Kerstin Bucher

Emerging Neurophysiological Specialization for Letter Strings

In adult readers, printed words and other letter strings activate specialized visual functions within 200 msec, as evident from neurophysiological recordings of brain activity. These fast, specialized responses to letter strings are thought to develop through plastic changes in the visual system. However, it is unknown whether this specialization emerges only with the onset of word reading, or represents a precursor of literacy. We compared 6-year-old kindergarten children who could not yet read words to adult readers. Both age groups detected immediate repetitions of visually presented words, pseudo-words, symbol strings, and pictures during event-related potential (ERP) mapping. Maps from seven corresponding ERP segments in children and adults were analyzed regarding fast (<250 msec) and slow (>300 msec) specialization for letter strings. Adults reliably differentiated words through increased fast (<150 msec) occipito-temporal N1 activity from symbols. Children showed a later, more mid-occipital N1 with marginal word-symbol differences, which were absent in those children with low letter knowledge. Children with high letter knowledge showed some fast sensitivity to letter strings, which was confined to right occipito-temporal sites, unlike the stronger adult N1 specialization. This suggests that a critical degree of early literacy induces some immature, but fast, specialization for letter strings before word reading becomes possible. Children also differentiated words from symbols in later segments through increased right occipito-temporal negativity for words. This slow specialization for letter strings was not modulated by letter knowledge and was absent in adults, possibly reflecting a visual precursor of literacy due to visual familiarity with letter strings.

Coarse neural tuning for print peaks when children learn to read

Adult readers exhibit increased fast N1 activity to wordlike strings in their event-related brain potential. This increase has been linked to visual expertise for print, implying a protracted monotonic development. We investigated the development of coarse neural tuning for print by studying children longitudinally before and after learning to read, and comparing them to skilled adults. The coarse N1 tuning, which had been absent in nonreading kindergarten children, emerged in less than 2 years after the same children had mastered basic reading skills in 2nd grade. The N1 became larger for words than symbol strings in every child, and this coarse tuning was stronger for faster readers. Fast brain processes thus specialize rapidly for print when children learn to read, and play an important functional role in the fluency of early reading. Comparing 2nd graders with adults revealed a further decrease of the coarse N1 tuning in adults, presumably reflecting further reading practice. This constitutes a prominent nonlinear development of coarse neurophysiological specialization for print. The maximum tuning in novice readers possibly reflects the high sensitivity of their neural network for visual aspects of print, and a more selective tuning in expert adult readers.

Evidence for developmental changes in the visual word processing network beyond adolescence

Late development of specialization in the visual word processing system was examined using event-related potentials (ERP) and functional magnetic resonance imaging (fMRI) of word and symbol string processing in groups of adolescents (15.2-17.3 years) and adults (19.8-30.8 years). We focused our ERP analyses on fast visual activity: the occipital P1 (82-131 ms) modulated by physical stimulus characteristics and the occipito-temporal N1 (132-256 ms) reflecting visual tuning for print. Our fMRI analyses concentrated on basal occipito-temporal activations in the visual word form area VWFA. For words, the correlation of fMRI activation in the VWFA and N1 amplitude confirmed the close relationship of the electrophysiological N1 with metabolic activity in the VWFA. Further support for this relationship came from low resolution electromagnetic tomography localizing the word-specific N1 near the VWFA. Both imaging techniques revealed age-independent differences between words and symbol strings. Late development, however, was preferentially detected with ERPs. Decreases of P1 and N1 amplitudes with age were not limited to words and suggested further maturation of the underlying brain microstructure and function. Following adolescence, decreasing N1 latencies specific to words point to continued specialization of the visual word processing system. Both N1 and fMRI measures correlated with reading performance. In summary, the similarity of global fMRI activation patterns between groups suggests a fully established distribution of the reading network in adolescence, while the decreasing N1 latencies for words indicate protracted fine tuning after adolescence.

Simultaneous EEG-fMRI during a Working Memory Task: Modulations in Low and High Frequency Bands

Background EEG studies of working memory (WM) have demonstrated load dependent frequency band modulations. FMRI studies have localized load modulated activity to the dorsolateral prefrontal cortex (DLPFC), medial prefrontal cortex (MPFC), and posterior parietal cortex (PPC). Recently, an EEG-fMRI study found that low frequency band (theta and alpha) activity negatively correlated with the BOLD signal during the retention phase of a WM task. However, the coupling of higher (beta and gamma) frequencies with the BOLD signal during WM is unknown. Methodology In 16 healthy adult subjects, we first investigated EEG-BOLD signal correlations for theta (5–7 Hz), alpha1 (8–10), alpha2 (10–12 Hz), beta1 (13–20), beta2 (20–30 Hz), and gamma (30–40 Hz) during the retention period of a WM task with set size 2 and 5. Secondly, we investigated whether load sensitive brain regions are characterised by effects that relate frequency bands to BOLD signals effects. Principal Findings We found negative theta-BOLD signal correlations in the MPFC, PPC, and cingulate cortex (ACC and PCC). For alpha1 positive correlations with the BOLD signal were found in ACC, MPFC, and PCC; negative correlations were observed in DLPFC, PPC, and inferior frontal gyrus (IFG). Negative alpha2-BOLD signal correlations were observed in parieto-occipital regions. Beta1-BOLD signal correlations were positive in ACC and negative in precentral and superior temporal gyrus. Beta2 and gamma showed only positive correlations with BOLD, e.g., in DLPFC, MPFC (gamma) and IFG (beta2/gamma). The load analysis revealed that theta and—with one exception—beta and gamma demonstrated exclusively positive load effects, while alpha1 showed only negative effects. Conclusions We conclude that the directions of EEG-BOLD signal correlations vary across brain regions and EEG frequency bands. In addition, some brain regions show both load sensitive BOLD and frequency band effects. Our data indicate that lower as well as higher frequency brain oscillations are linked to neurovascular processes during WM.

Tuning of the visual word processing system: distinct developmental ERP and fMRI effects.

Visual tuning for words vs. symbol strings yields complementary increases of fast occipito‐temporal activity (N1 or N170) in the event‐related potential (ERP), and posterior–anterior gradients of increasing word‐specific activity with functional magnetic resonance imaging (fMRI) in the visual word form system (VWFS). However, correlation of these coarse ERP and fMRI tuning responses seems limited to the most anterior part of the VWFS in adult and adolescent readers (Brem et al. [ 2006 ]: Neuroimage 29:822–837). We thus focused on fMRI tuning gradients of young readers with their more pronounced ERP print tuning, and compared developmental aspects of ERP and fMRI response tuning in the VWFS. Children (10.3 y, n = 19), adolescents (16.2 y, n = 13) and adults (25.2 y, n = 18) were tested with the same implicit reading paradigm using counterbalanced ERP and fMRI imaging. The word‐specific occipito‐temporal N1 specialization, its corresponding source activity, as well as the integrated source activity (0–700 ms) were most prominent in children and showed a marked decrease with age. The posterior–anterior fMRI gradient of word‐specific activity instead which was fully established in children did not develop further, but exhibited a dependence on reading skills independent of age. To conclude, prominent developmental dissociation of the ERP and fMRI tuning patterns emerged despite convergent VWFS localization. The ERP response may selectively reflect fast visual aspects of print specialization, which become less important with age, while the fMRI response seems dominated by integrated task‐ and reading‐related activations in the same regions. Hum Brain Mapp, 2009.

Neurophysiology in Preschool Improves Behavioral Prediction of Reading Ability Throughout Primary School

BACKGROUND More struggling readers could profit from additional help at the beginning of reading acquisition if dyslexia prediction were more successful. Currently, prediction is based only on behavioral assessment of early phonological processing deficits associated with dyslexia, but it might be improved by adding brain-based measures. METHODS In a 5-year longitudinal study of children with (n = 21) and without (n = 23) familial risk for dyslexia, we tested whether neurophysiological measures of automatic phoneme and tone deviance processing obtained in kindergarten would improve prediction of reading over behavioral measures alone. RESULTS Together, neurophysiological and behavioral measures obtained in kindergarten significantly predicted reading in school. Particularly the late mismatch negativity measure that indicated hemispheric lateralization of automatic phoneme processing improved prediction of reading ability over behavioral measures. It was also the only significant predictor for long-term reading success in fifth grade. Importantly, this result also held for the subgroup of children at familial risk. CONCLUSIONS The results demonstrate that brain-based measures of processing deficits associated with dyslexia improve prediction of reading and thus may be further evaluated to complement clinical practice of dyslexia prediction, especially in targeted populations, such as children with a familial risk.

Impaired semantic processing during sentence reading in children with dyslexia: Combined fMRI and ERP evidence

Developmental dyslexia is a specific disorder of reading acquisition characterized by a phonological core deficit. Sentence reading is also impaired in dyslexic readers, but whether semantic processing deficits contribute is unclear. Combining spatially and temporally sensitive neuroimaging techniques to focus on semantic processing can provide a more comprehensive characterization of sentence reading in dyslexia. We recorded brain activity from 52 children (16 with dyslexia, 31 controls) with functional magnetic resonance imaging (fMRI) and event-related potentials (ERP) in two separate counterbalanced sessions. The children silently read and occasionally judged simple sentences with semantically congruous or incongruous endings. fMRI and ERP activation during sentence reading and semantic processing was analyzed across all children and also by comparing children with dyslexia to controls. For sentence reading, we analyzed the response to all words in a sentence; for semantic processing, we contrasted responses to incongruous and congruous endings. Sentence reading was characterized by activation in a left-lateralized language network. Semantic processing was characterized by activation in left-hemispheric regions of the inferior frontal and superior temporal cortex and by an electrophysiological N400 effect after 240 ms with consistent left anterior source localization. Children with dyslexia showed decreased activation for sentence reading in inferior parietal and frontal regions, and for semantic processing in inferior parietal regions, and during the N400 effect. Together, this suggests that semantic impairment during sentence reading reduces dyslexic childrens response in left anterior brain regions underlying the more phasic N400 effect and subsequently modulates the more sustained BOLD response in left inferior parietal regions.

Neurophysiological signs of rapidly emerging visual expertise for symbol strings

The current study examined whether the repeated visual presentation of novel, meaningless symbol strings triggers rapid changes in event related potentials (ERP). Adult participants performed three versions of a word and symbol string repetition detection task in the same experimental session. Analyses focussed on the occipito-temporal N1 (∼150 ms) known to reflect early word-specific processing and stimulus categorisation. While the N1 to words did not change, the occipito-temporal negativity to symbol strings increased over runs and converged with the word N1. Later (∼220 ms) more positive occipito-temporal amplitudes to repeated words in the third compared to the first run implied a repetition priming effect. This suggests that symbol string processing changed over time due to visual learning and increased perceptual expertise.

The development of print tuning in children with dyslexia: Evidence from longitudinal ERP data supported by fMRI

A consistent finding in functional brain imaging studies of reading with dyslexia is reduced inferior occipito-temporal activation linked to deviant processing of visual word forms. Time-sensitive event-related potentials (ERP) further revealed reduced inferior occipito-temporal N1 tuning for print in dyslexic 2nd graders suggesting the reduction affects fast processing and the initial development of dyslexia. Here, we followed up the same groups with ERP recordings and investigated how fast print tuning deficits in dyslexia develop from 2nd to 5th grade. Using functional magnetic resonance imaging (fMRI), we further characterized spatial aspects of print tuning in the 5th grade. The robust N1 tuning deficit for print in the dyslexic 2nd graders had largely disappeared by grade 5 consistent with a developmental delay. Reduced word-specific activation in dyslexic 5th graders fMRI data occurred bilaterally in middle temporal regions and in the left posterior superior sulcus. Although no group differences in inferior occipito-temporal regions appeared in the whole brain analysis, a region of interest analysis of the Visual Word Form Area revealed that control children showed a more lateralized word-specific activation pattern than the children with dyslexia. The results suggest that while impaired N1 tuning for print plays a major role for dyslexia at the beginning of learning to read, other aspects of visual word form processing in the same region remain impaired in dyslexic children after several years of reading practice. Overall, neural deficits associated with dyslexia appear to be plastic and to change throughout development and reading acquisition.

Dorsal stream development in motion and structure-from-motion perception.

Little is known about the neural development underlying high order visual perception. For example, in detection of structures by coherently moving dots, motion information must interact with shape-based information to enable object recognition. Tasks involving these different motion-based discriminations are known to activate distinct specialized brain areas in adults. Here, we investigate neural development of normally developing children using functional magnetic resonance imaging (fMRI) during perception of randomly moving point-light dots (RM), coherently moving dots that formed a 3D rotating object (SFM) and static dots. Perception of RM enhanced neural activity as compared with static dots in motion processing-related visual areas, including visual area 3a (V3a), and middle temporal area (hMT+) in 10 adults (age 20-30 years). Children (age 5-6 years) showed less pronounced activity in area V3a than adults. Perception of SFM induced enhanced neural activity as compared to RM in adults in the left parietal shape area (PSA), whereas children increased neural activity within dorsal (V3a) and ventral brain areas (lingual gyrus) of the occipital cortex. These findings provide evidence of neural development within the dorsal pathway. First, maturation was associated with enhanced activity in specialized areas within the dorsal pathway during RM perception (V3a) and SFM perception (PSA). Secondly, high order visual perception-related neural development was associated with a shift in neural activity from low level shape and motion specialized areas in children, including partially immature area V3a, to high order areas in the parietal lobule (PSA) in adults.