Regional amplitude of the low-frequency fluctuations at rest predicts word-reading skill

Individuals' reading skills are critical for their educational development, but variation in reading skills is known to be large. The present study used functional magnetic resonance imaging (fMRI) to examine the role of spontaneous brain activity at rest in individual differences in reading skills in a large sample of participants (N=263). Specifically, we correlated individuals' word-reading skill with their fractional amplitude of low-frequency fluctuation (fALFF) of the whole brain at rest and found that the fALFFs of both the bilateral precentral gyrus (PCG) and superior temporal plane (STP) were positively associated with reading skills. The fALFF-reading association observed in these two regions remained after controlling for general cognitive abilities and in-scanner head motion. A cross-validation confirmed that the individual differences in word-reading skills were reliably correlated with the fALFF values of the bilateral PCG and STP. A follow-up task-based fMRI experiment revealed that the reading-related regions overlapped with regions showing a higher response to sentences than to pseudo-sentences (strings of pseudo-words), suggesting the resting-state brain activity partly captures the characteristics of task-based brain activity. In short, our study provides one of the first pieces of evidence that links spontaneous brain activity to reading behavior and offers an easy-to-access neural marker for evaluating reading skill.

[1]  A. Caramazza,et al.  Predicting Conceptual Processing Capacity from Spontaneous Neuronal Activity of the Left Middle Temporal Gyrus , 2012, The Journal of Neuroscience.

[2]  K. James,et al.  When writing impairs reading: letter perception's susceptibility to motor interference. , 2009, Journal of experimental psychology. General.

[3]  R. Wagner,et al.  The nature of phonological processing and its causal role in the acquisition of reading skills. , 1987 .

[4]  K. Pugh,et al.  The relationship between phonological and auditory processing and brain organization in beginning readers , 2013, Brain and Language.

[5]  Nancy Kanwisher,et al.  Functional specificity for high-level linguistic processing in the human brain , 2011, Proceedings of the National Academy of Sciences.

[6]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[7]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[8]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[9]  N. Kanwisher,et al.  New method for fMRI investigations of language: defining ROIs functionally in individual subjects. , 2010, Journal of neurophysiology.

[10]  P. Matthews,et al.  Testing for Dual Brain Processing Routes in Reading: A Direct Contrast of Chinese Character and Pinyin Reading Using fMRI , 2002, Journal of Cognitive Neuroscience.

[11]  Brian A. Wandell,et al.  The Development of Cortical Sensitivity to Visual Word Forms , 2011, Journal of Cognitive Neuroscience.

[12]  T. Conway,et al.  Preventing reading failure in young children with phonological processing disabilities: Group and individual responses to instruction. , 1999 .

[13]  Chaozhe Zhu,et al.  An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: Fractional ALFF , 2008, Journal of Neuroscience Methods.

[14]  Guinevere F. Eden,et al.  An Investigation into the Origin of Anatomical Differences in Dyslexia , 2014, The Journal of Neuroscience.

[15]  A. Song,et al.  Linking Sight and Sound: fMRI Evidence of Primary Auditory Cortex Activation during Visual Word Recognition , 2001, Brain and Language.

[16]  Yufeng Zang,et al.  Individual Differences in Impulsivity Predict Head Motion during Magnetic Resonance Imaging , 2014, PloS one.

[17]  M Coltheart,et al.  DRC: a dual route cascaded model of visual word recognition and reading aloud. , 2001, Psychological review.

[18]  Ying Han,et al.  Frequency-dependent changes in the amplitude of low-frequency fluctuations in amnestic mild cognitive impairment: A resting-state fMRI study , 2011, NeuroImage.

[19]  Christine L. Cox,et al.  The balance between feeling and knowing: affective and cognitive empathy are reflected in the brain's intrinsic functional dynamics. , 2012, Social cognitive and affective neuroscience.

[20]  R. Saxe,et al.  Language processing in the occipital cortex of congenitally blind adults , 2011, Proceedings of the National Academy of Sciences.

[21]  J. Raven,et al.  Manual for Raven's progressive matrices and vocabulary scales , 1962 .

[22]  N. Tzourio-Mazoyer,et al.  The weight of skill: Interindividual variability of reading related brain activation patterns in fluent readers , 2011, Journal of Neurolinguistics.

[23]  Y. Zang,et al.  Intrinsic resting‐state activity predicts working memory brain activation and behavioral performance , 2013, Human brain mapping.

[24]  B. Shaywitz,et al.  Paying attention to reading: The neurobiology of reading and dyslexia , 2008, Development and Psychopathology.

[25]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[26]  D. Hu,et al.  Neurobiological basis of head motion in brain imaging , 2014, Proceedings of the National Academy of Sciences.

[27]  Tim Fosker,et al.  Language-universal Sensory Deficits in Developmental Dyslexia: English, Spanish, and Chinese , 2011, Journal of Cognitive Neuroscience.

[28]  Russell A. Poldrack,et al.  Decoding Developmental Differences and Individual Variability in Response Inhibition Through Predictive Analyses Across Individuals , 2010, Front. Hum. Neurosci..

[29]  D. Geldmacher,et al.  The effect of character and array type on visual spatial search quality following traumatic brain injury. , 1998, Brain injury.

[30]  M. Raichle.  Two views of brain function , 2010, Trends in Cognitive Sciences.

[31]  Karin Humphreys,et al.  The psychology of language : from data to theory , 2001 .

[32]  Bharat B. Biswal,et al.  The oscillating brain: Complex and reliable , 2010, NeuroImage.

[33]  G Jobard,et al.  Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies , 2003, NeuroImage.

[34]  Frederick Mosteller,et al.  Understanding robust and exploratory data analysis , 1983 .

[35]  Monica Melby-Lervåg,et al.  Phonological skills and their role in learning to read: a meta-analytic review. , 2012, Psychological bulletin.

[36]  Bharat B. Biswal,et al.  Inter-individual differences in resting-state functional connectivity predict task-induced BOLD activity , 2010, NeuroImage.

[37]  Xu Wang,et al.  Neural correlates of the happy life: The amplitude of spontaneous low frequency fluctuations predicts subjective well-being , 2015, NeuroImage.

[38]  Esther Adi-Japha,et al.  Research in Developmental Disabilities Delayed motor skill acquisition in kindergarten children with language impairment , 2011 .

[39]  Bernard Mazoyer,et al.  What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis , 2011, NeuroImage.

[40]  Lindsey E. Richland,et al.  Early Executive Function Predicts Reasoning Development , 2013, Psychological science.

[41]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[42]  R. Goebel,et al.  Deviant processing of letters and speech sounds as proximate cause of reading failure: a functional magnetic resonance imaging study of dyslexic children. , 2010, Brain : a journal of neurology.

[43]  Karl J. Friston,et al.  The Effects of Presentation Rate During Word and Pseudoword Reading: A Comparison of PET and fMRI , 2000, Journal of Cognitive Neuroscience.

[44]  M. Raichle.  The Brain's Dark Energy , 2006, Science.

[45]  L. Fuchs,et al.  Neural predictors of individual differences in response to math tutoring in primary-grade school children , 2013, Proceedings of the National Academy of Sciences.

[46]  F. Ramus,et al.  Phonological deficits in specific language impairment and developmental dyslexia: towards a multidimensional model , 2013, Brain : a journal of neurology.

[47]  Feng Liu,et al.  Abnormal amplitude low-frequency oscillations in medication-naive, first-episode patients with major depressive disorder: a resting-state fMRI study. , 2013, Journal of affective disorders.

[48]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[49]  Jörg Lewald,et al.  The effect of brain lesions on sound localization in complex acoustic environments. , 2014, Brain : a journal of neurology.

[50]  Alfonso Caramazza,et al.  Where color rests: Spontaneous brain activity of bilateral fusiform and lingual regions predicts object color knowledge performance , 2013, NeuroImage.

[51]  Brian A Wandell,et al.  Learning to see words. , 2012, Annual review of psychology.

[52]  Hua Shu,et al.  Orthographic facilitation in Chinese spoken word recognition: An ERP study , 2012, Brain and Language.

[53]  Kenneth Hugdahl,et al.  The Right Planum Temporale Is Involved in Stimulus-Driven, Auditory Attention – Evidence from Transcranial Magnetic Stimulation , 2013, PloS one.

[54]  M. Roth,et al.  Premotor activations in response to visually presented single letters depend on the hand used to write: a study on left-handers , 2005, Neuropsychologia.

[55]  H. Wimmer,et al.  Functional abnormalities in the dyslexic brain: A quantitative meta‐analysis of neuroimaging studies , 2009, Human brain mapping.

[56]  David C. Geary,et al.  Hippocampal-neocortical functional reorganization underlies children's cognitive development , 2014, Nature Neuroscience.

[57]  R. Hari,et al.  What differs in visual recognition of handwritten vs. printed letters? An fMRI study , 2011, Human brain mapping.

[58]  Xiao Liu,et al.  Baseline BOLD correlation predicts individuals' stimulus-evoked BOLD responses , 2011, NeuroImage.

[59]  Siyuan Hu,et al.  Different neural pathways linking personality traits and eudaimonic well-being: a resting-state functional magnetic resonance imaging study , 2015, Cognitive, affective & behavioral neuroscience.

[60]  Xi-Nian Zuo,et al.  Amplitude of low-frequency oscillations in schizophrenia: A resting state fMRI study , 2010, Schizophrenia Research.

[61]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[62]  Jeffrey M. Zacks,et al.  Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses , 2006, Nature Neuroscience.

[63]  U. Goswami,et al.  Rhythmic processing in children with developmental dyslexia: Auditory and motor rhythms link to reading and spelling , 2008, Journal of Physiology-Paris.

[64]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[65]  A. Friederici.  The brain basis of language processing: from structure to function. , 2011, Physiological reviews.

[66]  Yufeng Zang,et al.  Linking inter-individual differences in neural activation and behavior to intrinsic brain dynamics , 2011, NeuroImage.