Neuroimaging Studies of Cognitive Development: Insights from Reading Research

1. Neuroimaging Studies of Cognitive Development: Insights from Reading Research • Kenneth R. Pugh, PhD • Yale University School of Medicine and Haskins Laboratories, New Haven CT.

2. Collaborators • Haskins Laboratories: Einar Mencl, Rebecca Sandak, Stephen Frost, Dina Moore, Stephanie Mason, Leonard Katz, Jay Rueckl, Donald Shankweiler, Annette Jenner, Jun Ren Lee, Carol Fowler, Alvin Liberman • Yale Reading Center: Ken Pugh (Director),Gina Della Porta, Kelley Delaney, Vanessa Dinicola, Priya Pugh, Michael Kochis • Yale Center for the Study of Learning and Attention: Bennett Shaywitz, Sally Shaywitz, Karen Marchione, John, Holahan, Jack Fletcher • Yale University/Diagnostic Radiology: John Gore, Todd Constable, Robert Fulbright, Pawel Skudlarski, Cheryl Lacadie

3. Why study brain? Reasons vary with discipline (e.g.,neuroscience, cognitive science, development or educational psychology) 1) Heritability studies suggest complex gene/environment contributions to atypical development. Neurobiological measures (e.g., measures of neuroanatomy, neurochemistry, or functional organization) yield mediating levels of analysis between gene and behavioral phenotype. 2) Better computational models: neural constraints from cooperative and competitive dynamics. 3) A potentially better account of individual differences in either typical or atypical development and individual differences in optimal intervention strategies for at-risk children. What works for whom. 4) Early detection of biomarkers associated with atypical cognitive development.

4. Language Reading and Brain • The development of fluent reading skill is essential for success in the modern world. • Significant numbers of children in all countries fail to acquire adequate literacy skills. • For many this is due largely to lack of good learning experience but for some will reflect difficulties that are brain-based (Reading Disability).

5. Outline of talk • 1) Neurobiological research must be grounded by solid cognitive/behavioral knowledge of strengths and weaknesses in typically and atypically developing readers. • 2) Mapping the reading circuit in typically or atypically developing readers: Basic taxonomy and developmental trajectories. • 3) Mapping the reading circuit in typically developing readers:Sub-specialization across the reading circuitry. • 4) Mapping the reading circuit in typically developing readers: Tradeoffs and dynamic changes associated with learning. • 5) Remediation and plasticity in struggling (RD) readers. • 6) New directions: multiple levels of analysis, cross linguistic accounts, early identification of risk factors.

6. How do skilled readers recognize words • 1) Skilled readers can read words fast (approx. 200-250 msec. to initial lexical acess) • 2) Pseudoword reading is nearly as fast! • Fluency depends on adequate integration of orthography, phonology, and semantics.

7. Impaired Word recognition in reading disability • Word identification is slow, labored, and error prone in RD (bottleneck for comprehension). • Early deficits in developing fine-grained phonemic awareness predict word reading difficulties later on. • These deficits in phonological awareness impede the development of efficient phonological assembly routines (grapheme to phoneme mapping) which, in turn, places severe limits on word (and pseudoword) reading fluency.

8. Outline of talk • 1) Neurobiological research must be grounded by solid cognitive/behavioral knowledge of typical and atypical strengths and weaknesses. • 2) Mapping the reading circuit in typically and atypically developing readers: Basic taxonomy and developmental trajectories. • 3) Mapping the reading circuit in typically developing readers:Sub-specialization across the reading circuitry. • 4) Mapping the reading circuit in typically developing readers: Tradeoffs and dynamic changes with learning. • 5) Remediation and plasticity in struggling (RD) readers. • 6) New directions: multiple levels of analysis, cross linguistic accounts, early identification of risk factors.

9. Language and Brain • Spoken language is a biological specialization but written language is largely a cultural invention. Moreover, spoken language is mastered naturally in almost all people, without direct instruction, but reading is difficult and reading failure occurs in large numbers of children across all written languages. • Implication: Literacy acquisition is a major challenge to brain plasticity.

10. Slice Locations

11. Auditory versus Visual Sentence Task Constable, Pugh et al., (2004)

12. Initial Model Individual Regions Pugh et al., 2000

13. Temporoparietal Anterior Occipitotemporal Left Hemisphere Reading Disability • Frequent finding: A large number of studies indicate that RD readers tend to under-activate both LH temporoparietal and LH ventral (occipitotemporal) regions during reading- and language tasks; this has been seen in several languages to date (Paulesu et al., 2001). • RH and frontal compensatory shift in RD

14. TD & RD Reading Children (Temple et al., 2004) Normal Readers Frontal & Temporo-parietal Frontal but NO Temporo-parietal Dyslexic Readers

15. Reading development: Establishing skill-related trajectories in NI and RD children (Shaywitz, Shaywitz, Pugh et al., 2002) (n= 144; ages 7-17)

16. Correlating activation with age and skill. • 1) Correlating brain activation with chronological age in NI and RD. This is aimed at addressing the question of whether neuro-developmental trajectories are similar or dissimilar in the two cohorts. • 2) Correlating activation with reading skill (after co-varying out age effects) allows us to isolate those neural systems that support fluent and accurate reading.

18. Reading Development: “Skill Zone” in Putative VWFA Activation Woodcock-Johnson Word Attack

19. Increases in reading skill are associated with increased specialization of ventral LH areas Plasticity in Reading Development • Beginning TD readers activate a widely distributed set of regions including temporoparietal and anterior sites. Temporoparietal Anterior Occipitotemporal

20. Overview of talk • 1) Neurobiological research must be grounded by solid cognitive/behavioral knowledge of typical and atypical strengths and weaknesses. • 2) Mapping the reading circuit in typically and atypically developing readers: Basic taxonomy and developmental trajectories. • 3) Mapping the reading circuit in typically developing readers:Sub-specialization across the reading circuitry. • 4) Mapping the reading circuit in typically developing readers: Tradeoffs and dynamic changes with adaptive learning. • 5) Remediation and plasticity in struggling (RD) readers. • 6) New directions: multiple levels of analysis, cross linguistic accounts, early identification of risk factors.

21. Initial Model Individual Regions

22. Developing a more fine-grained taxonomy (Pugh et al., 2005) • Using multiple tasks (and by manipulating orthographic, phonological, morphological, and semantic variables) we hope to develop a more detailed account of sub-specializations in the major LH reading systems (e.g.,determine which sub-regions are phonologically, morphologically, or semantically “tuned”). • Provides a more precise foundation from which to interpret RD differences. • Major focus is on the “tuning” characteristics of the skill correlated VWFA and yoked regions. • *General Design feature: Multiple experiments, each manipulating demands on a given factor in different ways, allows us to implement Garner’s principle of converging operations

23. Expt. 1: Comparison of semantic vs. phonological priming We used a double lexical decision task with 20 NI adolescent readers: • Prime types: BRIBE-TRIBE (O and P similar); COUCH-TOUCH (O similar, P dissimilar), OCEAN-WATER (semantically related) vs. HORSE-BRIBE (unrelated control).

25. Phonologically-tuned subsystems (Pugh et al.,2005) • Across seven studies identical voxels in the supramarginal gyrus (within the temporoparietal system), IFG (within the anterior system) and the PutativeVWFA (“Skill Zone” within the occipitotemporal system) showed phonological tuning characteristics. • * A crucial functional linkage between the skilled-related “VWFA” and more phonologically-analytic SMG and IFG regions is implied.

26. Semantically-tuned subsystems • By contrast, the angular gyrus (within the temporoparietal system) the middle/inferior temporal gyrus (within the ventral system), and ventral sites in frontal lobe, appear to have more abstract lexico-semantic functions across our studies (see Price et al., for similar claims). • Key: individual differences in activation patterns across subsets of these regions may be linked to individual differences in core deficits in behavioral performance, suggesting different approaches to remediation.

27. SMG/STG AG OT/ VWFA IFG MTG/ITG Updated view: The Reading Network • Hypothesized Role of component circuits • ‘Phonological’ • IFG • SMG/STG • ‘Semantic’ • MTG/ITG • AG • Putative ‘Visual word form Area’ • “Skill Zone” is phonologically and morphologically tuned

28. Outline of talk • 1) Neurobiological research must be grounded by solid cognitive/behavioral knowledge of typical and atypical strengths and weaknesses. • 2) Mapping the reading circuit in typically developing readers: Basic taxonomy and developmental trajectories. • 3) Mapping the reading circuit in typically developing readers:Sub-specialization across the reading circuitry. • 4) Mapping the reading circuit in typically developing readers: Tradeoffs and dynamic changes with adaptive learning. • 5) Remediation and plasticity in struggling (RD) readers. • 6) New directions: multiple levels of analysis, cross linguistic accounts, early identification of risk factors.

29. Implications of tradeoff and adaptive learning studies • An adequate theory, whether behavioral or neurobiological must be able to account not just for “main effects” , but instead such models stand or fall on their handling of complex interactions. • The data on tradeoff and adaptive learning, properly integrated into computational models, can yield key insights into individual differences in performance and development.

30. Frost,Mencl, Sandak, Moore, Mason, Rueckl, Katz, & Pugh (2005). • Can we identify the neural signature of the trade-off between semantics and phonology? • Phonology: The consistency effect. Consistent words (e.g., BEND) have a one to one orthographic to phonology mapping are named more rapidly than inconsistent words (e.g. BOWL)which have a one to many O > P mapping. • Semantics: Imageability. Concrete words (e.g., HORSE) have “richer” semantics and are named more quickly than abstract words (E.G., TRUTH). • Frequency: Word familiarity; high frequency words are named more quickly than low frequency words

31. Modulation of consistency effect by frequency and imageability • 1) Inconsistent words (e.g.,BOWL) are named more slowly than consistent words (e.g.,BEND) in general; this is referred to as the consistency effect. • 2) But this consistency effect on latencies is reduced for both high frequency and/or for high imageable words. • Top down modulation on phonological assembly (tradeoff) is seen behaviorally. • Q) WHAT ARE THE BRAIN CORRELATES OF THIS THREE WAY INTERACTION?

32. Design Go/no-go naming in a block fMRI session Stimuli: • Words (Consistency x Imageability x Frequency) • Pseudowords

33. Region of interest analysis IFG = Consistency (Main effect) MTG =Imageability (Main effect)

34. Implication: A tradeoff in activation patterns between semantically and phonologically tuned subsystems, suggests complex interactions among subsystems in response to stimulus characteristics. • Activation patterns directly mirror latency and accuracy data in this three way interaction between consistency, imageability, and frequency.

35. Sandak,Mencl, Frost, Rueckl, Katz, Moore, Mason, Fulbright, Constable, & Pugh (2004). Isolating the neurobiological signature of adaptive learning • What roles do distributed brain systems play in learning to read new words? • Three training conditions with multiple exposures: focused on orthographic, phonological, or semantic features.

36. NOIST PLOTE LANG LANG CCVCV BROAT BUG Design Pre-MRI behavioral training: Orthographic Phonological Semantic

37. Behavioral Results: transfer to simple naming fMRI cohort Pilot cohort

38. fMRI Session: Participants simplynamed: • trained pseudowords • untrained (novel) pseudowords • real words (high- & low-imageable)

39. Higher activation Lower activation Effect of Phonological Training R L z=+41 +32 +23 +14 +5 -5 -16 -27 Conjoint p < .01, uncorrected

40. Higher activation Lower activation Effect of Semantic Training R L z=+41 +32 +23 +14 +5 -5 -16 -27 Conjoint p < .01, uncorrected

41. Implications • Reinforcing different dimensions (e.g. phonological or semantic) facilitate word learning via different neural pathways. • Deficits in one or another pathway in subtypes of poor readers might suggest different training foci. • *Note: follow-up study recently examined combined training and showed greater learning with combined phonological and semantic conditions.

42. Neural Dynamics: Tradeoffs and Adaptive Learning • We need neurobiologically grounded computational models of reading development to help us make sense of learning dependent decreases and increases in brain responses, and to more adequately account for individual differences. Computational Modeling Neuroimaging

43. Outline of talk • 1) Neurobiological research must be grounded by solid cognitive/behavioral knowledge of typical and atypical strengths and weaknesses. • 2) Mapping the reading circuit in typically developing readers: Basic taxonomy and developmental trajectories. • 3) Mapping the reading circuit in typically developing readers:Sub-specialization across the reading circuitry. • 4) Mapping the reading circuit in typically developing readers: Tradeoffs and dynamic changes with adaptive learning. • 5) Remediation and plasticity in struggling (RD) readers. • 6) New directions: multiple levels of analysis, cross linguistic accounts, early identification of risk factors.

44. Increases in reading skill are associated with increased reading specialization at ventral LH zones. Plasticity in Reading Development • Beginning readers activate a widely distributed set of regions including temporoparietal and anterior sites. Temporoparietal Anterior Occipitotemporal

45. RD readers do not tend to show this neurodevelopmental trend. • Trajectory is rightward and frontward. • Question: Does intervention normalize this trajectory? Temporoparietal Anterior Occipitotemporal

46. Testing effects of intensive phonological remediation in RD in emergent readers • Overview: In collaboration with Dr. Benita Blachman (Syracuse University) we examined neurobiological changes associated with a nine month intervention emphasizing phonological awareness, alphabet principle, and vocabulary development in young children (Shaywitz et al., 2004). • 3 Groups: NI (N = 28); RD control (N =12), RD Treatment (N = 32). Each group scanned at baseline (average age = 6.5), one year later (post-treatment), and for the RD Treatment Group at one year follow up. • (see Simos et al., Temple et al., and Eden et al for similar intervention data with different phonological training protocols)

47. Testing effects of intensive phonological remediation in RD in emergent readers • Key behavioral result: Reliable improvement on a battery of reading-related tests for the treatment relative to the control RD group (Blachman et al., 2005) after nine months of intensive evidence based training.Effects stable at one year follow up.

49. Treatment Group: Year 3 (follow-up) minus Year 1 (Pre-Treatment)

50. What have we gained from these neurobiological studies of remediation in at risk readers? • The identification of a neurobiological signature of successful intervention (LH posterior increases) yields a potentially very sensitive outcome measure to help discriminate between different approaches that might all produce some transient gains in reading performance.