The Neuronal Correlates of Digits Backward Are Revealed by Voxel-Based Morphometry and Resting-State Functional Connectivity Analyses

Digits backward (DB) is a widely used neuropsychological measure that is believed to be a simple and effective index of the capacity of the verbal working memory. However, its neural correlates remain elusive. The aim of this study is to investigate the neural correlates of DB in 299 healthy young adults by combining voxel-based morphometry (VBM) and resting-state functional connectivity (rsFC) analyses. The VBM analysis showed positive correlations between the DB scores and the gray matter volumes in the right anterior superior temporal gyrus (STG), the right posterior STG, the left inferior frontal gyrus and the left Rolandic operculum, which are four critical areas in the auditory phonological loop of the verbal working memory. Voxel-based correlation analysis was then performed between the positive rsFCs of these four clusters and the DB scores. We found that the DB scores were positively correlated with the rsFCs within the salience network (SN), that is, between the right anterior STG, the dorsal anterior cingulate cortex and the right fronto-insular cortex. We also found that the DB scores were negatively correlated with the rsFC within an anti-correlation network of the SN, between the right posterior STG and the left posterior insula. Our findings suggest that DB performance is related to the structural and functional organizations of the brain areas that are involved in the auditory phonological loop and the SN.

[1]  Fiona M. Richardson,et al.  Auditory STM Capacity Correlates with Gray Matter Density in the Left Posterior STS in Cognitively Normal and Dyslexic Adults. , 2011 .

[2]  Caroline Catmur,et al.  Auditory Short-term Memory Capacity Correlates with Gray Matter Density in the Left Posterior STS in Cognitively Normal and Dyslexic Adults , 2011, Journal of Cognitive Neuroscience.

[3]  W. Grodd,et al.  Language comprehension vs. language production: Age effects on fMRI activation , 2011, Brain and Language.

[4]  A. Diamond,et al.  Interventions Shown to Aid Executive Function Development in Children 4 to 12 Years Old , 2011, Science.

[5]  Michael Falkenstein,et al.  Age-Related Differences in Working Memory Performance in A 2-Back Task , 2011, Front. Psychology.

[6]  Huafu Chen,et al.  Altered gray matter morphometry and resting-state functional and structural connectivity in social anxiety disorder , 2011, Brain Research.

[7]  S. Kinomura,et al.  Correlation between gray/white matter volume and cognition in healthy elderly people , 2011, Brain and Cognition.

[8]  Katiuscia Sacco,et al.  Functional connectivity of the insula in the resting brain , 2011, NeuroImage.

[9]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[10]  Michelle Hampson,et al.  Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. , 2010, Magnetic resonance imaging.

[11]  G. Glover,et al.  Individual differences in auditory sentence comprehension in children: An exploratory event-related functional magnetic resonance imaging investigation , 2010, Brain and Language.

[12]  C. Caltagirone,et al.  Regional brain atrophy and functional disconnection across Alzheimer's disease evolution , 2010, Journal of Neurology, Neurosurgery & Psychiatry.

[13]  H. Coslett,et al.  Localization of sublexical speech perception components , 2010, Brain and Language.

[14]  Marnie E. Shaw,et al.  Switching between executive and default mode networks in posttraumatic stress disorder: alterations in functional connectivity. , 2010, Journal of psychiatry & neuroscience : JPN.

[15]  S. Rombouts,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[16]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[17]  William W. Seeley,et al.  Anterior insula degeneration in frontotemporal dementia , 2010, Brain Structure and Function.

[18]  Martin Lepage,et al.  Medial prefrontal cortex activity during memory encoding of pictures and its relation to symptomatic improvement after citalopram treatment in patients with major depression. , 2010, Journal of psychiatry & neuroscience : JPN.

[19]  Efstathios D. Gennatas,et al.  Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. , 2010, Brain : a journal of neurology.

[20]  Working memory in children assessed by the Brown-Peterson Task. , 2010, Pro-fono : revista de atualizacao cientifica.

[21]  David G. Norris,et al.  Functional connectivity between brain regions involved in learning words of a new language , 2010, Brain and Language.

[22]  Chunshui Yu,et al.  Increased neural resources recruitment in the intrinsic organization in major depression. , 2010, Journal of affective disorders.

[23]  Gilles Pourtois,et al.  Errors recruit both cognitive and emotional monitoring systems: Simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI , 2010, Neuropsychologia.

[24]  Maria Engström,et al.  Right-hemispheric brain activation correlates to language performance , 2010, NeuroImage.

[25]  Francois-Xavier Alario,et al.  Distinct representations of phonemes, syllables, and supra-syllabic sequences in the speech production network , 2009, NeuroImage.

[26]  Jennifer T. Crinion,et al.  Anterior temporal lobe connectivity correlates with functional outcome after aphasic stroke , 2009, Brain : a journal of neurology.

[27]  M. Seghier,et al.  The left superior temporal gyrus is a shared substrate for auditory short-term memory and speech comprehension: evidence from 210 patients with stroke , 2009, Brain : a journal of neurology.

[28]  Frederick L Coolidge,et al.  Does Greater Phonological Storage Capacity Correlate with Levels of Intentionality and Theory of Mind? , 2009, Psychological reports.

[29]  Rupert Lanzenberger,et al.  Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies , 2009, NeuroImage.

[30]  Cathy J. Price,et al.  Neuroanatomical markers of speaking Chinese , 2009, Human brain mapping.

[31]  D. Collier,et al.  Association of cerebral deficits with clinical symptoms in antipsychotic-naive first-episode schizophrenia: an optimized voxel-based morphometry and resting state functional connectivity study. , 2009, The American journal of psychiatry.

[32]  Natasa Kovacevic,et al.  Spatiotemporal analysis of auditory "what" and "where" working memory. , 2009, Cerebral cortex.

[33]  Kevin Murphy,et al.  The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? , 2009, NeuroImage.

[34]  D. Rodríguez Salgado,et al.  Natural sex hormone cycles and gender differences in memory. , 2009, Actas espanolas de psiquiatria.

[35]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[36]  Thomas J. Grabowski,et al.  The Left Posterior Superior Temporal Gyrus Participates Specifically in Accessing Lexical Phonology , 2008, Journal of Cognitive Neuroscience.

[37]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[38]  Bradley R. Buchsbaum,et al.  The Search for the Phonological Store: From Loop to Convolution , 2008, Journal of Cognitive Neuroscience.

[39]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[40]  Mark A. Hasegawa-Johnson,et al.  Brain anatomy differences in childhood stuttering , 2008, NeuroImage.

[41]  K. Watkins,et al.  Structural and functional abnormalities of the motor system in developmental stuttering. , 2007, Brain : a journal of neurology.

[42]  M. D’Esposito Working memory. , 2008, Handbook of clinical neurology.

[43]  N. Cowan What are the differences between long-term, short-term, and working memory? , 2008, Progress in brain research.

[44]  C. Carter,et al.  Anterior cingulate cortex and conflict detection: An update of theory and data , 2007, Cognitive, affective & behavioral neuroscience.

[45]  Derek G. V. Mitchell,et al.  Common regions of dorsal anterior cingulate and prefrontal–parietal cortices provide attentional control of distracters varying in emotionality and visibility , 2007, NeuroImage.

[46]  M. Greenlee,et al.  Behavioral and Brain Functions , 2007 .

[47]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[48]  M. Weiner,et al.  Reduced hippocampal functional connectivity in Alzheimer disease. , 2007, Archives of neurology.

[49]  Vince D. Calhoun,et al.  Functional neural networks underlying response inhibition in adolescents and adults , 2007, Behavioural Brain Research.

[50]  Yuan Zhou,et al.  The relationship within and between the extrinsic and intrinsic systems indicated by resting state correlational patterns of sensory cortices , 2007, NeuroImage.

[51]  Bruce L. Miller,et al.  Anatomical Correlates of Sentence Comprehension and Verbal Working Memory in Neurodegenerative Disease , 2007, The Journal of Neuroscience.

[52]  James T. McCracken,et al.  Atypical Brain Activation During Simple & Complex Levels of Processing in Adult ADHD , 2007, Journal of attention disorders.

[53]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[54]  Peter Falkai,et al.  Dynamic interactions between neural systems underlying different components of verbal working memory , 2007, Journal of Neural Transmission.

[55]  L. Zago,et al.  Right hemisphere dominance for auditory attention and its modulation by eye position: an event related fMRI study. , 2007, Restorative neurology and neuroscience.

[56]  B. Shinn-Cunningham,et al.  Task-modulated “what” and “where” pathways in human auditory cortex , 2006, Proceedings of the National Academy of Sciences.

[57]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[58]  Helen L Jamison,et al.  Hemispheric specialization for processing auditory nonspeech stimuli. , 2006, Cerebral cortex.

[59]  Vinod Menon,et al.  Where and When the Anterior Cingulate Cortex Modulates Attentional Response: Combined fMRI and ERP Evidence , 2006, Journal of Cognitive Neuroscience.

[60]  J. Hirsch,et al.  A Neural Representation of Categorization Uncertainty in the Human Brain , 2006, Neuron.

[61]  C. Price,et al.  Right anterior superior temporal activation predicts auditory sentence comprehension following aphasic stroke. , 2005, Brain : a journal of neurology.

[62]  J. Allman,et al.  Intuition and autism: a possible role for Von Economo neurons , 2005, Trends in Cognitive Sciences.

[63]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Anthony Randal McIntosh,et al.  The Role of Anterior Cingulate Cortex in Working Memory is Shaped by Functional Connectivity , 2005, Journal of Cognitive Neuroscience.

[65]  Paul C. Locasto,et al.  A systematic investigation of the functional neuroanatomy of auditory and visual phonological processing , 2005, NeuroImage.

[66]  K. R. Ridderinkhof,et al.  Impaired cognitive control and reduced cingulate activity during mental fatigue. , 2005, Brain research. Cognitive brain research.

[67]  Xiwen Sun,et al.  Age-dependent brain activation during forward and backward digit recall revealed by fMRI , 2005, NeuroImage.

[68]  A. Boemio,et al.  Hierarchical and asymmetric temporal sensitivity in human auditory cortices , 2005, Nature Neuroscience.

[69]  Angela D Friederici,et al.  � Human Brain Mapping 24:11–20(2005) � Voice Perception: Sex, Pitch, and the Right Hemisphere , 2022 .

[70]  Andreas Meyer-Lindenberg,et al.  Shared and distinct neurophysiological components of the digits forward and backward tasks as revealed by functional neuroimaging , 2004, Neuropsychologia.

[71]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[72]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[73]  D. Tulsky,et al.  Memory Span on the Wechsler Scales , 2004, Journal of clinical and experimental neuropsychology.

[74]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[75]  Hidenao Fukuyama,et al.  Functional roles of the cingulo-frontal network in performance on working memory , 2004, NeuroImage.

[76]  Karsten Specht,et al.  Functional segregation of the temporal lobes into highly differentiated subsystems for auditory perception: an auditory rapid event-related fMRI-task , 2003, NeuroImage.

[77]  A. Friederici,et al.  Phonological processing in language production: time course of brain activity , 2003, Neuroreport.

[78]  G. Waters,et al.  The reliability and stability of verbal working memory measures , 2003, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[79]  A. Baddeley Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[80]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[81]  A. Baddeley Working memory and language: an overview. , 2003, Journal of communication disorders.

[82]  Hidenao Fukuyama,et al.  The neural basis of individual differences in working memory capacity: an fMRI study , 2003, NeuroImage.

[83]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[84]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[85]  F. Collette,et al.  Brain imaging of the central executive component of working memory , 2002, Neuroscience & Biobehavioral Reviews.

[86]  W. Gehring,et al.  Functions of the Medial Frontal Cortex in the Processing of Conflict and Errors , 2001, The Journal of Neuroscience.

[87]  J. Fiez,et al.  Functional Magnetic Resonance Imaging (fmri) Was Used to Investigate the Neural Substrates of Component Processes in Verbal Working Memory. Based on Behavioral Research Using , 2022 .

[88]  R. Zatorre,et al.  Spectral and temporal processing in human auditory cortex. , 2001, Cerebral cortex.

[89]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[90]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[91]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[92]  Y Hoshi,et al.  Visuospatial imagery is a fruitful strategy for the digit span backward task: a study with near-infrared optical tomography. , 2000, Brain research. Cognitive brain research.

[93]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

[94]  J. Fiez,et al.  A Comment on the Functional Localization of the Phonological Storage Subsystem of Working Memory , 1999, Brain and Cognition.

[95]  Edward Awh,et al.  The anterior cingulate cortex lends a hand in response selection , 1999, Nature Neuroscience.

[96]  J. Allman,et al.  A neuronal morphologic type unique to humans and great apes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[97]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[98]  J. Jonides,et al.  Neuroimaging analyses of human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[99]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[100]  E E Smith,et al.  Components of verbal working memory: evidence from neuroimaging. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[101]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[102]  A Baddeley,et al.  The fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[103]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[104]  C. Degueldre,et al.  Regional brain activity during working memory tasks. , 1996, Brain : a journal of neurology.

[105]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[106]  O Nalcioglu,et al.  Quantification of magnetic resonance scans for hippocampal and parahippocampal atrophy in Alzheimer's disease , 1991, Neurology.

[107]  H Goodglass,et al.  Language function, foot of the third frontal gyrus, and rolandic operculum. , 1981, Archives of neurology.

[108]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.