1 neuroimaging studies of cognitive development: insights from reading research kenneth r. pugh, phd...

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Neuroimaging Studies of Neuroimaging Studies of Cognitive Development: Insights Cognitive Development: Insights

from Reading Researchfrom Reading Research

• Kenneth R. Pugh, PhD

• Yale University School of Medicine and Haskins Laboratories, New Haven CT.

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CollaboratorsCollaborators

• 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

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Why study brain?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.

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Language Reading and BrainLanguage 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).

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Outline of talkOutline 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.

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How do skilled readers recognize How do skilled readers recognize wordswords

• 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.

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• 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.

Impaired Word recognition in Impaired Word recognition in reading disabilityreading disability

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• 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.


• 4) Mapping the reading circuit in typically developing readers: Tradeoffs and dynamic changes with learning.



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Language and BrainLanguage 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.

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Slice LocationsSlice Locations

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Auditory versus Visual Sentence TaskConstable, Pugh et al., (2004)

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Temporoparietal(dorsal)

Occipitotemporal(ventral)

Anterior

AGSMG

OT

ITG

MTGSTG

IFGIFGi

AG = angular gyrusSMG = supramarginal gyrusOT = occipitotemporal junctureMTG = middle temporal gyrusSTG = superior temporal gyrus

ITG = inferior temporal gyrusIFG = inferior frontal gyrus

(BA 44)IFGi = inferior frontal gyrus

(BA 45/47)

Initial Model Individual Regions

Pugh et al., 2000

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• 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

Reading DisabilityReading Disability

Occipitotemporal

Anterior

Temporoparietal

Left Hemisphere

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Normal Readers

Dyslexic Readers

TD & RD Reading Children (Temple TD & RD Reading Children (Temple et al., 2004)et al., 2004)

Frontal& Temporo-

parietal

Frontalbut NO

Temporo-parietal

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Reading development: Establishing

skill-related trajectories in NI and

RD children (Shaywitz, Shaywitz, Pugh et al., 2002)

(n= 144; ages 7-17)

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Correlating activation with age Correlating activation with age and skill.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.

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Reading Development: “Skill Zone” in Putative VWFA

Woodcock-Johnson Word Attack

Act

ivat

ion

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•Beginning TD readers activate a widely distributed set of regions including temporoparietal and anterior sites.

Plasticity in Reading DevelopmentPlasticity in Reading Development

Anterior

Occipitotemporal

Temporoparietal

• Increases in reading skill are associated with increased specialization of ventral LH areas

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Overview of talkOverview of talk


• 2) Mapping the reading circuit in typically and atypically developing readers: Basic taxonomy and developmental trajectories.


• 4) Mapping the reading circuit in typically developing readers: Tradeoffs and dynamic changes with adaptive learning.



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Temporoparietal(dorsal)

Occipitotemporal(ventral)

Anterior

AGSMG

OT

ITG

MTGSTG

IFGIFGi

AG = angular gyrusSMG = supramarginal gyrusOT = occipitotemporal junctureMTG = middle temporal gyrusSTG = superior temporal gyrus

ITG = inferior temporal gyrusIFG = inferior frontal gyrus

(BA 44)IFGi = inferior frontal gyrus

(BA 45/47)

Initial Model Individual Regions

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Developing a more fine-grained Developing a more fine-grained taxonomy (Pugh et al., 2005)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 Provides a more precise foundation from which to interpret RD differences.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 Garner’s principle of converging operationsconverging operations

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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).

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Phonologically-tuned subsystems Phonologically-tuned subsystems (Pugh et al.,2005)(Pugh et al.,2005)

• Across seven studies identical voxels in the supramarginal gyrus (within the temporoparietal system), IFG (within the anterior system) and the Putative VWFA (“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.

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Semantically-tuned subsystemsSemantically-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.

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Updated view: The Reading Updated view: The Reading NetworkNetwork

IFG MTG/ITG

OT/VWFA

SMG/STG AG

• 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

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• 2) Mapping the reading circuit in typically developing readers: Basic taxonomy and developmental trajectories.





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Implications of tradeoff and Implications of tradeoff and adaptive learning studiesadaptive 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.

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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

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Modulation of consistency effect Modulation of consistency effect by frequency and imageabilityby 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 effectconsistency 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?

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DesignDesign

Go/no-go naming in a block fMRI session

Stimuli:

• Words (Consistency x Imageability x Frequency)• Pseudowords

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IFG = Consistency

MTG =Imageability

Region of interest analysis

(Main effect)

(Main effect)

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• 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.

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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.

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DesignDesign

Pre-MRI behavioral training:

NOIST

CCVCV

PLOTE

BROAT

LANG

LANG

BUG

Orthographic Phonological Semantic

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Behavioral Results: transfer to Behavioral Results: transfer to simple namingsimple naming

Pilot cohortfMRI cohort

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fMRI Session:

Participants simply named:

• trained pseudowords

• untrained (novel) pseudowords

• real words (high- & low-imageable)

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Effect of Phonological TrainingEffect of Phonological Training

+5 -5 -16 -27

z=+41 +32 +23 +14

Higher activationLower activation

Conjoint p < .01, uncorrected

R L

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Effect of Semantic TrainingEffect of Semantic Training

+5 -5 -16 -27

z=+41 +32 +23 +14

Higher activationLower activation

Conjoint p < .01, uncorrected

R L

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ImplicationsImplications

• 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.

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Neural Dynamics: Tradeoffs and Neural Dynamics: Tradeoffs and Adaptive LearningAdaptive 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.

NeuroimagingComputational

Modeling

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• 5) Remediation and plasticity in struggling (RD) readers.

• 6) New directions: multiple levels of analysis, cross linguistic accounts, early identification of risk factors.

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•Beginning readers activate a widely distributed set of regions including temporoparietal and anterior sites.

Plasticity in Reading DevelopmentPlasticity in Reading Development

Anterior

Occipitotemporal

Temporoparietal

• Increases in reading skill are associated with increased reading specialization at ventral LH zones.

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• RD readers do not tend to show this neurodevelopmental trend.

• Trajectory is rightward and frontward.

• Question: Does intervention normalize this trajectory?

Anterior

Occipitotemporal

Temporoparietal

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Testing effects of intensive Testing effects of intensive phonological remediation in RD in phonological remediation in RD in

emergent readersemergent 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)(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)

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Testing effects of intensive Testing effects of intensive phonological remediation in RD in phonological remediation in RD in

emergent readersemergent 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.

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Treatment Group:

Year 3 (follow-up)

minus Year 1 (Pre-

Treatment)

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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.

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What is missing to date?What is missing to date?

Limitation of extant remediation studies: Contrast of single intervention with no-treatment control gives no information on treatment resistors (individual difference focus is needed).

We must use designs that contrast multiple interventions and examine learner/intervention-type interactions. What works for whom.

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Supported by the National Institute of Child Health and Human Development (NICHD) and by the Office of Vocational and Adult Education (OVAE) and the Office of Special Education and Rehabilitative Services (OSERS) of the U. S. Department of Education.

Adolescent Reading ProjectEducational Testing Service

Haskins Laboratories

Kennedy Krieger Institute

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Primary QuestionPrimary Question

What instructional approach is most effective

for struggling adolescent readers with

particular types of skills and backgrounds?

(What works for whom?)

1. To learn more about what struggling adolescent readers are like with regard to their reading skills, reading-related cognitive skills, and brain activation patterns.

2. To provide 3 kinds of reading intervention and compare their effectiveness for improving reading skills of adolescents with different initial behavioral and neurobiological profiles.

3. To see what kinds of behavioral and neurobiological changes accompany improvements in reading, and

under what conditions these changes occur.

Major Aims:

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30% fluencydecoding 70%

Corrective Reading (CR) Highly scripted, systematic phonics curriculum. Word recognition efficiency and text-reading fluency are practiced using decodable passages.

90% fluency10%

Guided Repeated Reading (GRR) Lessons include tutor modeling, shared reading, and multiple student readings of passages. Texts are selected for appeal to adolescents. Embedded phonics instruction occurs occasionally as needed.

decoding 40% 60% fluency

Decoding & Fluency Training (DeFT) Combination of CR and GRR in alternation by the same tutor.

The Three Approaches to Intervention

Students and tutors are randomly assigned to a program.

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• N=13N• pre/post training scans (across training method)

• T2 > T1 changes

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• 5) Remediation and plasticity in struggling (RD) readers. • 6) New directions: multiple levels of analysis, cross

linguistic accounts, early identification of risk factors.

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Next steps: Going beyond description.

• A mediating level of analysis in linking behavioral variation to the genetic variation (sub-group identification is critical). Functional imaging is descriptive of brain state, not inherently explanatory.

• (note new developments in genetics, sMRI, DTI, spectroscopy, etc. to get closer to mechanism).

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New NIH funded projects (2005-New NIH funded projects (2005-2010; Ken Pugh,PI)2010; Ken Pugh,PI)

• 1) Longitudinal tracking study (ages 7.5-9.5)

• Focus is on identifying genetic, neuroanatomic, neurochemistry, neurociruitry, behavioral relations over the course of reading development in typically developing and high risk childen.

• The primary goal is to develop a better understanding of brain building mechanisms in RD (why RD readers develop a poorly structured LH system for reading).

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Next steps: Cross Linguistic Next steps: Cross Linguistic researchresearch

• Cross-linguistic developmental studies will allow us to:

• 1) Identify language specific and language invariant aspects of typical development. Does the relative weighting of different regions at different stages vary systematically as a function of factors such as orthographic depth?

• 2) Identify language invariant bio-markers of risk for RD (e.g., ventral pathway).

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New NIH-funded project (2006-New NIH-funded project (2006-2011; Haskins PO, Pr. 3 Pugh PI)2011; Haskins PO, Pr. 3 Pugh PI)

• 2) Longitudinal tracking (ages 5.5-8.5 and ages 8.5-11.5).

• Comparable data will be acquired over this critical developmental period for children learning to read in very different languages (English, Finnish, Chinese). We seek to understand language invariant factors in typical and atypical reading development.

• Different writing systems result in somewhat different profiles in RD, yet in all RD kids are reading in a non-fluent manner.

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Why study brain?Why study brain?

1) A mediating level of analysis between genes and behavior.

2) Better computational models: neural constraints.

3) A potentially better account of individual differences in either typical or atypical development.

4) A potentially better account of individual differences in response to intervention for at-risk children. What works for whom.

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Adolescent RD learning and Adolescent RD learning and plasticity: Repetition Effectsplasticity: Repetition Effects

• We compared NI and RD readers on the linear effects on words seen 6 times over the course of a scanning run.

• Given the previous tradeoff data we anticipated linear decrease in NI (replicating Katz et al., 2005) but linear increase in RD.

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Implications of NI/RD differences Implications of NI/RD differences on effects of facilitatory variableson effects of facilitatory variables

• 1) The phonologically-tuned subsystem in adolescent RD appears to be poorly trained but not fundamentally disrupted.

• 2) Factors that facilitate performance, such as semantic support or repetition can increase the coherence of processing in this subsystem.

• Ideal training in this population will strengthen phonological coherence and generalize to new items.

1 neuroimaging studies of cognitive development: insights from reading research kenneth r. pugh, phd...

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