Origins of the specialization for letters and numbers in ventral occipitotemporal cortex

Hannagan, Thomas; Amedi, Amir; Cohen, Laurent; Dehaene‐Lambertz, Ghislaine; Dehaene, Stanislas

doi:10.1016/j.tics.2015.05.006

Cited by 201 publications

(191 citation statements)

References 102 publications

(132 reference statements)

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“…Our results support the biased connectivity hypothesis in regards to the development of the NFA (8): that the selectivity within the NFA may be driven by its intrinsic connectivity with the aIPS. However, such an interaction between the aIPS and pITG may be direct or indirect, possibly mediated by a third structure such as the thalamus, which plays a role in regulating information flow between cortical areas (75)(76)(77).…”

Section: Task-based and Intrinsic Coupling Of Activity Across Neuronalsupporting

confidence: 84%

“…These findings reveal information about the dynamics of numerical processing in the brain and also provide insight into the fine-grained functional architecture and connectivity within the human brain. A lthough the ability to approximate or compare rough quantities is present even in human infants (1) and in other species such as nonhuman primates (2)(3)(4) and birds (5), the association of exact quantities with symbols (e.g., the numeral "10") or verbal representations (e.g., the word "ten") is unique to humans exposed to such culturally learned entities (6)(7)(8). Moreover, dissociable number-and quantity-related behavioral deficits (i.e., deficits relating to symbolic or verbal numerical representations versus abstract quantity representations) are associated with different lesion locations within the brain (9)(10)(11)(12)(13)(14).…”

mentioning

confidence: 99%

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Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

Daitch

Foster

Schrouff

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Brain areas within the lateral parietal cortex (LPC) and ventral temporal cortex (VTC) have been shown to code for abstract quantity representations and for symbolic numerical representations, respectively. To explore the fast dynamics of activity within each region and the interaction between them, we used electrocorticography recordings from 16 neurosurgical subjects implanted with grids of electrodes over these two regions and tracked the activity within and between the regions as subjects performed three different numerical tasks. Although our results reconfirm the presence of math-selective hubs within the VTC and LPC, we report here a remarkable heterogeneity of neural responses within each region at both millimeter and millisecond scales. Moreover, we show that the heterogeneity of response profiles within each hub mirrors the distinct patterns of functional coupling between them. Our results support the existence of multiple bidirectional functional loops operating between discrete populations of neurons within the VTC and LPC during the visual processing of numerals and the performance of arithmetic functions. These findings reveal information about the dynamics of numerical processing in the brain and also provide insight into the fine-grained functional architecture and connectivity within the human brain.A lthough the ability to approximate or compare rough quantities is present even in human infants (1) and in other species such as nonhuman primates (2-4) and birds (5), the association of exact quantities with symbols (e.g., the numeral "10") or verbal representations (e.g., the word "ten") is unique to humans exposed to such culturally learned entities (6-8). Moreover, dissociable number-and quantity-related behavioral deficits (i.e., deficits relating to symbolic or verbal numerical representations versus abstract quantity representations) are associated with different lesion locations within the brain (9-14). These observations in part motivated the Triple Code model positing that the human brain contains three different numerical representations: symbolic, verbal, and abstract quantity, each coded in a different brain region (15,16). The model also predicts that, depending on task demands (e.g., simple visual recognition of a numeral versus determining the larger of two numerals versus verbal naming of a numeral), all or a subset of these brain regions interact with each other (15, 16).Neuroimaging, electrophysiology, and lesion studies in both humans and nonhuman primates have long implicated the parietal lobe, particularly the anterior segment of the intraparietal sulcus (aIPS), in abstract quantity representations irrespective of the modality of presentation (e.g., "4" vs. "four" vs. "::"), with specific neurons or neuronal populations exhibiting tuning around a preferred numerosity (4, 17-25). Moreover, brain activity within this region and its functional and anatomical connectivity with other brain regions are correlated with mathematical performance in individual subjects (26)(27)(28)(29),...

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Section: Task-based and Intrinsic Coupling Of Activity Across Neuronalsupporting

confidence: 84%

mentioning

confidence: 99%

Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

Daitch

Foster

Schrouff

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Hence, during reading acquisition, mapping between graphemes and phonemes, or orthographic-phonological binding (7), could generate the ipsilateral left hemispheric engagement of posterior brain regions to letter strings. This view is supported by spatial constraints in establishing intrahemispheric vs. interhemispheric connections (8,16) and by privileged and/or preexisting connectivity with language areas as suggested by functional connectivity analyses in fMRI (41) and tractography (37,42).…”

Section: Early Left Lateralization For Print: Stimulus Properties or mentioning

confidence: 98%

“…First, because minimal knowledge of graphemephoneme association is sufficient to induce neural changes, it implies early establishment of functional connections between posterior visual and anterior phonological regions during development, which may be relying on preexisting structural connectivity (41,42). Second, because familiar, but not unfamiliar, symbols trigger a (right-lateralized) discrimination response, it shows that limited knowledge of certain classes of visual stimuli suffice to develop circuits that are specialized for processing these stimuli.…”

Section: Early Left Lateralization For Print: Stimulus Properties or mentioning

confidence: 99%

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

Lochy¹,

Reybroeck²,

Rossion³

2016

Proc. Natl. Acad. Sci. U.S.A.

147

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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.A dult expert reading, a complex yet effortless and fast process (i.e., occurring at an average of 200 ms per word; ref. 1), critically depends on the left ventral occipito-temporal cortex (2). This left hemispheric specialization is thought to arise during children's reading acquisition through reentrant mapping of sound representations in the left temporal and frontal cortices to letter representations in ipsilateral posterior areas (3-5). Even though the exact onset of this leftward specialization is not known, this process appears to take considerable time during formal reading acquisition (6-8).Functional magnetic resonance imaging (fMRI) reveals the typical left lateralized adult-like brain pattern for letter strings only in proficient readers (ref. 9 for a metaanalysis) and in natural settings, significant left lateralization appears only when children have already acquired formal reading ability, approximately at 7 y of age (10). In developmental studies with direct measures of brain activity (electro/magneto-encephalography, EEG/MEG), the typical reading adult occipito-temporal response evoked by letter strings at approximately 200 ms after stimulus onset (i.e., N1 or N170; refs. 11 and 12) is absent in preschool children, even if they can already categorize or name letters. Typically, sensitivity to print has been shown after 1 y (13), or 1.5 y of schooling (14), thus, afte...

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“…Although the stimuli used in our visual search task were letters, the FG area that showed decreased activation after training did not match the visual word form area location, which is lateral to our coordinate (Hannagan et al, 2015;Cohen et al, 2000). However, a very close match was found between our FG activations and the results of a previous perceptual learning fMRI investigation .…”

Section: Training Effects: Changes In Occipital Cortexmentioning

confidence: 75%

Brain bases of the automaticity via visual search task

Bohabonay¹

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AgradecimientosLa presente tesis es el resultado de un trabajo realizado con gran dedicación. Antes de presentar este trabajo, quiero dedicar unas líneas a dar las gracias a todas las personas que me han ayudado durante este tiempo.Quiero dar las gracias a mis directores de tesis, el Dr. César Ávila y el Dr. Alfonso Barrós. Al Dr. César Ávila por darme la oportunidad de formar parte de su grupo de investigación y, también, por plantearme nuevos retos en cada fase de mis estudios de doctorado, tanto con la elaboración de las tareas experimentales como con el análisis de datos y la interpretación de los resultados. Al Dr. Alfonso Barrós, darle las gracias por ofrecerme diferentes perspectivas para resolver los problemas que surgen al investigar. También por todas las veces que me ha orientado y me ha ayudado a resolver dudas. Ambos me han ayudado a desarrollar un punto de vista crítico en la investigación y ser más independiente.Quiero dar las gracias al Dr. Jorge Sepulcre por darme la oportunidad de realizar una estancia de investigación en su grupo. También por enseñarme una perspectiva de trabajo diferente, crítica, detallada y exigente. Gracias a la Dra. Cristina Forn por ayudarme en todos los aspectos de mi docencia universitaria y por ser mi tutora en el programa de Formación de Profesorado Novel. Gracias a la Dra. Noelia Ventura Campos por enseñarme a analizar los datos de neuroimagen y por contestar todas mis dudas. Gracias a los tres por toda la paciencia y tiempo dedicado.A mis compañeros/as de laboratorio. Gracias por toda la ayuda que me habéis ofrecido durante estos años. Por hacerme formar parte de un grupo excelente, muy trabajador pero a la vez divertido. Gracias a Anna, por las tardes de escáner, por los recados cuando estaba de estancia, por organizar eventos, pero sobre todo, por ser muy positiva. Gracias a Marian, Patri y Paola, porque empezamos juntas, por todo lo compartido y todas nuestras conversaciones. Gracias también a mis otros compañeros/as de laboratorio: Maya, Mireia, Víctor, Jesús, Aina, Juan Carlos, Javi, Javi Panach, Ana Sanjuán y María Jesús.A mis amigos. A mis psicólogos: Ger, Patri, Bego, Marta, Marian y Víctor. Porque empezamos juntos la carrera de Psicología y porque seguimos superando retos juntos. Gracias a Guada por acompañarme desde el principio, por nuestros cafés, pero sobre todo, por ser siempre tan optimista. Gracias a Patri Fortea, por reflejarse tantas veces en mí, porque tu sueño de ser doctora me ha ayudado en mí camino. Gracias Eli, Hande, Laura, Vero y Paula, por apoyarme en diferentes momentos durante el doctorado.A mi familia. Gracias por creer en mí. A mi madre y a mi padre, gracias por enseñarme el valor del trabajo y el esfuerzo, sin ello no hubiera llegado a donde estoy hoy. Muchas gracias por enseñarme a tener paciencia. A mi hermana Noemí y mi hermano Néstor, gracias por ser mi ejemplo a seguir, por vuestra ayuda incondicional, por ser mí guía, mi punto de apoyo, por darme vuestra opinión y vuestros consejos.. Table of contents JustificationAmong all ...

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Origins of the specialization for letters and numbers in ventral occipitotemporal cortex

Cited by 201 publications

References 102 publications

Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

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

Brain bases of the automaticity via visual search task

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