What Brain Imaging Tells us about Reading Acquisition

What Brain Imaging Tells us about Reading Acquisition and Intervention Guinevere Eden Center for the Study of Learning Gallaudet University Georgetown University Supported by the NIH and NSF Wake Forest University

Reading is a Cultural Invention First use of alphabet - 1800 B. C. Divination Characters on Oracle Bones Shang Dynasty 1400 -1100 BC

Reading has to be Learned – in Different Ways Alphabetic Logographic Bolger et al. (2005)

Learning to Read Changes the Brain Petersson et al. (2007) Dehaene et al. (2010)

LDAH

Brain Imaging

Franz Gall (1758 -1828) Phrenology

10 Second Cortical Anatomy Motor Touch Vision Hearing

Parallel Visual Pathways Dorsal pathway Where What Ventral pathway (parvocellular): form color object identification face identity (magnocellular): motion location mental rotation spatial relationships

Left Hemisphere: Right Hemisphere: Word Form Area Face/Object Area

Face Processing Kanwisher et al, 1997

Gauthier et al. , 1999

Left Hemisphere: Right Hemisphere: Word Form Area Face/Object Area

● Reading Acquisition ● Precocious Reading ● Reading Disability

Learning to Read • Phases of reading acquisition (Ehri, 1992) – Pre-alphabetic- visual – Partial alphabetic- phonological cues – Full alphabetic- decoding – Consolidated Alphabetic- chunking, analogy • Phonological processing abilities are critical (Wagner and Torgesen, 1987)

Research Questions • What is the neural basis of visual word processing in healthy children? • How does the neural basis of word processing change during schooling? • What is the relationship between these neural systems and phonological skills?

Reading in Typical Children Simos et al. , 2001 8 year old 28 year old MEG (MSI) 12 Children (8 -15 years) 16 Adults (23 -28 years) Real word recognition Increasing left inferior frontal gyrus Lateralization of infero-temporal cortex No change in left temporoparietal cortex

The neural basis of reading • Left inferior frontal gyrus • Left temporoparietal cortex • Left inferotemporal cortex

The neural basis of reading • Left inferior frontal gyrus • Left temporoparietal cortex • Left inferotemporal cortex Orthography Direct Lexical Access

The neural basis of reading • Left inferior frontal gyrus • Left temporoparietal cortex • Left inferotemporal cortex Cross-modal integration Phonological assembly Semantics

The neural basis of reading • Left inferior frontal gyrus • Left temporoparietal cortex • Left inferotemporal cortex Semantics Phonological assembly

Center for the Study of Learning, Georgetown University

Implicit Word Processing - = Adapted from Price et al, 1996 41 normal subjects

Task Performance Words vs. False Fonts Reaction Time R 2=. 00 n. s. 20 Reaction Time Difference (ms) Accuracy Difference (% correct) Accuracy 15 10 5 0 -5 -10 -15 6 8 10 12 14 16 18 20 22 Age (Years) R 2=. 03 n. s. 200 150 100 50 0 -50 -100 -150 -200 6 8 10 12 14 16 18 20 22 Age (Years)

Implicit Reading Activity 6 - 9. 4 y 9. 4 - 18 y 20 - 23 y n=13 n=15 Turkeltaub et al. Nature Neuroscience, 2003

f. MRI Developmental Changes in Activity Reading Composite p<. 001, peak p<. 0001

Samuel Orton 1925 “In the process of early visual education… the storage of memory images of letters and words occurs in both hemispheres…. the process of learning to read entails the elision from the focus of attention of the confusing memory images of the nondominant hemisphere”

Phonology and Reading • Types of phonological processing (Wagner & Torgesen, 1987) – Phonological awareness (LAC) – Phonological naming (RAN) – Working memory (Digit Span) • Subtypes of dyslexia are associated with these types of phonology • Are these abilities associated with different aspects of reading?

1998 2000

National Reading Panel, 2000: Five Component Skills Essential for reading Phonemic Awareness Phonics Fluency Vocabulary Comprehension strategies Identifying words accurately and fluently Constructing meaning once words are identified

Phonological Awareness Lindamood Auditory Conceptualization Test (LAC) “Show me /p/ /t/ /p/” “If this says ‘eth’, show me ‘ith’

Phonological Naming Rapid Automatized Naming Test (RAN) s a o d o p a p d o s d a o a p s p d s o p s p d o s a o p a d o p s p a s d s p o a o d

Working Memory Digit Span “ 3 8 2 4” “ 7 4 6 2 5” “ 9 2 3 6 1 8” “ 5 3 8 2 7 4 6” “ 2 5 4 3 2 8 9 4”

Correlations with Phonology Phonological Awareness Phonological Recoding Working Memory p<. 005, peak p<. 0005 Turkeltaub et al. Nature Neuroscience, 2003

Conclusions Young Readers Phonology Young readers activate left temporoparietal cortex, related to phonological awareness

Conclusions Young Readers Phonology Young readers activate temporoparietal cortex, related to phonological awareness Reading Acquisition Reading acquisition= Right posterior cortex (nonlinguistic visual) Left frontal & temporal (phonology, semantics)

Reading in Children Aged 6 to 9 Chinese and American Data provided by LH Tan Turkeltaub et al. , 2003

The neural basis of precocious reading acquisition: f. MRI case study of hyperlexic reading

Hyperlexia • Developmental disorder of communication (usually autism spectrum) • Extremely precocious reading learned very early without explicit instruction • Reading scores above expectation, with comprehension commensurate with verbal ability • Incidence ≈ 2 / 10, 000 (Burd et al. , 1985, Yeargin- Allsopp, 2003)

Ethan • 10 -year-old boy • Disordered – expressive/receptive language (first word at 3. 5 y) – social interaction – motor coordination • Pervasive Developmental Disorder- Not Otherwise Specified • Early intense interest in text • Precocious reading

Ethan’s Reading Scores Word I. D. Word Attack GORT Passage GORT Comp. Age eq. 5 y-11 m 8 y-10 m 9 y-4 m 10. 3 <7. 9 9 y-9 m 15 y-1 m 16 y-11 m 14. 9 12. 1 Age

Dyslexic vs. Hyperlexic Reading Words Dyslexic 11. 1 yr therapeutic bouquet trivialities Hyperlexic 7. 0 yr

Hyperlexia Hypotheses Left Hemisphere Phonological Advantage Welsh et al. , 1987 Right Hemisphere Visual Advantage Cobrinik, 1982

Methods • Same f. MRI methods as cross sectional study • Compared Ethan to two control groups – Age Matched (n=9) – Reading Matched (n=8)

Ethan- Implicit Reading Turkeltaub et al. , Neuron 2004 P<. 005

Ethan vs. Controls Left Hemisphere Age Matched (n=9) Reading Matched (n=8)

Ethan vs. Controls Right Hemisphere Reading Acquisition Age Matched (n=9) Reading Matched (n=8) Turkeltaub et al. Neuron, 2004

Hyperlexia Hypotheses Left Hemisphere Phonological Advantage Welsh et al. , 1987 Right Hemisphere Visual Advantage Cobrinik, 1982

Conclusions • In contrast to single hemisphere theories, Ethan demonstrated both – Hyper-activity in left hemisphere phonological areas – Increased activity in right hemisphere visual areas • Left temporoparietal cortex is hyperactive in hyperlexia

Reading Research Policy and Education Basic Research Translational Research

The International Dyslexia Association / NICHD Research Definition of Dyslexia is a specific learning disability that is neurological in origin. It is characterized by difficulties with accurate and / or fluent word recognition and by poor spelling and decoding abilities. . .

The International Dyslexia Association / NICHD Research Definition of Dyslexia … These difficulties typically result from a deficit in the phonological component of language that is often unexpected in relation to other cognitive abilities and the provision of effective classroom instruction…

The International Dyslexia Association / NICHD Research Definition of Dyslexia … Secondary consequences may include problems in reading comprehension and reduced reading experience that can impede growth of vocabulary and background knowledge.

Developmental Dyslexia Research • Behavioral Evidence • Anatomical and Physiological evidence • Genetic evidence Practice • Early identification • Remediation

Developmental Dyslexia • 15% of the population is Learning Disabled • 75 -80% or these are Dyslexic • 5 to 12 % school aged children in the US have basic deficits in reading (IQ discrepant model versus low achievement) • Males and females a not equally affected

Developmental Dyslexia • 74% of poor 3 rd graders were still impaired when tested in high school • “Compensated” adult dyslexics still demonstrate measurable underlying problems • 60% of poor adult readers have undetected or untreated LD • 50% of juvenile delinquents have undetected LD

Developmental Dyslexia Research • Behavioral Evidence • Anatomical and Physiological evidence • Genetic evidence Practice • Early identification • Remediation

Behavioral Evaluation of Dyslexia Measurement: • Single Word Reading • Phonemic Awareness • Automatic Naming Speed • Sequential Working Memory

Behavioral Evaluation of Dyslexia Measurement: Single Word Reading • Phonemic Awareness • Automatic Naming Speed predictive • Sequential Working Memory

Behavioral Manifestations of Developmental Dyslexia • Phonological Processing – Sound segmentation and manipulation – Rapid name retrieval – Verbal working memory

Behavioral Manifestations of Developmental Dyslexia • Phonological Processing – Sound segmentation and manipulation – Rapid name retrieval – Verbal working memory • Sensorimotor Processing – Visual motion processing – Motor coordination – Auditory processing

Ramus, TINS 2004

Visual Motion Perception: Controls versus Dyslexics Eden et al. , Nature 1996

Demb et al. , 1997 Proc. Nat. Acad. Sci.

Ramus, TINS 2004

Ramus 2004 • Genetically driven focal cortical abnormalities disrupt processes in the left hemisphere (phonological processing) • Under certain hormonal conditions these disruptions propagate to the thalamus, leading to sensory impairment • These disruptions also extend to posterior parietal cortex and cerebellum

Developmental Dyslexia Research • Behavioral Evidence • Anatomical and Physiological evidence • Genetic evidence Practice • Early identification • Remediation

Anatomical Variations Left I II IV Right V VI Galaburda et al. 1985

Neural Basis of Dyslexia: Structural MRI Studies Findings reported only once Findings reported more than once Eckert et al. 2004

Left Hemisphere White Matter Tracts and Dyslexia • Reduced fractional anisotropy (FA) in L arcuate fasciculus. • Positive correlation of L arcuate fasciculus FA with PA. • Positive correlation of L inferior fronto-occipital fasciculus FA with orthographic processing. Vandermosten et al. 2012

White Matter Studies of Dyslexia Children • Compared to Typical Readers – – – – • Reduced FA in left IFG (Rimrodt et al. , 2010) Reduced FA in left temporo-parietal WM (Rimdodt et al. , 2010) Reduced FA of inferior-fronto occipital fasciculus (Rollins et al. , 2009) Reduced FA of inferior longitudinal fasciculus (Rollins et al. , 2009) Increased posterior corpus collosum (Hasan et al. , 2012) Reduced left superior longitudinal fasciculus FA (Carter et al. , 2009) Abnormal orientation of right superior longitudinal fasciculus (Carter et al. , 2009) Correlations – – Positive for reading speed and left IFG FA (Rimrodt et al. , 2010) Positive for posterior corpus collosum mean diffusivity with word reading and comprehension (Hasan et al. , 2012) Positive for superior corona radiata and single/pseudoword reading (Odegard et al. , 2009) Positive for left temporo-parietal WM with reading scores (Niogi and Mc. Candliss, 2006) Adults • Compared to Typical Readers – Reduced FA of left arcuate fasciculus (Vandermosten et al. , 2012) – Reduced FA in bilateral temporo-parietal WM (Klingberg et al. , 2000) – Reduced FA bilateral fronto-temporal WM (Steinbrink et al. , 2008) – Reduced FA left temporo-parietal WM (Steinbrink et al. , 2008) • Correlations – Positive for phonemic awareness and speech perception with FA of left arcuate fasciculus (Vandermosten et al. , 2012) – Positive for left temporo-parietal WM and reading score (Klingberg et al. , 2000)

Flowers, Wood, & Naylor, 1991

Neurobiological Basis of Reading Typical Readers

Neurobiological Basis of Reading Typical Readers Dyslexic Readers

Phoneme Deletion TASK Task Stimulus fixate repeat delete + rat rat Response Processes fixation vocalization at vocalization + phonological manipulation

Typical Readers: Deletion versus Repetition left right

Dyslexic Readers: Deletion versus Repetition left right

Group Comparison: Controls > Dyslexics left right Eden et al. , Neuron 2004

Dyslexia across cultures: same or different? Same brain region less active in dyslexics during reading tasks in all countries Controls > Dyslexics Paulesu et al. , 2001

Developmental Dyslexia Research • Behavioral Evidence • Anatomical and Physiological evidence • Genetic evidence Practice • Early identification • Remediation

Genetic Basis of Dyslexia • 75 - 100% concordance in monozygotic twins • 35 - 40% concordance in first degree relatives • Chromosomes 1, 2, 6, 15 and 18 are implicated in various studies

Developmental Dyslexia Research • Behavioral Evidence • Anatomical and Physiological evidence • Genetic evidence Practice • Early identification • Remediation

Early Identification • Letter and word recognition (correctly pronouncing printed letters and words) • Phonemic awareness (recognition of specific sounds in a word) • Naming speed (speed of naming of letters, digits or common objects that are already known) Predictive Assessment of Reading (PAR) Source: Wake Forest University

Early Identification Predictive Assessment of Reading (PAR) Source: Wake Forest University

Early Identification of Dyslexia Comprehensive Test of Phonological Processing (CTOPP) Early Literacy Screening (NCLD) Fox in a Box Predictive Assessment of Reading (PAR) Phonological Awareness Literacy Screening (PALS) Test of Word Reading Efficiency (TOWRE) Test of Phonological Awareness (TOPA) Texas Primary Reading Inventory Source: Parenting a Struggling Reader, Hall & Moats

Developmental Dyslexia Research • Behavioral Evidence • Anatomical and Physiological evidence • Genetic evidence Practice • Early identification • Remediation

Remediation Approaches • Phonology and other language structures are explicitly and systematically taught • Large amount of practice given & small group or one-one • Use of enhancing techniques (multi-sensory techniques linking listening, speaking, reading, and writing)

Examples of Multisensory Remediation Approaches Orton-Gillingham Alphabetic Phonics Slingerland Spaulding Wilson Language LANGUAGE! Project Read http: //www. interdys. org/ Sonday System Lindamood-Bell Phonographix June and Samuel Orton

Research and Science Policy No Child Left Behind Act, Reading First, 2001 • Requires methods that are used in the classroom to teach children how to read to be based upon valid scientific findings • Based on findings from the National Reading Panel: Meta-analysis of scientific studies on reading that met certain criteria

Institute of Educational Sciences US Department of Education Guidelines on how to evaluate whether an educational intervention is supported by rigorous evidence Randomized controlled trials + Effective in two or more settings = Strong Evidence Pre-post studies do not comprise “strong” or even “possible evidence” - often produce erroneous results

Institute of Educational Sciences US Department of Education Coalition for Evidence-Based Policy “There a vast array of educational interventions that claim to improve educational outcomes and to be supported by evidence…. . . introduced with great fanfare as being able to produce dramatic gains… …yielding little in the way of positive and long lasting changes”

After Intervention ( Before Intervention - = )

Pretesting Posttesting Dyslexia-specific brain activation profile becomes normal following successful remedial training Simos, Fletcher, et al. Neurology, 2002

Developmental Dyslexia Research • Behavioral Evidence • Anatomical and Physiological evidence • Genetic evidence Practice • Early identification • Remediation

Standard Score Growth in Total Reading Skill Before, During, and Following Intensive Intervention 95 90 85 LIPS 80 EP 75 P-Pretest Pre Post 1 year 2 year Interval Between Measurements Torgesen, et al. , 2001

Study Design • Assignment of individuals into different interventions • Groups are equal in reading measures prior to the intervention • Compare the two groups after intervention Group 1 Group 2 Pre intervention A Post intervention B

June and Samuel Orton

Adult Phonological Intervention Study Subjects: • 20 Adults from Orton Center, recruited through Wake Forest University Intervention: • 112. 5 hours of Lindamood-Bell (over 8 weeks) Before and after measures: • Behavior: reading, phonemic awareness • Physiology (f. MRI): phonemic segmentation

Skills Targeted by Intervention Visual Imagery (SI) Phonemic Awareness (TAAS)

Skills Supporting Reading Non-Word Reading (WJWASS) Phonemic Transfer Index (DST)

Oral Reading Skills Real Word Reading Accuracy Reading Rate Reading (WRAT) (GORT) Comprehension (GORT)

After Intervention ( Before Intervention - = )

Intervention Before After No Intervention

ANOVA Group x Day: Increases in Activity Following Intervention left right Eden et al. , Neuron 2004

ANOVA Group x Day: Increases in Activity Following Intervention left right Eden et al. , Neuron 2004

Conclusion • After phonological intervention adults with dyslexia show increased activation in the left and right hemispheres. • The right hemisphere areas are similar to those in the left hemisphere involved in phonological processing in good readers.

Increases in Activity Following Intervention Children Left Inferior Frontal Gyrus: increases in children (average 9 years) N=32

Skills Targeted by Intervention *** ** *** p<0. 001, ** p<0. 01, * p<0. 05

Reading Skills *** *** p<0. 001, ** p<0. 01, * p<0. 05

Skills Supporting Reading * *** p<0. 001, ** p<0. 01, * p<0. 05

What else changes in the brain? What’s the matter GRAY MATTER?

Draganski et al. , Nature 2004

Research Design • 11 dyslexic children: reading intervention followed by no instruction No Intervention Reading Intervention SCAN 1 SCAN 2 8 weeks SCAN 3 8 weeks • Anatomical scans obtained at each time point for analysis of gray matter volume

Behavioral Changes After Intervention

Gray Matter Volume Increases After Intervention Left Fusiform/Hippocampus Left Precuneus Right Hippocampus Right Cerebellum

Percent Change in Gray Matter Volume

Overall Summary • Regions know to be involved in the processing of information from multiple sensory modalities are also involved in reading. • The neurobiological representation of reading is established early on.

Overall Summary • Dyslexic individuals show under- activity in these regions, especially parietal cortex. • Brain activity changes following intensive remediation. Adults and children exhibit different patterns. • Structural changes are also observed following intervention.

Who will have the greatest reading gains after the intervention? Those who show brain activity in inferior parietal cortex prior to the intervention. Activity here is predictive of the amount of reading improvement.

Developmental Dyslexia Research • Behavioral Evidence • Anatomical and Physiological evidence • Genetic evidence Practice • Early identification • Remediation

Wake Forest University Lynn Flowers Frank Wood Debi Hill Gallaudet University Carol La. Sasso Kelly Crain John Agnew Kate Cappell Emily Curran Emma Cole Iain De. Witt Erin Einbinder Lynn Gareau Karen Jones Daniel Koo Anthony Krafnick Joe Maisog Martha Miranda Alison Merikangas Corinna Moore Eileen Napoliello Olumide Olulade Jenni Rosenberg Peter Turkeltaub Robert Twomey John Van. Meter Supported by NSF, NICHD, NIDCD, NIMH

The 63 rd International Dyslexia Association Annual Conference http: //www. interdys. org/

http: //csl. georgetown. edu