Usha Goswami
Alan J. Power
Marie Lallier
Andrea Facoetti- 1Department of Psychology, Centre for Neuroscience in Education, University of Cambridge, Cambridge, UK
- 2Basque Centre on Cognition, Brain and Language, San Sebastian, Spain
- 3General Psychology, University of Padua, Padua, Italy
Human cognitive systems such as language represent the sensory world as unitary. For example, the “speech signal” is perceived as a single auditory stimulus, and different visual features and textures in the visual field are perceived holistically as unitary objects. Yet sensory neuroscience demonstrates the diversity of encoding in the neural systems supporting sensory perception. Different aspects of sensory information are processed in parallel, often at different timescales and by different populations of neurons. Further, research into the function of neuronal oscillations (e.g., Buzsáki and Draguhn, 2004) reveals a key role in processing sensory information. In this special issue, we investigate the developmental implications of one neuroscientific theory based on oscillations that is relevant to reading education and developmental dyslexia, the “temporal sampling” framework (hereafter TSF, Goswami, 2011). The TSF identifies specific oscillatory mechanisms that may be impaired in dyslexia. We expect that deeper understanding of neural mechanisms of information-processing will eventually enable deeper understanding of developmental disorders of learning, such as dyslexia. Developmental dyslexia is a disorder in the acquisition of successful reading and spelling skills that is found in ~7% of children across cultures.
The ability to read and write—the achievement of literacy—is one of the most complex and sophisticated cognitive skills developed by the brain. Literacy skills develop as a result of direct teaching, usually in childhood, and become fluent during years of practice. By adulthood, most brains have read millions of words. This makes it difficult to disentangle cause from effect when studying sensory and neural factors. Dyslexia is usually only diagnosed after 2–3 years of schooling, when the brain has already had considerable experience of reading and reading tuition. Dyslexia is diagnosed when children who are receiving adequate teaching and who have no overt sensory or neurological problems fail to develop fast, efficient and age-appropriate reading and spelling.
The TSF was proposed as the neural basis for the extraction of phonological information from speech via auditory oscillatory encoding (Goswami, in press). Based on work by Poeppel, Greenberg, Giraud, Ghitza and many others (Giraud and Poeppel, 2012, for a recent summary), the TSF linked “sampling” of the speech stream by auditory cortical networks operating at different timescales or oscillatory frequencies (delta, theta, gamma) to the emergence of phonological (linguistic) coding of speech by children. Poeppel and others argued that cortical oscillations enabled the representation of different temporal rates of amplitude modulation in the complex speech signal. These temporal frequency bands yield complementary “windows” of information relating to cognitive linguistic units such as syllables (theta rate) and phonemes (gamma rate, see Poeppel, 2003). Accordingly, the TSF proposed that atypical oscillatory sampling at one or more temporal rates in children with dyslexia could cause phonological difficulties in specifying linguistic units such as syllables.
Phonological difficulties in dyslexia are related to difficulties in the accurate perception of amplitude “rise time” (related to modulation rate). The TSF proposed that atypical oscillatory entrainment at syllable-relevant rates of amplitude modulation (delta [~ stressed syllable rate], theta [~ syllable rate]) could be one neural cause of the “phonological deficit” found in children and adults with dyslexia across languages and orthographies. This theory is about early developmental mechanisms, nevertheless impaired oscillatory sampling in auditory cortex could, over developmental time, lead to atypical functioning of the left-lateralized “reading network” identified in many fMRI studies of older children (Richlan, 2012, for a recent overview; Clark et al., 2014, for a relevant longitudinal study). This should be true across languages. Indeed, rise time perception is impaired in English, French, Spanish, Hungarian, Finnish, Chinese, and Dutch dyslexic children (see Goswami and Leong, 2013, for an overview). The “phonological deficit” in dyslexia is found in all of these languages, and manifests as difficulties in oral tasks such as recognizing prosodic stress, counting syllables, and counting or deleting phonemes (the smallest phonological units in a language; Ziegler and Goswami, 2005, for a cross-language review). These and other phonological tasks are considered by some of the auditory-based contributions to the special issue (Lehongre et al., 2013; Power et al., 2013; White-Schwoch and Kraus, 2013; Sela, 2014 this issue).
The aim of this special issue, however, was to simultaneously invite colleagues who work on visual sensory processing to consider whether atypical oscillatory “temporal sampling” may explain the pervasive visual processing deficits in dyslexia reported in many orthographies (e.g., Facoetti et al., 2010; Lallier and Valdois, 2012). Visual and auditory sensory theories of dyslexia are typically considered to compete with each other, indeed a recent review counted 12 competing theories of developmental dyslexia (Ramus and Ahissar, 2012). The act of reading of course depends upon many visual processes. Examples are (for alphabetic orthographies) serial letter recognition, visual grouping of repeating letter patterns in familiar words, and the left-to-right (or in some orthographies, right-to-left) horizontal linear tracking of print. Practice in reading (reading experience) will obviously train the brain in aspects of visual processing related to reading. Such visual practice is necessarily reduced in children with dyslexia (reading is effortful, so the child reads less). Disentangling the effects of reading experience on the brain across the many different sensory and cognitive components that support the development of reading and writing is thus experimentally challenging. Nevertheless, by studying particular aspects of non-linguistic visual processing in isolation (such as magnocellular function, or eye movements), research can begin to disentangle cause from effect in developmental dyslexia.
In this special issue, a number of the different aspects of impaired visual and visuo-spatial attentional processing found in dyslexia are studied and possible relations with oscillatory temporal sampling are considered (see De Luca et al., 2013; Lallier et al., 2013; Conlon et al., 2013; Gori et al., 2014; Ruffino et al., 2014; Varvara et al., 2014 this issue). Theoretically, these contributions consider whether spatiotemporal sampling of information by the visual system may be impaired in dyslexia (see Pammer, 2014; Vidyasagar, 2013 this issue). Indeed, Vidyasagar argues that a visual sampling impairment may be primary to the auditory difficulties in dyslexia documented by other contributors, a provocative claim which requires longitudinal studies. In fact, in order to establish the possible causal role of different visual and auditory sensory processes to reading development, and to identify their sequential contributions during the developmental learning trajectory, a range of developmental research designs are required.
At minimum, evidence is required that:
1. the sensory/neural deficit precedes being taught to read
2. the sensory/neural deficit affects aspects of cognitive development other than reading (e.g., musical development for auditory deficits, conceptual development for visual deficits) in predictable ways
3. the sensory/neural deficit can be demonstrated when children with dyslexia are compared to younger children whose reading skills are matched with the dyslexics (this research design aims to equate the effect of reading experience on the brain; the reading level match research design)
4. developmental trajectories are followed in longitudinal studies, exploring the complex interplay of auditory and visual sensory/neural and cognitive processes during the development of reading, thereby establishing the developmental primacy of the candidate deficit
5. the sensory/neural deficit is consistent across different languages and orthographies
6. training the candidate deficit has demonstrable effects upon subsequent reading development
Longitudinal studies, beginning before reading is taught and carried out across languages, are enormously important to the field (e.g., Boets et al., 2011; Franceschini et al., 2012). Sensory/neural deficits may change over developmental time. Perhaps a sensory factor critical for early development becomes less relevant when studying older children, or is no longer apparent when studying adults. Sensory/neural deficits may also manifest differently in different languages, for example as a consequence of factors such as orthographic grain size (e.g., the phonemic grain size is practiced by readers of alphabetic languages, whereas Japanese readers practice the syllable grain size) or phonology (e.g., rhythmic or phonetic differences, such as whether a language has many sonorant phonemes and is syllable-timed, such as Spanish, or many plosive phonemes and is stress-timed, such as English). Reading difficulties may be comorbid with other difficulties such as attention-deficit-hyperactivity disorder (ADHD); the possible effects of co-morbid disorders on sensory processing must be taken into account (Thaler et al., 2009). The studies in this special issue document and calibrate some of these aspects of auditory and visual processing that seem to be important in developmental dyslexia. Incorporating all of these aspects of sensory processing into oscillatory studies will be the next task for developmental research into dyslexia.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Boets, B., Vandermosten, M., Cornelissen, P., Wouters, J., and Ghesquiere, P. (2011). Coherent motion sensitivity and reading development in the transition from prereading to reading stage. Child Dev. 82, 854–869. doi: 10.1111/j.1467-8624.2010.01527.x
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Buzsáki, G., and Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science 304, 1926–1929. doi: 10.1126/science.1099745
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Clark, K., Helland, T., Specht, K., Narr, K., Manis, F., Toga, A., et al. (2014). Neuroanatomical precursors of dyslexia identified from pre-reading through age 11. Brain. doi: 10.1093/brain/awu229. [Epub ahead of print].
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Conlon, E., Lilleskaret, G., Wright, C. M., and Stuksrud, A. (2013). Why do adults with dyslexia have poor global motion sensitivity? Front. Hum. Neurosci. 7:859. doi: 10.3389/fnhum.2013.00859
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
De Luca, M., Pontillo, M., Primativo, S., Spinelli, D., and Zoccolotti, P. (2013). The eye-voice lead during oral reading in developmental dyslexia. Front. Hum. Neurosci. 7:696. doi: 10.3389/fnhum.2013.00696
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Facoetti, A., Trussardi, A. N., Ruffino, M., Lorusso, M. L., Cattaneo, C., Galli, R., et al. (2010). Multisensory spatial attention deficits are predictive of phonological decoding skills in developmental dyslexia. J. Cogn. Neurosci. 22, 1011–1025. doi: 10.1162/jocn.2009.21232
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Franceschini, S., Gori, S., Ruffino, M., Pedrolli, K., and Facoetti, A. (2012). A causal link between visual spatial attention and reading acquisition. Curr. Biol. 22, 814–819. doi: 10.1016/j.cub.2012.03.013
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Giraud, A. L., and Poeppel, D. (2012). Cortical oscillations and speech processing: emerging computational principles and operations. Nat. Neurosci. 15, 511–517. doi: 10.1038/nn.3063
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Gori, S., Cecchini, P., Bigoni, A., Molteni, M., and Facoetti, A. (2014). Magnocellular-dorsal pathway and sub-lexical route in developmental dyslexia. Front. Hum. Neurosci. 8:460. doi: 10.3389/fnhum.2014.00460
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Goswami, U. (2011). A temporal sampling framework for developmental dyslexia. Trends Cogn. Sci. 15, 3–10. doi: 10.1016/j.tics.2010.10.001
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Goswami, U. (in press). Sensory theories of developmental dyslexia: three challenges for research. Nat. Rev. Neurosci.
Goswami, U., and Leong, V. (2013). Speech rhythm and temporal structure: converging perspectives? Lab. Phonol. 4, 67–92. doi: 10.1515/lp-2013-0004
Lallier, M., Donnadieu, S., and Valdois, S. (2013). Investigating the role of visual and auditory search in reading and developmental dyslexia. Front. Hum. Neurosci. 7:597. doi: 10.3389/fnhum.2013.00597
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Lallier, M., and Valdois, S. (2012). “Sequential versus simultaneous processing deficits in developmental dyslexia,” in Dyslexia - A Comprehensive and International Approach, eds T. N. Wydell and L. Fern-Pollak (Rijeka, Croatia: In Tech), 73–108.
Lehongre, K., Morillon, B., Giraud, A.-L., and Ramus, F. (2013). Impaired auditory sampling in dyslexia: further evidence from combined fMRI and EEG. Front. Hum. Neurosci. 7:454. doi: 10.3389/fnhum.2013.00454
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Pammer, K. (2014). Temporal sampling in vision and implications for dyslexia. Front. Hum. Neurosci. 8:933. doi: 10.3389/fnhum.2013.00933
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Poeppel, D. (2003). The analysis of speech in different temporal integration windows: cerebral lateralization as ‘asymmetric sampling in time’. Speech Commun. 41, 245–255. doi: 10.1016/S0167-6393(02)00107-3
Power, A. J., Mead, N., Barnes, L., and Goswami, U. (2013). Neural entrainment to rhythmic speech in children with developmental dyslexia. Front. Hum. Neurosci. 7:777. doi: 10.3389/fnhum.2013.00777
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Ramus, F., and Ahissar, M. (2012). Developmental dyslexia: the difficulties of interpreting poor performance, and the importance of normal performance. Cogn. Neuropsychol. 29, 104–122. doi: 10.1080/02643294.2012.677420
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Richlan, F. (2012). Developmental dyslexia: dysfunction of a left hemisphere reading network. Front. Hum. Neurosci. 6:120. doi: 10.3389/fnhum.2012.00120
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Ruffino, M., Gori, S., Boccardi, D., Molteni, M., and Facoetti, A. (2014). Spatial and temporal attention are both sluggish in poor phonological decoders with developmental dyslexia. Front. Hum. Neurosci. 8:331. doi: 10.3389/fnhum.2014.00331
Sela, I. (2014). Visual and auditory synchronization deficits among dyslexic readers as compared to non-impaired readers: a cross-correlation algorithm analysis. Front. Hum. Neurosci. 8:364. doi: 10.3389/fnhum.2014.00364
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Thaler, V., Urton, K., Heine, A., Hawelka, S., Engl, V., and Jacobs, A. M. (2009). Different behaviour and eye movement patterns of dyslexic readers with and without attentional deficits during single word reading. Neuropsychologia 47, 2436–2445. doi: 10.1016/j.neuropsychologia.2009.04.006
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Varvara, P., Varuzza, C., Sorrentino, A. C. P., Vicari, S., and Menghini, D. (2014). Executive functions in developmental dyslexia. Front. Hum. Neurosci. 8:120. doi: 10.3389/fnhum.2014.00120
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Vidyasagar, T. R. (2013). Reading into neuronal oscillations in the visual system: implications for developmental dyslexia. Front. Hum. Neurosci. 7:811. doi: 10.3389/fnhum.2013.00811
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
White-Schwoch, T., and Kraus, N. (2013). Physiologic discrimination of stop consonants relates to phonological skills in pre-readers: a biomarker for subsequent reading ability? Front. Hum. Neurosci. 7:899. doi: 10.3389/fnhum.2013.00899
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Ziegler, J. C., and Goswami, U. (2005). Reading acquisition, developmental dyslexia, and skilled reading across languages: a psycholinguistic grain size theory. Psychol. Bull. 131, 3–29. doi: 10.1037/0033-2909.131.1.3
Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar
Keywords: dyslexia, oscillations, reading, phonology, attention
Citation: Goswami U, Power AJ, Lallier M and Facoetti A (2014) Oscillatory “temporal sampling” and developmental dyslexia: toward an over-arching theoretical framework. Front. Hum. Neurosci. 8:904. doi: 10.3389/fnhum.2014.00904
Received: 04 July 2014; Accepted: 22 October 2014;
Published online: 07 November 2014.
Edited by:
Hauke R. Heekeren, Freie Universität Berlin, GermanyReviewed by:
Arthur M. Jacobs, Freie Universität Berlin, GermanyCopyright © 2014 Goswami, Power, Lallier and Facoetti. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: ucg10@cam.ac.uk