquisition of the first praxia is the gateway into the world of cognition [54]. Intentional movements may evidently represent cortical involvement in conscious responses to sensory stimulation. During the same period attention matures from the pre-attentive stage to selective attention, moving from a bottom-up way through the reticular ascendant system (attention is driven by stimulus salience) to a cortical modulation in selecting the target. Hence, exactly at the age of 3-4 months there is a definite anatomical-functional turn that underlies the transition from subcortically to cortically dependent functions, namely as to auditory processing from discrimination to perception. The phase of perception (second semester) The beginning of this period corresponds to the achievement of phonemic categorization, i.e. acquisition of sensitivity to the phonetic categories of the native language, with loss of sensitivity towards intermediate phonetic units: e.g., Japanese babies will not be able anymore to discriminate between l and r, belonging to the same category in their language. Such ability to perceive phonetic categories is achieved at the age of six months when native language has been fully acquired with an almost “magnetic” mechanism (native phonemes operate like a magnet in selecting phonetic contrasts infants can process) [52, 55]. Going into the perceptive stage with all described architectural changes of cognition (cortical processing of auditory stimuli), aims of infants during the second semester of life will concern the identification of word forms through the segmentation of the continuous speech flux. Such segmentation, initially regarding phonological features would occur through another statistical mechanism. Mainly, it refers to the higher frequency with which infants meet adjacent syllables belonging to the structure of the same word in comparison to the less usual adjacent syllables belonging to distinct words. This kind of statistical selection is named the method of “adjacent transitional probabilities”. Further speech cues help word identification such as prosody and other emotional relational factors [56], but also cues highly dependent on cognition (stress pattern, phonotactic rules). Particular relevance has been given to the effects of relational factors on perceptive abilities of the infant in language learning (social gating theory) [57]. That is supported by mirror neurons theory [58]. This particular neuronal component involving at the same time perception and action appears especially engaged in language learning [59]. Around the end of the semester, the infant acquires the symbolic function associating the word form to its meaning (age of the first lemma production); in the following years grammatical and syntactic function will develop. The semantic component will be another strong cue for segmentation. Behavioral assessments in the perception phase Behavioral assessments concerning the progressive acquisition of perceptual abilities in the second semester of life are essentially based on the paradigm of head turning (HT) with bimodal stimuli (visual-acoustic), usually reinforced by operant conditioning (visually reinforced conditioned head-turn paradigms). Babies on the lap of their mothers, inside a soundproof booth, are first trained to associate the target sound with a visually interesting scene and then tested measuring the correct orientation of HT towards desired visuo-auditory stimuli [60].
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Cognitive abilities (sustained attention, speed of encoding, ability to consolidate information into memory, selective orienting, learning) are in this case evidently involved So, it is important to keep attention alert during the assessment. The same technique has been used to assess the ability to perceive RAPs when cognitive competence (intentional motility) fully allows HT behavior [52, 60]. Predictive abilities of these assessments [61] are now considered in the context of a speech development supported by the bootstrapping model (metaphor of the small rings to strap boots). Phonetic perception would stimulate segmentation that further produces semantic association (word form meaning). Then, there will be a cascade up to build morpho-syntactic features. Limits of behavioural techniques Methodology performed to check the first acquisitions of language during the first year of life has been generally experimental and has been seldom used in clinical practice because of several technical limits . First of all results of these assessments are generally at a group level and do not account for individual performances. Groups more frequently considered are preterm newborns vs term born or belonging to families at risk of presenting language developmental disorders. The lack of individual results prevents their full clinical use for prediction and early treatment of eventual disorder. Panneton & Newman [49] underline the relevance of the variability of responses inside the same group; some infants seem to prefer novel stimuli while others are more sensitive towards familiar ones, so significantly contaminating results of studies [62]. Furthermore, the complexity of assessments makes difficult their application. In particular, the strong dependence of the success in the test by the attentive ability makes flimsy the judgment on the results. Last but not least, it is not always easy to bring the child's behavior in the setting of the examination to the usual condition of multiple environmental stimulation. Integrative assessment techniques: neurophysiology and neuroimaging Neurophysiology Evoked potentials are especially useful, because they allow to follow the path of sensory inputs with a reliable correspondence with the recording time even though change generators of potential remain approximate. Auditory evoked event-related potentials (AERP) are widely used to assess the auditory brain function or its disorders, both in its exogenous component (simple response to acoustic stimulation) and endogenous (such is the case with the MMN). Regarding the latter, it is a derived value, resulting from a subtraction of the potential obtained from standard stimulus from that produced by a new stimulus (it is the mode of the oddball paradigm, comparable to what occurs in behavioral techniques of discrimination).. As already mentioned in the introduction, the mismatch negativity, detectable as early as in newborns without their attention participation, testifies to the first expression of "knowledge" in the infant. The peculiarity at this age is that the generators of the AERP, in a period of life so full of structural changes as in the first year of life, determine potential wave forms dynamically different over time, suggesting to call MMN in this phase the mismatch response (MMR) [9]. Indeed, AERPs show a a fronto-central positive response in newborns that progressively decline during the first year of life. So, MMR at birth will be moderately positive to become after some months definitely negative as in adults (MMN). There are several studies using evoked potentials to assess discrimination and perception abilities in the infant [51, 63]. Evoked potentials have been performed, for example, to assess discrimination between native and non native speech in term
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newborns vs preterms at nine months of the gestational age : no difference was found between the two groups showing that maturation predominates on exercise that preterm infants undergo [64]. Such techniques were performed also to draw information predictive of language specific disorders (LSD) [65-68] or generally of cognitive development [69], in order to start a specific early habilitation. Often, studies concern preterm newborns [70, 71]. Another neurophysiological technique, gamma power (gamma oscillations of EEG activity) has been used to early assess language in the context of the cognitive competence [72]. Neuroimaging All the various neuroimaging techniques (structural MRI, functional MRI, near infrared spectroscopy, etc.) are extraordinarily useful for the identification of the brain regions where auditory stimulus is processed. Functional techniques in particular are based on regional increase of blood oxygenation (BOLD, blood oxygen level dependent) in functional MRI, or hemoglobin/oxyhemoglobin ratio in near infrared spettroscopy (NIRS). The interest of neuroimaging studies is relevant, particularly at the beginning of the development. It was surprising to find the result of a structural MRI on infants of 1-4 months which revealed a higher growth of the frontal infero-lateral region (Broca's area), compared to the superior temporal sulcus, testifying an earlier cortical maturation of the auditory dorsal pathway; it is not apparently consistent with the later emergence of speech production [73]. These findings are however compatible with the results of other studies using functional MRI by the same research group that show an early activation of the auditory dorsal pathway [5, 74]. In particular, this research has confirmed the existence of a physiological imbalance of the superior temporal sulcus predominant in the right hemisphere (competent in music processing), consistently with the quoted higher “musical” sensitivity in infants’ speech preference during the first months of life. Neuroimaging studies open new horizons in research related to early speech processing, although there are several difficulties in the interpretation of signals. For example, the cortical activation signal is certainly ambiguous, being able to present as positive (increase the oxygenation of the blood) or vice versa as the negative sign in younger subjects; in the latter case, the reduced vascular capacity to meet the demands of oxygen by the active cortex would produce a decrease in the ratio of oxyhemoglobin to deoxyhemoglobin [9]. Concluding notes The progress made in recent years by studies of auditory and language processing in early ages of life gives us the certainty of being on the brink of a "revolutionary" extension of the clinical use of behavioral assessments, in particular, in the context of diagnostic tools useful for the follow-up of newborns/young infants at risk. The availability of reliable behavioral examination methods to investigate the early auditory and speech development will allow to explore beside motor and visual competences a field whose relevance is outstanding for language and higher cognitive ability development. Hence. new progress in strategies of early specific habilitation will be implemented [75]. References 1) Nazzi T, Bertoncini J, Mehler J. Language discrimination by newborns: toward an understanding of the role of rhythm. J Exp Psychol: Hum Percept Perform. 1998; 24: 756–766. 2) Ramus F, Nespor M, Mehler J. Correlates of linguistic rhythm in the speech signal.
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ACCEPTED MANUSCRIPT An update on the early development of language is reported Different kinds of behavioral assessment during the first year of life are described Indications and limitations of early language behavioral assessments are illustrated
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The diagnostic and prognostic utility of early language assessment is underlined
S1090-3798(14)00079-8
DOI:
10.1016/j.ejpn.2014.04.015
Reference:
YEJPN 1786
To appear in:
European Journal of Paediatric Neurology
Received Date: 28 December 2013 Revised Date:
16 April 2014
Accepted Date: 27 April 2014
Please cite this article as: Guzzetta F, Behavioural assessment of language brain processing in the first year of life , European Journal of Paediatric Neurology (2014), doi: 10.1016/j.ejpn.2014.04.015. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Behavioural assessment of language brain processing in the first year of life Francesco Guzzetta (Child Neurology and Psychiatry, Catholic University, Rome (Italy) Prof. Francesco Guzzetta Via Boezio 2 I-00193 Roma Tel. 3473316159 e-mail: [email protected] Review Key words; early language assessment; language brain processing; early development; early language disorder; newborns at risk Running title: auditory brain processing in the first year of life Abstract An up-to-date review of the behavioural assessments of language development in the first year of life is reported. After recalling the anatomical bases of the early development of the auditory system, the different stages of language development during the first year of life are considered: discrimination, transition and perception. The different kinds of behavioural assessment during the course of the first year are then described by stressing their indications and limitations. Human newborns are extraordinarily competent in the world of sounds and speech. They are able to cortically process acoustic features of language: rhythm (1, 2), stress and prosody (3), voice timber (4). speech (5-7) or native language (8). On the contrary, vocal production appears extremely poor. Such apparent physiological asymmetry might depend on different levels of maturation. The first sign indicating the ability to discriminate between the spectro-temporal features of sounds is demonstrated by neurophysiology: an electrophysiological response to changes of auditory inputs (deviant stimulus) after a repetitive stimulation with the same sound (standard stimulus) is revealed as a modification of the evoked potential, called mismatch negativity (MMN). MMN can be recordable even without attention (which makes possible the assessment in the neonate), and testify the ability of discrimination and recognition memory, capturing the first manifestations of cognition at birth. However, a number of other techniques are used to assess speech perception skills in infants during the first year of life, including those based on psychophysical responses (changes in gross movements or sucking; neuro-vegetative reflexes) or on intentional motor behavior. Anatomical and physiological bases of early auditory development There is an evident correlation between the maturation of acoustic cerebral pathways and the development of auditory function. I refer to the review of Eggermont & Moore (9) for a detailed analysis of the anatomical and physiological development of auditory cerebral structures, while I summarize here the main features of this development during the third trimester of gestation and the first year of life. During this period two stages of the auditory function maturation can be distinguished. The first one refers to the ability to discriminate, i.e. to recognize the differences between simple sounds or any speech phonemes. The second one refers to the ability to perceive, i.e. to recognize speech structure up to link the stimulus to its meaning. Discriminative abilities of acoustic stimuli are already present in the last trimester of gestation at a time when only brain stem and cortical marginal layers seem to have reached the early steps of maturation. At that time there was the emergence and initial growth from the cochlear nerve to thalami of axonal neurofilaments (first apparent in histochemical studies at about the 16th week of gestational life), followed by myelination visible by 27-29 weeks of fetal life, with increasing dendritic arborization and synapse formation. All that corresponds to the function of one subsystem underlying discrimination, responsible for the first analysis of stimulus features.
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The second important subsystem expressing the parallel cortical maturation essentially consists of the temporary organization of the marginal layer This layer is mainly made of intrinsic transitory neurons, Cajal Retzius (CR) cells whose main role is attracting migrating neurons to form cortical layers, and of cell processes consisting of axons and dendrites, in particular coming from the peripheral pathways through the reticular ascendant system (RAS). Brainstem with its peripheral afferents and the marginal layer are thus the anatomical substrates for the discrimination processing in this first period of life. The second stage of auditory function starts at the beginning of the second semester of life and consists of the anatomical maturation of the cortex and its connections. Axonal neuro-filaments and myelination progressively involve auditory radiation, while cortex lamination is achieved. At this stage, the role of marginal layer is changing, going through the apoptosis of CR cells and the development of new transcortical connections. New connections with medial geniculate body will eventually substitute RAS. Maturing cortex thus becomes the substrate of perception. Cortical maturation is obviously dependent on sensory inputs as demonstrated by the negative effects of hearing loss and conversely by the positive consequences of deprivation correction by early cochlear implants. Pre-cognitive abilities In the very first months of life the reception of the auditory stimulus is mediated by several abilities usually considered as pre-cognitive because of the absence of an operational awareness. Information processing model gives an useful frame to explain the first steps of development through the individuation of individual basal abilities including auditory function [10]. There are several tools based on the information processing model to asses cognitive competence of young infants [11]. Similarly to MMN, they generally assess the ability to discriminate a novel stimulus from an old one that has left a memory trace. Among these tests, the Fagan test of infant intelligence (FTII) [12] has shown its good predictive ability as to subsequent cognitive development [13], definitely higher than that of traditional developmental scales [14]. There is an increasing body of literature investigating the role of pre-cognitive abilities on language development [15-19]. Some basic functions were particularly studied to predict later capacity of language development: visual recognition memory, speed of information processing, attention, and representation ability. Visual recognition memory is based on the child's preference for novel stimuli using the paradigm of comparison between two paired stimuli [20], and is expressed by a score of novelty given by the percentage of time spent by infants in looking at the novel stimulus in relation to the total time spent in looking at both stimuli (familiar and new). Stimulus familiarity has foundation so in the phenomenon of habituation, expressing the progressive loss of interest for repeated stimuli which leave a memory trace. As a result, the new interest of the infant observed when the stimulus changes (dishabituation), can be seen as a measure of discrimination ability. A better visual recognition memory in the first months of life correlates with better understanding of language in the following months, [21] and better ability of expression (lexicon and morpho-syntactic rules) in the following years [19, 22]. The speed of information processing in infants is tested as a measure of response time in a paradigm of "violation of expectation" (orientation towards foreseeable or unforeseeable events) [23] or as a measure of the time to encode information using familiarization (familiarization time) [24]. Although this approach showed some predictive value for later cognitive development [25], little is known on its predictive
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value for language development [26]. However, it appears convincing that the processing speed can influence positively the development of language, as shown by tests for RAP (rapid auditory processing) performed in early ages. They demonstrate how language development is based on the ability to process efficiently and accurately short auditory stimuli presented in rapid sequences [27] (see below). Measuring the evolution of visual attention in the first few months of life can provide some useful information about the maturation of the attentive function, from the subcortical visual skills up to selective attention [28]. Looking at times and rate of displacement (shift) of gaze, as visual indicators of ability to direct the gaze towards objects of interest, was useful in predicting cognitive development [29, 30]. Shared attention and eye contact are certainly at the basis of language, although specific contributions about the influence of attention on language development are scarce and contradictory [31, 32]. Representation competence is defined as "the ability to extract common points from the experiences and to draw an abstract or symbolic representation " [19], all skills necessary to the development of language. To detect such skills in infants, a number of assessment techniques were proposed with various targets: tactual-visual cross-modal transfer, where information about shape is extracted from one modality and applied to another [33], anticipation of events that requires rule abstraction in placement of details in a series of images [34], object permanence which concerns the ability of keeping in mind a hidden object [35] and symbolic game which consists of using one object to represent another one [36]. All these tests, particularly the last two, gave results useful to predict language development [37, 38]. The examinations of the so-called pre-cognitive functions, detected by techniques inspired by the model of information processing provides therefore reliable information about the development of language. The phase of discrimination Auditory discriminative abilities are acquired in the first phase of development, from 28 weeks of gestational age to six months of life. Such kind of discrimination between two sounds belonging to speech or not (universal discrimination) does not need attention, at least conscious attention; it belongs to the pre-attentive stage of auditory processing, consistent with age-specific anatomical-physiological features (see above), auditory inputs coming from the bottom (sensory peripheral structures) without a higher control [39]. The way to investigate discrimination abilities when motility is not yet intentional (pre-praxic stage) consists of examining rudimentary motor responses, non nutritive sucking, orienting reflex, or neurovegetative behaviours (e.g., heart rate changes). Also visual fixation times, when visual targets are associated with speech stimuli may express discrimination abilities and looking time may show the preference towards a kind of linguistic or non-linguistic sounds [40]. Similarly, habituation with specific audio-visual targets allows to check discrimination in infants that prefer new stimuli instead of habituated standard stimuli [41]. At this stage, especially in the first weeks factors more linked to “musical” features of speech (rhythm, prosody) than to phonetic components are predominant, as shown by adaptive changes of the mother speech in order to favor the baby comprehension: high tone exaggeration, slowing of verbal flux, inserting long pauses and stressing the rhythm (motherese is the name to indicate this kind of speech). This particular speech is clearly preferred by infants [40], which in a first stage prefer the maternal source of speech compared to the style of elocution. The attraction towards motherese however ,decreases with time [42], paralleling the progressive loss of ability to discriminate contrasts of non-native language. The relevance of the relational dimension at this early stage of language
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development has led to stress its emotional aspect (vocal emotion) [43]. The preference for the exaggerated characteristics of motherese could come from sensitivity to its emotional value more than to its intrinsic characteristics [44]. But, even more, the maturation of first language appears to depend on a dynamic and mutual relationship between the child and the mother [45]. The reduction of abilities to discriminate between hundreds of possibilities to a few tens of phonetic sounds belonging to native language is particularly characteristic of the last part of this stage. The gradual approach to a selection of only the speech contrasts of the native language is mainly the result of a learning activity relating to phonetic contrasts, to which the child is usually exposed (statistical learning of distributional frequency). Assessment techniques in the discrimination phase. Most assessment techniques in the discrimination phase are experimental and have had a fundamental value in the advancement of knowledge on the processing of auditory stimuli in this stage of development. Early assessment studies inclusive of a more or less prolonged follow up to highlight any predictive capability in language development or, more generally in cognitive development, although not yet commonly used in clinical practice, have a true clinical significance. This type of study, which provides tools for early treatment and prevention of language developmental disorders may give useful information for understanding some mechanisms of speech development [46]. Although there are controversial data on the role of the auditory processing of acoustic non-linguistic stimuli in respect to the phonological structure of speech [47], observer-based methods during the discriminative stage are generally used to measure the ability to respond to novel acoustic stimuli (linguistic or not). Babies on the caregiver’s lap inside a soundproof booth undergo repeated acoustic stimulations alternating with a novel one. An observer outside the booth starts stimulation trials blindly and checks psychophysic behavioural response (see above) to stimulus change. An experimenter inside the booth helps the observer to keep baby’s attention alert [48]. Another protocol to measure the auditory processing abilities in this period takes advantage of visual fixation during acoustic stimulation. The comparison between looking times after presentation of repeated visual target generating two kinds of acoustic stimuli allows the evaluation of stimulus preference. The preference may be also assessed after the habituation to a standard stimulus to test the discrimination with a novel stimulus [49]. This preferential looking intermodal paradigm is widely used in research and now extended to the clinical-diagnostic use [50]. A different kind of evaluation in these first months of life, based always on habituation and recognition memory, may concern suprasegmental (not referring to phonetic features) parameters, e.g. to measure a skill to accurately process repetitive, short and rapid (RAP, rapid auditory processing) auditory stimuli, linguistic or not [51]. The ability to perform the analysis of stimuli sequences (in the range of tens of milliseconds) will allow the construction of maps of phonetic language [52], and its difficulty can predict a disorder of language development [53] Transition from discrimination to perception Around the sixth month, discrimination stage based on sub-cortical mechanisms ends and perception induced by the experience of native phonetic contrasts becomes operational, with always higher involvement of cortical activity. Indeed, transition in auditory processing is progressive, grossly around between 4th and 6th month; however, what is the direction of the maturation process in the other various developmental parameters?
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If another relevant sensory processing, the visual one is considered, at about the 4th month specific tests such as fixation shift under competition shows the achievement of cortical involvement in visual function [28]. In the same way the transition from the pre-praxic stage to that of intentional motility occurs around the 4th .month. The acquisition of the first praxia is the gateway into the world of cognition [54]. Intentional movements may evidently represent cortical involvement in conscious responses to sensory stimulation. During the same period attention matures from the pre-attentive stage to selective attention, moving from a bottom-up way through the reticular ascendant system (attention is driven by stimulus salience) to a cortical modulation in selecting the target. Hence, exactly at the age of 3-4 months there is a definite anatomical-functional turn that underlies the transition from subcortically to cortically dependent functions, namely as to auditory processing from discrimination to perception. The phase of perception (second semester) The beginning of this period corresponds to the achievement of phonemic categorization, i.e. acquisition of sensitivity to the phonetic categories of the native language, with loss of sensitivity towards intermediate phonetic units: e.g., Japanese babies will not be able anymore to discriminate between l and r, belonging to the same category in their language. Such ability to perceive phonetic categories is achieved at the age of six months when native language has been fully acquired with an almost “magnetic” mechanism (native phonemes operate like a magnet in selecting phonetic contrasts infants can process) [52, 55]. Going into the perceptive stage with all described architectural changes of cognition (cortical processing of auditory stimuli), aims of infants during the second semester of life will concern the identification of word forms through the segmentation of the continuous speech flux. Such segmentation, initially regarding phonological features would occur through another statistical mechanism. Mainly, it refers to the higher frequency with which infants meet adjacent syllables belonging to the structure of the same word in comparison to the less usual adjacent syllables belonging to distinct words. This kind of statistical selection is named the method of “adjacent transitional probabilities”. Further speech cues help word identification such as prosody and other emotional relational factors [56], but also cues highly dependent on cognition (stress pattern, phonotactic rules). Particular relevance has been given to the effects of relational factors on perceptive abilities of the infant in language learning (social gating theory) [57]. That is supported by mirror neurons theory [58]. This particular neuronal component involving at the same time perception and action appears especially engaged in language learning [59]. Around the end of the semester, the infant acquires the symbolic function associating the word form to its meaning (age of the first lemma production); in the following years grammatical and syntactic function will develop. The semantic component will be another strong cue for segmentation. Behavioral assessments in the perception phase Behavioral assessments concerning the progressive acquisition of perceptual abilities in the second semester of life are essentially based on the paradigm of head turning (HT) with bimodal stimuli (visual-acoustic), usually reinforced by operant conditioning (visually reinforced conditioned head-turn paradigms). Babies on the lap of their mothers, inside a soundproof booth, are first trained to associate the target sound with a visually interesting scene and then tested measuring the correct orientation of HT towards desired visuo-auditory stimuli [60].
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Cognitive abilities (sustained attention, speed of encoding, ability to consolidate information into memory, selective orienting, learning) are in this case evidently involved So, it is important to keep attention alert during the assessment. The same technique has been used to assess the ability to perceive RAPs when cognitive competence (intentional motility) fully allows HT behavior [52, 60]. Predictive abilities of these assessments [61] are now considered in the context of a speech development supported by the bootstrapping model (metaphor of the small rings to strap boots). Phonetic perception would stimulate segmentation that further produces semantic association (word form meaning). Then, there will be a cascade up to build morpho-syntactic features. Limits of behavioural techniques Methodology performed to check the first acquisitions of language during the first year of life has been generally experimental and has been seldom used in clinical practice because of several technical limits . First of all results of these assessments are generally at a group level and do not account for individual performances. Groups more frequently considered are preterm newborns vs term born or belonging to families at risk of presenting language developmental disorders. The lack of individual results prevents their full clinical use for prediction and early treatment of eventual disorder. Panneton & Newman [49] underline the relevance of the variability of responses inside the same group; some infants seem to prefer novel stimuli while others are more sensitive towards familiar ones, so significantly contaminating results of studies [62]. Furthermore, the complexity of assessments makes difficult their application. In particular, the strong dependence of the success in the test by the attentive ability makes flimsy the judgment on the results. Last but not least, it is not always easy to bring the child's behavior in the setting of the examination to the usual condition of multiple environmental stimulation. Integrative assessment techniques: neurophysiology and neuroimaging Neurophysiology Evoked potentials are especially useful, because they allow to follow the path of sensory inputs with a reliable correspondence with the recording time even though change generators of potential remain approximate. Auditory evoked event-related potentials (AERP) are widely used to assess the auditory brain function or its disorders, both in its exogenous component (simple response to acoustic stimulation) and endogenous (such is the case with the MMN). Regarding the latter, it is a derived value, resulting from a subtraction of the potential obtained from standard stimulus from that produced by a new stimulus (it is the mode of the oddball paradigm, comparable to what occurs in behavioral techniques of discrimination).. As already mentioned in the introduction, the mismatch negativity, detectable as early as in newborns without their attention participation, testifies to the first expression of "knowledge" in the infant. The peculiarity at this age is that the generators of the AERP, in a period of life so full of structural changes as in the first year of life, determine potential wave forms dynamically different over time, suggesting to call MMN in this phase the mismatch response (MMR) [9]. Indeed, AERPs show a a fronto-central positive response in newborns that progressively decline during the first year of life. So, MMR at birth will be moderately positive to become after some months definitely negative as in adults (MMN). There are several studies using evoked potentials to assess discrimination and perception abilities in the infant [51, 63]. Evoked potentials have been performed, for example, to assess discrimination between native and non native speech in term
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newborns vs preterms at nine months of the gestational age : no difference was found between the two groups showing that maturation predominates on exercise that preterm infants undergo [64]. Such techniques were performed also to draw information predictive of language specific disorders (LSD) [65-68] or generally of cognitive development [69], in order to start a specific early habilitation. Often, studies concern preterm newborns [70, 71]. Another neurophysiological technique, gamma power (gamma oscillations of EEG activity) has been used to early assess language in the context of the cognitive competence [72]. Neuroimaging All the various neuroimaging techniques (structural MRI, functional MRI, near infrared spectroscopy, etc.) are extraordinarily useful for the identification of the brain regions where auditory stimulus is processed. Functional techniques in particular are based on regional increase of blood oxygenation (BOLD, blood oxygen level dependent) in functional MRI, or hemoglobin/oxyhemoglobin ratio in near infrared spettroscopy (NIRS). The interest of neuroimaging studies is relevant, particularly at the beginning of the development. It was surprising to find the result of a structural MRI on infants of 1-4 months which revealed a higher growth of the frontal infero-lateral region (Broca's area), compared to the superior temporal sulcus, testifying an earlier cortical maturation of the auditory dorsal pathway; it is not apparently consistent with the later emergence of speech production [73]. These findings are however compatible with the results of other studies using functional MRI by the same research group that show an early activation of the auditory dorsal pathway [5, 74]. In particular, this research has confirmed the existence of a physiological imbalance of the superior temporal sulcus predominant in the right hemisphere (competent in music processing), consistently with the quoted higher “musical” sensitivity in infants’ speech preference during the first months of life. Neuroimaging studies open new horizons in research related to early speech processing, although there are several difficulties in the interpretation of signals. For example, the cortical activation signal is certainly ambiguous, being able to present as positive (increase the oxygenation of the blood) or vice versa as the negative sign in younger subjects; in the latter case, the reduced vascular capacity to meet the demands of oxygen by the active cortex would produce a decrease in the ratio of oxyhemoglobin to deoxyhemoglobin [9]. Concluding notes The progress made in recent years by studies of auditory and language processing in early ages of life gives us the certainty of being on the brink of a "revolutionary" extension of the clinical use of behavioral assessments, in particular, in the context of diagnostic tools useful for the follow-up of newborns/young infants at risk. The availability of reliable behavioral examination methods to investigate the early auditory and speech development will allow to explore beside motor and visual competences a field whose relevance is outstanding for language and higher cognitive ability development. Hence. new progress in strategies of early specific habilitation will be implemented [75]. References 1) Nazzi T, Bertoncini J, Mehler J. Language discrimination by newborns: toward an understanding of the role of rhythm. J Exp Psychol: Hum Percept Perform. 1998; 24: 756–766. 2) Ramus F, Nespor M, Mehler J. Correlates of linguistic rhythm in the speech signal.
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ACCEPTED MANUSCRIPT An update on the early development of language is reported Different kinds of behavioral assessment during the first year of life are described Indications and limitations of early language behavioral assessments are illustrated
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The diagnostic and prognostic utility of early language assessment is underlined