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PLOS ONE  2012 

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

DOI: 10.1371/journal.pone.0031877

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Abstract:

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.

References

[1]  Baddeley A (1992) Working memory. Science 255: 556–559.
[2]  Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4: 829–839.
[3]  Cowan N (2008) What are the differences between long-term, short-term, and working memory? Prog Brain Res 169: 323–338.
[4]  Baddeley AD (1986) Working memory. New York: Oxford University Press.
[5]  Baddeley AD, Hitch G (1974) Working memory. In: Bower GH, editor. The psychology of learning and motivation. San Diego: Academic Press. pp. 47–90.
[6]  Baddeley A (1996) The fractionation of working memory. Proc Natl Acad Sci U S A 93: 13468–13472.
[7]  Baddeley A (2003) Working memory and language: an overview. J Commun Disord 36: 189–208.
[8]  Becker JT, MacAndrew DK, Fiez JA (1999) A comment on the functional localization of the phonological storage subsystem of working memory. Brain Cogn 41: 27–38.
[9]  Buchsbaum BR, D'Esposito M (2008) The search for the phonological store: from loop to convolution. J Cogn Neurosci 20: 762–778.
[10]  Paulesu E, Frith CD, Frackowiak RS (1993) The neural correlates of the verbal component of working memory. Nature 362: 342–345.
[11]  Smith EE, Jonides J, Marshuetz C, Koeppe RA (1998) Components of verbal working memory: evidence from neuroimaging. Proc Natl Acad Sci U S A 95: 876–882.
[12]  Chein JM, Fiez JA (2001) Dissociation of verbal working memory system components using a delayed serial recall task. Cereb Cortex 11: 1003–1014.
[13]  Smith EE, Jonides J (1998) Neuroimaging analyses of human working memory. Proc Natl Acad Sci U S A 95: 12061–12068.
[14]  Salmon E, Van der Linden M, Collette F, Delfiore G, Maquet P, et al. (1996) Regional brain activity during working memory tasks. Brain 119: 1617–1625.
[15]  Collette F, Van der Linden M (2002) Brain imaging of the central executive component of working memory. Neurosci Biobehav Rev 26: 105–125.
[16]  Richardson FM, Ramsden S, Ellis C, Burnett S, Megnin O, et al. (2011) Auditory STM capacity correlates with gray matter density in the left posterior STS in cognitively normal and dyslexic. J Cogn Neurosci 23: 3746–3756.
[17]  Wilde NJ, Strauss E, Tulsky DS (2004) Memory span on the Wechsler scales. J Clin Exp Neuropsychol 26: 539–549.
[18]  Wynn RM, Coolidge FL (2009) Does greater phonological storage capacity correlate with levels of intentionality and theory of mind? Psychol Rep 105: 625–632.
[19]  Waters GS, Caplan D (2003) The reliability and stability of verbal working memory measures. Behav Res Methods Instrum Comput 35: 550–564.
[20]  Taki Y, Kinomura S, Sato K, Goto R, Wu K, et al. (2011) Correlation between gray/white matter volume and cognition in healthy elderly people. Brain Cogn 75: 170–176.
[21]  Amici S, Brambati SM, Wilkins DP, Ogar J, Dronkers NL, et al. (2007) Anatomical correlates of sentence comprehension and verbal working memory in neurodegenerative disease. J Neurosci 27: 6282–6290.
[22]  Gili T, Cercignani M, Serra L, Perri R, Giove F, et al. (2011) Regional brain atrophy and functional disconnection across Alzheimer's disease evolution. J Neurol Neurosurg Psychiatry 82: 58–66.
[23]  Liao W, Xu Q, Mantini D, Ding J, Machado-de-Sousa JP, et al. (2011) Altered gray matter morphometry and resting-state functional and structural connectivity in social anxiety disorder. Brain Res 1388: 167–177.
[24]  Lui S, Deng W, Huang X, Jiang L, Ma X, et al. (2009) Association of cerebral deficits with clinical symptoms in antipsychotic-naive first-episode schizophrenia: an optimized voxel-based morphometry and resting state functional connectivity study. Am J Psychiatry 166: 196–205.
[25]  Kesslak JP, Nalcioglu O, Cotman CW (1991) Quantification of magnetic resonance scans for hippocampal and parahippocampal atrophy in Alzheimer's disease. Neurology 41: 51–54.
[26]  Allen G, Barnard H, McColl R, Hester AL, Fields JA, et al. (2007) Reduced hippocampal functional connectivity in Alzheimer disease. Arch Neurol 64: 1482–1487.
[27]  Gong YX (1982) Manual of modified Wechsler Adult Intelligence Scale (WAISRC), Hunan Med College, Changsha, China.
[28]  Oldfield RC (1971) the assessment and analysis of handness: the Edinburgh inventory. Neuropsychologia 9: 97–113.
[29]  Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38: 95–113.
[30]  Vaz IA, Cordeiro PM, Macedo EC, Lukasova K (2010) Working memory in children assessed by the Brown-Peterson Task. Pro Fono 22: 95–100.
[31]  Otero Dadín C, Rodríguez Salgado D, Andrade Fernández E (2009) Natural sex hormone cycles and gender differences in memory. Actas Esp Psiquiatr 37: 68–74.
[32]  Wild-Wall N, Falkenstein M, Gajewski PD (2011) Age-related differences in working memory performance in a 2-back task. Front Psychol 2: 186.
[33]  Diamond A, Lee K (2011) Interventions shown to aid executive function development in children 4 to 12 years old. Science 333: 959–964.
[34]  Fair DA, Cohen AL, Dosenbach NU, Church JA, Miezin FM, et al. (2008) The maturing architecture of the brain's default network. Proc Natl Acad Sci U S A 105: 4028–4032.
[35]  Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, et al. (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103: 13848–13853.
[36]  Stevens MC, Kiehl KA, Pearlson GD, Calhoun VD (2007) Functional neural networks underlying response inhibition in adolescents and adults. Behav Brain Res 181: 12–22.
[37]  Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, et al. (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102: 9673–9678.
[38]  Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A 100: 253–258.
[39]  Lowe MJ, Mock BJ, Sorenson JA (1998) Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7: 119–132.
[40]  Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009) The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage 44: 893–905.
[41]  Weissenbacher A, Kasess C, Gerstl F, Lanzenberger R, Moser E, et al. (2009) Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. Neuroimage 47: 1408–1416.
[42]  Ahveninen J, J??skel?inen IP, Raij T, Bonmassar G, Devore S, et al. (2006) Task-modulated “what” and “where” pathways in human auditory cortex. Proc Natl Acad Sci U S A 103: 14608–14613.
[43]  Alain C, McDonald KL, Kovacevic N, McIntosh AR (2009) Spatiotemporal analysis of auditory “what” and “where” working memory. Cereb Cortex 19: 305–14.
[44]  Zatorre RJ, Belin P (2001) Spectral and temporal processing in human auditory cortex. Cereb Cortex 11: 946–953.
[45]  Jamison HL, Watkins KE, Bishop DV, Matthews PM (2006) Hemispheric specialization for processing auditory nonspeech stimuli. Cereb Cortex 16: 1266–1275.
[46]  Petit L, Simon G, Joliot M, Andersson F, Bertin T, et al. (2007) Right hemisphere dominance for auditory attention and its modulation by eye position: an event related fMRI study. Restor Neurol Neurosci 25: 211–225.
[47]  Lattner S, Meyer ME, Friederici AD (2005) Voice perception: Sex, pitch, and the right hemisphere. Hum Brain Mapp 24: 11–20.
[48]  van Ettinger-Veenstra HM, Ragnehed M, H?llgren M, Karlsson T, Landtblom AM, et al. (2010) Right-hemispheric brain activation correlates to language performance. Neuroimage 49: 3481–3488.
[49]  Yeatman JD, Ben-Shachar M, Glover GH, Feldman HM (2010) Individual differences in auditory sentence comprehension in children: An exploratory event-related functional magnetic resonance imaging investigation. Brain Lang 114: 72–79.
[50]  Lidzba K, Schwilling E, Grodd W, Kr?geloh-Mann I, Wilke M (2011) Language comprehension vs. language production: Age effects on fMRI activation. Brain Lang 119: 6–15.
[51]  Crinion JT, Green DW, Chung R, Ali N, Grogan A, et al. (2009) Neuroanatomical markers of speaking Chinese. Hum Brain Mapp 30: 4108–4115.
[52]  Crinion J, Price CJ (2005) Right anterior superior temporal activation predicts auditory sentence comprehension following aphasic stroke. Brain 128: 2858–2871.
[53]  Warren JE, Crinion JT, Lambon Ralph MA, Wise RJ (2009) Anterior temporal lobe connectivity correlates with functional outcome after aphasic stroke. Brain 132: 3428–3442.
[54]  Turkeltaub PE, Coslett HB (2010) Localization of sublexical speech perception components. Brain Lang 114: 1–15.
[55]  Peeva MG, Guenther FH, Tourville JA, Nieto-Castanon A, Anton JL, et al. (2010) Distinct representations of phonemes, syllables, and supra-syllabic sequences in the speech production network. Neuroimage 50: 626–638.
[56]  Graves WW, Grabowski TJ, Mehta S, Gupta P (2008) The left posterior superior temporal gyrus participates specifically in accessing lexical phonology. J Cogn Neurosci 20: 1698–1710.
[57]  Burton MW, Locasto PC, Krebs-Noble D, Gullapalli RP (2005) A systematic investigation of the functional neuroanatomy of auditory and visual phonological processing. Neuroimage 26: 647–661.
[58]  Heim S, Friederici AD (2003) Phonological processing in language production: time course of brain activity. Neuroreport 14: 2031–2033.
[59]  Leff AP, Schofield TM, Crinion JT, Seghier ML, Grogan A, et al. (2009) The left superior temporal gyrus is a shared substrate for auditory short-term memory and peech comprehension: evidence from 210 patients with stroke. Brain 132: 3401–3410.
[60]  Specht K, Reul J (2003) Functional segregation of the temporal lobes into highly differentiated subsystems for auditory perception: an auditory rapid event-related fMRI-task. Neuroimage 20: 1944–1954.
[61]  Boemio A, Fromm S, Braun A, Poeppel D (2005) Hierarchical and asymmetric temporal sensitivity in human auditory cortices. Nat Neurosci 8: 389–395.
[62]  Rothmayr C, Baumann O, Endestad T, Rutschmann RM, Magnussen S, et al. (2007) Dissociation of neural correlates of verbal and non-verbal visual working memory with different delays. Behav Brain Funct 3: 56.
[63]  Gerton BK, Brown TT, Meyer-Lindenberg A, Kohn P, Holt JL, et al. (2004) Shared and distinct neurophysiological components of the digits forward and backward tasks as revealed by functional neuroimaging. Neuropsychologia 42: 1781–1787.
[64]  Veroude K, Norris DG, Shumskaya E, Gullberg M, Indefrey P (2010) Functional connectivity between brain regions involved in learning words of a new language. Brain Lang 113: 21–27.
[65]  Tonkonogy J, Goodglass H (1981) Language function, foot of the third frontal gyrus, and rolandic operculum. Arch Neurol 38: 486–490.
[66]  Chang SE, Erickson KI, Ambrose NG, Hasegawa-Johnson MA, Ludlow CL (2008) Brain anatomy differences in childhood stuttering. NeuroImage 39: 1333–1344.
[67]  Watkins KE, Smith SM, Davis S, Howell P (2008) Structural and functional abnormalities of the motor system in developmental stuttering. Brain 131: 50–59.
[68]  Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Rev 22: 229–244.
[69]  Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3: 655–666.
[70]  Craig AD (2009) How do you feel—now? The anterior insula and human awareness. Nat Rev Neurosci 10: 59–70.
[71]  Cauda F, D'Agata F, Sacco K, Duca S, Geminiani G, et al. (2011) Functional connectivity of the insula in the resting brain. Neuroimage 55: 8–23.
[72]  Deen B, Pitskel NB, Pelphrey KA (2011) Three systems of insular functional connectivity identified with cluster analysis. Cereb Cortex 21: 1498–1506.
[73]  Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, et al. (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27: 2349–2356.
[74]  Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214: 655–667.
[75]  Menon V, Adleman NE, White CD, Glover GH, Reiss AL (2001) Error-related brain activation during a Go/NoGo response inhibition task. Hum Brain Mapp 12: 131–143.
[76]  Curtis CE, D'Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7: 415–423.
[77]  Kerns JG, Cohen JD, MacDonald AW 3rd, Cho RY, Stenger VA, et al. (2004) Anterior cingulate conflict monitoring and adjustments in control. Science 303: 1023–1026.
[78]  Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004) The role of the medial frontal cortex in cognitive control. Science 306: 443–447.
[79]  Peyron R, Laurent B, García-Larrea L (2000) Functional imaging of brain responses to pain. A review and meta-analysis. Neurophysiol Clin 30: 263–288.
[80]  Grinband J, Hirsch J, Ferrera VP (2006) A neural representation of categorization uncertainty in the human brain. Neuron 49: 757–763.
[81]  Nimchinsky EA, Gilissen E, Allman JM, Perl DP, Erwin JM, et al. (1999) A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci U S A 96: 5268–5273.
[82]  Allman JM, Watson KK, Tetreault NA, Hakeem AY (2005) Intuition and autism: a possible role for Von Economo neurons. Trends Cogn Sci 9: 367–373.
[83]  Sridharan D, Levitin DJ, Menon V (2008) A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci U S A 105: 12569–12574.
[84]  Smith EE, Jonides J (1999) Storage and executive processes in the frontal lobes. Science 283: 1657–1661.
[85]  Crottaz-Herbette S, Menon V (2006) Where and When the Anterior Cingulate Cortex Modulates Attentional Response: Combined fMRI and ERP Evidence. J Cogn Neurosci 18: 766–780.
[86]  Luo Q, Mitchell D, Jones M, Mondillo K, Vythilingam M, et al. (2007) Common regions of dorsal anterior cingulate and prefrontal-parietal cortices provide attentional control of distracters varying in emotionality and visibility. Neuroimage 38: 631–639.
[87]  Botvinick MM, Cohen JD, Carter CS (2004) Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn Sci 8: 539–546.
[88]  Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, et al. (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280: 747–749.
[89]  Carter CS, van Veen V (2007) Anterior cingulate cortex and conflict detection: an update of theory and data. Cogn Affect Behav Neurosci 7: 367–379.
[90]  Gehring WJ, Knight RT (2000) Prefrontal–cingulate interactions in action monitoring. Nat Neurosci 3: 516–520.
[91]  Gehring WJ, Fencsik DE (2001) Functions of the medial frontal cortex in the processing of conflict and errors. J Neurosci 21: 9430–9437.
[92]  Pourtois G, Vocat R, N'Diaye K, Spinelli L, Seeck M, et al. (2010) Errors recruit both cognitive and emotional monitoring systems: simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI. Neuropsychologia 48: 1144–1159.
[93]  Lorist MM, Boksem MA, Ridderinkhof KR (2005) Impaired cognitive control and reduced cingulate activity during mental fatigue. Brain Res Cogn Brain Res 24: 199–205.
[94]  Awh E, Gehring WJ (1999) The anterior cingulate cortex lends a hand in response selection. Nat Neurosci 2: 853–854.
[95]  Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2: 417–424.
[96]  Lenartowicz A, McIntosh AR (2005) The role of anterior cingulate cortex in working memory is shaped by functional connectivity. J Cogn Neurosci 17: 1026–1042.
[97]  Osaka M, Osaka N, Kondo H, Morishita M, Fukuyama H, et al. (2003) The neural basis of individual differences in working memory capacity: an fMRI study. Neuroimage 18: 789–797.
[98]  Kondo H, Morishita M, Osaka N, Osaka M, Fukuyama H, et al. (2004) Functional roles of the cingulo-frontal network in performance on working memory. Neuroimage 21: 2–14.
[99]  Zhou J, Greicius MD, Gennatas ED, Growdon ME, Jang JY, et al. (2010) Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 133: 1352–1367.
[100]  Seeley WW (2010) Anterior insula degeneration in frontotemporal dementia. Brain Struct Funct 214: 465–475.
[101]  Daniels JK, McFarlane AC, Bluhm RL, Moores KA, Clark CR, et al. (2010) Switching between executive and default mode networks in posttraumatic stress disorder: alterations in functional connectivity. J Psychiatry Neurosci 35: 258–266.
[102]  Veer IM, Beckmann CF, van Tol MJ, Ferrarini L, Milles J, et al. (2010) Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Front Syst Neurosci 4: 41.
[103]  Tian LX, Jiang TZ, Liu Y, Yu CS, Wang K, et al. (2007) The relationship within and between the extrinsic and intrinsic systems indicated by resting state correlational patterns of sensory cortices. Neuroimage 36: 684–690.
[104]  Zhou Y, Yu C, Zheng H, Liu Y, Song M, et al. (2010) Increased neural resources recruitment in the intrinsic organization in major depression. J Affect Disord 121: 220–230.
[105]  Grube O, Muller T, Falkai P (2007) Dynamic interactions between neural systems underlying different components of verbal working memory. J Neural Transm 114: 1047–1050.
[106]  Hampson M, Driesen N, Roth JK, Gore JC, Constable RT (2010) Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. Magn Reson Imaging 28: 1051–1057.
[107]  Hoshi Y, Oda I, Wada Y, Ito Y, Yutaka Yamashita, et al. (2000) Visuospatial imagery is a fruitful strategy for the digit span backward task: a study with near-infrared optical tomography. Brain Res Cogn Brain Res 9: 339–342.
[108]  Sun X, Zhang X, Chen X, Zhang P, Bao M, et al. (2005) Age-dependent brain activation during forward and backward digit recall revealed by fMRI. Neuroimage 26: 36–47.
[109]  Hale TS, Bookheimer S, McGough JJ, Phillips JM, McCracken JT (2007) Atypical brain activation during simple and complex levels of processing in adult ADHD: an fMRI study. J Atten Disord 11: 125–140.

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