Stronger neural response to canonical finger-number configurations in deaf compared to hearing adults revealed by FPVS-EEG.

The linguistic counting system of deaf signers consists of a manual counting format that uses specific structures for number words. Interestingly, the number signs from 1 to 4 in the Belgian sign languages correspond to the finger-montring habits of hearing individuals. These hand configurations could therefore be considered as signs (i.e., part of a language system) for deaf, while they would simply be number gestures (not linguistic) for hearing controls. A Fast Periodic Visual Stimulation design was used with electroencephalography recordings to examine whether these finger-number configurations are differently processed by the brain when they are signs (in deaf signers) as compared to when they are gestures (in hearing controls). Results showed that deaf signers show stronger discrimination responses to canonical finger-montring configurations compared to hearing controls. A second control experiment furthermore demonstrated that this finding was not merely due to the experience deaf signers have with the processing of hand configurations, as brain responses did not differ between groups for finger-counting configurations. Number configurations are therefore processed differently by deaf signers, but only when these configurations are part of their language system.

Developmental changes in neural letter-selectivity: A 1-year follow-up of beginning readers.

The developmental course of neural tuning to visual letter strings is unclear. Here we tested 39 children longitudinally, at the beginning of grade 1 (6.45 ± 0.33 years old) and 1 year after, with fast periodic visual stimulation in electroencephalography to assess the evolution of selective neural responses to letter strings and their relationship with emerging reading abilities. At both grades, frequency-tagged letter strings were discriminated from pseudofont strings (i.e. letter-selectivity) over the left occipito-temporal cortex, with effects observed at the individual level in 62% of children. However, visual words were not discriminated from pseudowords (lexical access) at either grade. Following 1 year of schooling, letter-selective responses showed a specific increase in amplitude, a more complex pattern of harmonics, and were located more anteriorly over the left occipito-temporal cortex. Remarkably, at both grades, neural responses were highly significant at the individual level and correlated with individual reading scores. The amplitude increase in letter-selective responses between grades was not found for discrimination responses of familiar keyboard symbols from pseudosymbols, and was not related to a general increase in visual stimulation responses. These findings demonstrate a rapid onset of left hemispheric letter selectivity, with 1 year of reading instruction resulting in increased emerging reading abilities and a clear quantitative and qualitative evolution within left hemispheric neural circuits for reading.

Selective visual representation of letters and words in the left ventral occipito-temporal cortex with intracerebral recordings.

We report a comprehensive cartography of selective responses to visual letters and words in the human ventral occipito-temporal cortex (VOTC) with direct neural recordings, clarifying key aspects of the neural basis of reading. Intracerebral recordings were performed in a large group of patients (n = 37) presented with visual words inserted periodically in rapid sequences of pseudofonts, nonwords, or pseudowords, enabling classification of responses at three levels of word processing: letter, prelexical, and lexical. While letter-selective responses are found in much of the VOTC, with a higher proportion in left posterior regions, prelexical/lexical responses are confined to the middle and anterior sections of the left fusiform gyrus. This region overlaps with and extends more anteriorly than the visual word form area typically identified with functional magnetic resonance imaging. In this region, prelexical responses provide evidence for populations of neurons sensitive to the statistical regularity of letter combinations independently of lexical responses to familiar words. Despite extensive sampling in anterior ventral temporal regions, there is no hierarchical organization between prelexical and lexical responses in the left fusiform gyrus. Overall, distinct word processing levels depend on neural populations that are spatially intermingled rather than organized according to a strict postero-anterior hierarchy in the left VOTC.

The right hemispheric dominance for face perception in preschool children depends on the visual discrimination level.

The developmental origin of human adults' right hemispheric dominance in response to face stimuli remains unclear, in particular because young infants' right hemispheric advantage in face-selective response is no longer present in preschool children, before written language acquisition. Here we used fast periodic visual stimulation (FPVS) with scalp electroencephalography (EEG) to test 52 preschool children (5.5 years old) at two different levels of face discrimination: discrimination of faces against objects, measuring face-selectivity, or discrimination between individual faces. While the contrast between faces and nonface objects elicits strictly bilateral occipital responses in children, strengthening previous observations, discrimination of individual faces in the same children reveals a strong right hemispheric lateralization over the occipitotemporal cortex. Picture-plane inversion of the face stimuli significantly decreases the individual discrimination response, although to a much smaller extent than in older children and adults tested with the same paradigm. However, there is only a nonsignificant trend for a decrease in right hemispheric lateralization with inversion. There is no relationship between the right hemispheric lateralization in individual face discrimination and preschool levels of readings abilities. The observed difference in the right hemispheric lateralization obtained in the same population of children with two different paradigms measuring neural responses to faces indicates that the level of visual discrimination is a key factor to consider when making inferences about the development of hemispheric lateralization of face perception in the human brain.

Lateralized Neural Responses to Letters and Digits in First Graders.

The emergence of visual cortex specialization for culturally acquired characters like letters and digits, both arbitrary shapes related to specific cognitive domains, is yet unclear. Here, 20 young children (6.12 years old) were tested with a frequency-tagging paradigm coupled with electroencephalogram recordings to assess discrimination responses of letters from digits and vice-versa. One category of stimuli (e.g., letters) was periodically inserted (1/5) in streams of the other category (e.g., digits) presented at a fast rate (6 Hz). Results show clear right-lateralized discrimination responses at 6 Hz/5 for digits within letters, and a trend for left-lateralization for letters. These results support an early developmental emergence of ventral occipito-temporal cortex specialization for visual recognition of digits and letters, potentially in relation with relevant coactivated brain networks.

Left cortical specialization for visual letter strings predicts rudimentary knowledge of letter-sound association in preschoolers.

Reading, one of the most important cultural inventions of human society, critically depends on posterior brain areas of the left hemisphere in proficient adult readers. In children, this left hemispheric cortical specialization for letter strings is typically detected only after approximately 1 y of formal schooling and reading acquisition. Here, we recorded scalp electrophysiological (EEG) brain responses in 5-y-old (n = 40) prereaders presented with letter strings appearing every five items in rapid streams of pseudofonts (6 items per second). Within 2 min of recording only, letter strings evoked a robust specific response over the left occipito-temporal cortex at the predefined frequency of 1.2 Hz (i.e., 6 Hz/5). Interindividual differences in the amplitude of this electrophysiological response are significantly related to letter knowledge, a preschool predictor of later reading ability. These results point to the high potential of this rapidly collected behavior-free measure to assess reading ability in developmental populations. These findings were replicated in a second experiment (n = 26 preschool children), where familiar symbols and line drawings of objects evoked right-lateralized and bilaterally specific responses, respectively, showing the specificity of the early left hemispheric dominance for letter strings. Collectively, these findings indicate that limited knowledge of print in young children, before formal education, is sufficient to develop specialized left lateralized neuronal circuits, thereby pointing to an early onset and rapid impact of left hemispheric reentrant sound mapping on posterior cortical development.

Does Extensive Training at Individuating Novel Objects in Adulthood Lead to Visual Expertise? The Role of Facelikeness.

Human adults have a rich visual experience thanks to seeing human faces since birth, which may contribute to the acquisition of perceptual processes that rapidly and automatically individuate faces. According to a generic visual expertise hypothesis, extensive experience with nonface objects may similarly lead to efficient processing of objects at the individual level. However, whether extensive training in adulthood leads to visual expertise remains debated. One key issue is the extent to which the acquisition of visual expertise depends on the resemblance of objects to faces in terms of the spatial configuration of parts. We therefore trained naive human adults to individuate a large set of novel parametric multipart objects. Critically, one group of participants trained with the objects in a "facelike" stimulus orientation, whereas a second group trained with the same objects but with the objects rotated 180° in the picture plane into a "nonfacelike" orientation. We used a fast periodic visual stimulation EEG protocol to objectively quantify participants' ability to discriminate untrained exemplars before and after training. EEG responses associated with the frequency of identity change in a fast stimulation sequence, which reflects rapid and automatic perceptual processes, were observed over lateral occipital sites for both groups before training. There was a significant, albeit small, increase in these responses after training but only for the facelike group and only to facelike stimuli. Our findings indicate that perceived facelikeness plays a role in visual expertise and highlight how the adult perceptual system exploits familiar spatial configurations when learning new object categories.

Frequency-tagging EEG reveals the effect of attentional focus on abstract magnitude processing.

While humans can readily access the common magnitude of various codes such as digits, number words, or dot sets, it remains unclear whether this process occurs automatically, or only when explicitly attending to magnitude information. We addressed this question by examining the neural distance effect, a robust marker of magnitude processing, with a frequency-tagging approach. Electrophysiological responses were recorded while participants viewed rapid sequences of a base numerosity presented at 6 Hz (e.g., "2") in randomly mixed codes: digits, number words, canonical dot, and finger configurations. A deviant numerosity either close (e.g., "3") or distant (e.g., "8") from the base was inserted every five items. Participants were instructed to focus their attention either on the magnitude number feature (from a previous study), the parity number feature, a nonnumerical color feature or no specific feature. In the four attentional conditions, we found clear discrimination responses of the deviant numerosity despite its code variation. Critically, the distance effect (larger responses when base/deviant are distant than close) was present when participants were explicitly attending to magnitude and parity, but it faded with color and simple viewing instructions. Taken together, these results suggest automatic access to an abstract number representation but highlight the role of selective attention in processing the underlying magnitude information. This study therefore provides insights into how attention can modulate the neural activity supporting abstract magnitude processing.

Linguistic and attentional factors - Not statistical regularities - Contribute to word-selective neural responses with FPVS-oddball paradigms.

Studies using frequency-tagging in electroencephalography (EEG) have dramatically increased in the past 10 years, in a variety of domains and populations. Here we used Fast Periodic Visual Stimulation (FPVS) combined with an oddball design to explore visual word recognition. Given the paradigm's high sensitivity, it is crucial for future basic research and clinical application to prove its robustness across variations of designs, stimulus types and tasks. This paradigm uses periodicity of brain responses to measure discrimination between two experimentally defined categories of stimuli presented periodically. EEG was recorded in 22 adults who viewed words inserted every 5 stimuli (at 2 Hz) within base stimuli presented at 10 Hz. Using two discrimination levels (deviant words among nonwords or pseudowords), we assessed the impact of relative frequency of item repetition (set size or item repetition controlled for deviant versus base stimuli), and of the orthogonal task (focused or deployed spatial attention). Word-selective occipito-temporal responses were robust at the individual level (significant in 95% of participants), left-lateralized, larger for the prelexical (nonwords) than lexical (pseudowords) contrast, and stronger with a deployed spatial attention task as compared to the typically used focused task. Importantly, amplitudes were not affected by item repetition. These results help understanding the factors influencing word-selective EEG responses and support the validity of FPVS-EEG oddball paradigms, as they confirm that word-selective responses are linguistic. Second, they show its robustness against design-related factors that could induce statistical (ir)regularities in item rate. They also confirm its high individual sensitivity and demonstrate how it can be optimized, using a deployed rather than focused attention task, to measure implicit word recognition processes in typical and atypical populations.

Spatial Resolution Evaluation Based on Experienced Visual Categories With Sweep Evoked Periodic EEG Activity.

Purpose: Visual function is typically evaluated in clinical settings with visual acuity (VA), a test requiring to behaviorally match or name optotypes such as tumbling E or Snellen letters. The ability to recognize these symbols has little in common with the automatic and rapid visual recognition of socially important stimuli in real life. Here we use sweep visual evoked potentials to assess spatial resolution objectively based on the recognition of human faces and written words. Methods: To this end, we tested unfamiliar face individuation1 and visual word recognition2 in 15 normally sighted adult volunteers with a 68-electrode electroencephalogram system. Results: Unlike previous measures of low-level visual function including VA, the most sensitive electrode was found at an electrode different from Oz in a majority of participants. Thresholds until which faces and words could be recognized were evaluated at the most sensitive electrode defined individually for each participant. Word recognition thresholds corresponded with the VA level expected from normally sighted participants, and even a VA significantly higher than expected from normally sighted individuals for a few participants. Conclusions: Spatial resolution can be evaluated based on high-level stimuli encountered in day-to-day life, such as faces or written words with sweep visual evoked potentials.

Is human face recognition lateralized to the right hemisphere due to neural competition with left-lateralized visual word recognition? A critical review.

The right hemispheric lateralization of face recognition, which is well documented and appears to be specific to the human species, remains a scientific mystery. According to a long-standing view, the evolution of language, which is typically substantiated in the left hemisphere, competes with the cortical space in that hemisphere available for visuospatial processes, including face recognition. Over the last decade, a specific hypothesis derived from this view according to which neural competition in the left ventral occipito-temporal cortex with selective representations of letter strings causes right hemispheric lateralization of face recognition, has generated considerable interest and research in the scientific community. Here, a systematic review of studies performed in various populations (infants, children, literate and illiterate adults, left-handed adults) and methodologies (behavior, lesion studies, (intra)electroencephalography, neuroimaging) offers little if any support for this reading lateralized neural competition hypothesis. Specifically, right-lateralized face-selective neural activity already emerges at a few months of age, well before reading acquisition. Moreover, consistent evidence of face recognition performance and its right hemispheric lateralization being modulated by literacy level during development or at adulthood is lacking. Given the absence of solid alternative hypotheses and the key role of neural competition in the sensory-motor cortices for selectivity of representations, learning, and plasticity, a revised language-related neural competition hypothesis for the right hemispheric lateralization of face recognition should be further explored in future research, albeit with substantial conceptual clarification and advances in methodological rigor.

A shared numerical magnitude representation evidenced by the distance effect in frequency-tagging EEG.

Humans can effortlessly abstract numerical information from various codes and contexts. However, whether the access to the underlying magnitude information relies on common or distinct brain representations remains highly debated. Here, we recorded electrophysiological responses to periodic variation of numerosity (every five items) occurring in rapid streams of numbers presented at 6 Hz in randomly varying codes-Arabic digits, number words, canonical dot patterns and finger configurations. Results demonstrated that numerical information was abstracted and generalized over the different representation codes by revealing clear discrimination responses (at 1.2 Hz) of the deviant numerosity from the base numerosity, recorded over parieto-occipital electrodes. Crucially, and supporting the claim that discrimination responses reflected magnitude processing, the presentation of a deviant numerosity distant from the base (e.g., base "2" and deviant "8") elicited larger right-hemispheric responses than the presentation of a close deviant numerosity (e.g., base "2" and deviant "3"). This finding nicely represents the neural signature of the distance effect, an interpretation further reinforced by the clear correlation with individuals' behavioral performance in an independent numerical comparison task. Our results therefore provide for the first time unambiguously a reliable and specific neural marker of a magnitude representation that is shared among several numerical codes.

Canonical representations of fingers and dots trigger an automatic activation of number semantics: an EEG study on 10-year-old children.

Over the course of development, children must learn to map a non-symbolic representation of magnitude to a more precise symbolic system. There is solid evidence that finger and dot representations can facilitate or even predict the acquisition of this mapping skill. While several behavioral studies demonstrated that canonical representations of fingers and dots automatically activate number semantics, no study so far has investigated their cerebral basis. To examine these questions, 10-year-old children were presented a behavioral naming task and a Fast Periodic Visual Stimulation EEG paradigm. In the behavioral task, children had to name as fast and as accurately as possible the numbers of dots and fingers presented in canonical and non-canonical configurations. In the EEG experiment, one category of stimuli (e.g., canonical representation of fingers or dots) was periodically inserted (1/5) in streams of another category (e.g., non-canonical representation of fingers or dots) presented at a fast rate (4 Hz). Results demonstrated an automatic access to number semantics and bilateral categorical responses at 4 Hz/5 for canonical representations of fingers and dots. Some differences between finger and dot configuration's processing were nevertheless observed and are discussed in light of an effortful-automatic continuum hypothesis.

Dissociated face- and word-selective intracerebral responses in the human ventral occipito-temporal cortex.

The extent to which faces and written words share neural circuitry in the human brain is actively debated. Here, we compare face-selective and word-selective responses in a large group of patients (N = 37) implanted with intracerebral electrodes in the ventral occipito-temporal cortex (VOTC). Both face-selective (i.e., significantly different responses to faces vs. non-face visual objects) and word-selective (i.e., significantly different responses to words vs. pseudofonts) neural activity is isolated with frequency-tagging. Critically, this sensitive approach allows to objectively quantify category-selective neural responses and disentangle them from general visual responses. About 70% of significant electrode contacts show either face-selectivity or word-selectivity only, with the expected right and left hemispheric dominance, respectively. Spatial dissociations are also found within core regions of face and word processing, with a medio-lateral dissociation in the fusiform gyrus (FG) and surrounding sulci, respectively. In the 30% of overlapping face- and word-selective contacts across the VOTC or in the FG and surrounding sulci, between-category-selective amplitudes (faces vs. words) show no-to-weak correlations, despite strong correlations in both the within-category-selective amplitudes (face-face, word-word) and the general visual responses to words and faces. Overall, these observations support the view that category-selective circuitry for faces and written words is largely dissociated in the human adult VOTC.

The non-linear development of the right hemispheric specialization for human face perception.

The developmental origins of human adults' right hemispheric specialization for face perception remain unclear. On the one hand, infant studies have shown a right hemispheric advantage for face perception. On the other hand, it has been proposed that the adult right hemispheric lateralization for face perception slowly emerges during childhood due to reading acquisition, which increases left lateralized posterior responses to competing written material (e.g., visual letters and words). Since methodological approaches used in infant and children typically differ when their face capabilities are explored, resolving this issue has been difficult. Here we tested 5-year-old preschoolers varying in their level of visual letter knowledge with the same fast periodic visual stimulation (FPVS) paradigm leading to strongly right lateralized electrophysiological occipito-temporal face-selective responses in 4- to 6-month-old infants (de Heering and Rossion, 2015). Children's face-selective response was quantitatively larger and differed in scalp topography from infants', but did not differ across hemispheres. There was a small positive correlation between preschoolers' letter knowledge and a non-normalized index of right hemispheric specialization for faces. These observations show that previous discrepant results in the literature reflect a genuine nonlinear development of the neural processes underlying face perception and are not merely due to methodological differences across age groups. We discuss several factors that could contribute to the adult right hemispheric lateralization for faces, such as myelination of the corpus callosum and reading acquisition. Our findings point to the value of FPVS coupled with electroencephalography to assess specialized face perception processes throughout development with the same methodology.

Impact of Learning to Read in a Mixed Approach on Neural Tuning to Words in Beginning Readers.

The impact of learning to read in a mixed approach using both the global and phonics teaching methods on the emergence of left hemisphere neural specialization for word recognition is yet unknown in children. Taking advantage of a natural school context with such a mixed approach, we tested 42 first graders behaviorally and with Fast Periodic Visual Stimulation using electroencephalographic recordings (FPVS-EEG) to measure selective neural responses to letter strings. Letter strings were inserted periodically (1/5) in pseudofonts in 40 s sequences displayed at 6 Hz and were either words globally taught at school, that could therefore be processed by visual whole-word form recognition (global method), or control words/pseudowords eliciting grapheme-phoneme (GP) mappings (phonics method). Results show that selective responses (F/5, 1.2 Hz) were left lateralized for control stimuli that triggered GP mappings but bilateral for globally taught words. It implies that neural mechanisms recruited during visual word processing are influenced by the nature of the mapping between written and spoken word forms. GP mappings induce left hemisphere discrimination responses, and visual recognition of whole-word forms induce bilateral responses, probably because the right hemisphere is relatively more involved in holistic visual object recognition. Splitting the group as a function of the mastery of GP mappings into "good" and "poor" readers strongly suggests that good readers actually processed all stimuli (including global words) predominantly with their left hemisphere, while poor readers showed bilateral responses for global words. These results show that in a mixed approach of teaching to read, global method instruction may induce neural processes that differ from those specialized for reading in the left hemisphere. Furthermore, given their difficulties in automatizing GP mappings, poor readers are especially prone to rely on this alternative visual strategy. A preprint of this paper has been released on Biorxiv (van de Walle de Ghelcke et al., 2018).

Spatial associations for musical stimuli: a piano in the head?

This study was aimed at examining whether pitch height and pitch change are mentally represented along spatial axes. A series of experiments explored, for isolated tones and 2-note intervals, the occurrence of effects analogous to the spatial numerical association of response codes (SNARC) effect. Response device orientation (horizontal vs. vertical), task, and musical expertise of the participants were manipulated. The pitch of isolated tones triggered the automatic activation of a vertical axis independently of musical expertise, but the contour of melodic intervals did not. By contrast, automatic associations with the horizontal axis seemed linked to music training for pitch and, to a lower extent, for intervals. These results, discussed in the light of studies on number representation, provide a new example of the effects of musical expertise on music cognition.

Multiple levels of letter representation in written spelling: evidence from a single case of dysgraphia with multiple deficits.

In this paper, we report a detailed analysis of the impaired performance of a dysgraphic individual, AD, who produced similar rates of letter-level errors in written spelling, oral spelling, and typing. We found that the distribution of various letter error types displayed a distinct pattern in written spelling on the one hand and in oral spelling and typing on the other. In particular, noncontextual letter substitution errors (i.e., errors in which the erroneous letter that replaces the target letter does not occur elsewhere within the word) were virtually absent in oral spelling and typing and mainly found in written spelling. In contrast, letter deletion errors and multiple-letter errors were typically found in oral spelling and very exceptional in written spelling. Only contextual letter substitution errors (i.e., errors in which the erroneous letter that replaces the target letter is identical to a letter occurring earlier or later in the word) were found in similar proportions in the three tasks. We argue that these contrasting patterns of letter error distribution result from damage to two distinct levels of letter representation and processing within the spelling system, namely, the amodal graphemic representation held in the graphemic buffer and the letter form representation computed by subsequent writing-specific processes. Then, we examined the relationship between error and target in the letter substitution errors produced in written and oral spelling and found evidence that distinct types of letter representation are processed at each of the hypothetized levels of damage: symbolic letter representation at the graphemic level and representation of the component graphic strokes at the letter form processing level.

A robust index of lexical representation in the left occipito-temporal cortex as evidenced by EEG responses to fast periodic visual stimulation.

Despite decades of research on reading, including the relatively recent contributions of neuroimaging and electrophysiology, identifying selective representations of whole visual words (in contrast to pseudowords) in the human brain remains challenging, in particular without an explicit linguistic task. Here we measured discrimination responses to written words by means of electroencephalography (EEG) during fast periodic visual stimulation. Sequences of pseudofonts, nonwords, or pseudowords were presented through sinusoidal contrast modulation at a periodic 10 Hz frequency rate (F), in which words were interspersed at regular intervals of every fifth item (i.e., F/5, 2 Hz). Participants monitored a central cross color change and had no linguistic task to perform. Within only 3 min of stimulation, a robust discrimination response for words at 2 Hz (and its harmonics, i.e., 4 and 6 Hz) was observed in all conditions, located predominantly over the left occipito-temporal cortex. The magnitude of the response was largest for words embedded in pseudofonts, and larger in nonwords than in pseudowords, showing that list context effects classically reported in behavioral lexical decision tasks are due to visual discrimination rather than decisional processes. Remarkably, the oddball response was significant even for the critical words/pseudowords discrimination condition in every individual participant. A second experiment replicated this words/pseudowords discrimination, and showed that this effect is not accounted for by a higher bigram frequency of words than pseudowords. Without any explicit task, our results highlight the potential of an EEG fast periodic visual stimulation approach for understanding the representation of written language. Its development in the scientific community might be valuable to rapidly and objectively measure sensitivity to word processing in different human populations, including neuropsychological patients with dyslexia and other reading difficulties.