The neural correlates of the verbal component of working memory
Abstract
By repeating words 'in our head', verbal material (such as telephone numbers) can be kept in working memory almost indefinitely. This 'articulatory loop' includes a subvocal rehearsal system and a phonological store. Little is known about neural correlates of this model of verbal short-term memory. We therefore measured regional cerebral blood flow, an index of neuronal activity, in volunteers performing a task engaging both components of the articulatory loop (short-term memory for letters) and a task which engages only the subvocal rehearsal system (rhyming judgement for letters). Stimuli were presented visually and the subjects did not speak. We report here that comparisons of distribution of cerebral blood flow in these conditions localized the phonological store to the left supramarginal gyrus whereas the subvocal rehearsal system was associated with Broca's area. This is, to our knowledge, the first demonstration of the normal anatomy of the components of the 'articulatory loop'.
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During silent articulation and verbal working memory, activation in the left posterior inferior frontal gyrus (Broca's area, BA 44) and/or left premotor cortex (BA 6) is associated with inner speech.
“During silent articulation (McGuire et al., 1996a,b) and verbal working memory (Paulesu et al., 1993; Fiez et al., 1996b; Salmon et al., 1996; Schumacher et al., 1996), activation in the left posterior inferior frontal gyrus (Broca's area, BA 44) and/or left premotor cortex (BA 6) was associated with “inner speech”.”
From A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading (2012) · cites this paper as Paulesu et al., 1993
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The fractionation of working memory
Baddeley, A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13468 · Cited by 709 · see citing works
Who Did What and When? Using Word- and Clause-Level ERPs to Monitor Working Memory Usage in Reading
King, J. W., & Marta Kutas, A. (1995) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1995.7.3.376 · Cited by 681 · see citing works
Functional connectivity in the human language system: a cortico-cortical evoked potential study
Matsumoto, R., Nair, D. R., LaPresto, E., Najm, I., Bingaman, W. E., Shibasaki, H., & Lüders, H. O. (2004) · Brain · doi:10.1093/brain/awh246 · Cited by 677 · see citing works
“This connection may play an important role in phonological processing, as revealed in neuroimaging studies which showed activation of SMG in phonological storage and of Broca’s area in subvocal rehearsal or phonological segmentation (Zatorre et al., 1992, 1996; Paulesu et al., 1993).”
Functional and Anatomical Aspects of Prefrontal Pathology in Schizophrenia
Goldman-Rakic, P. S., & Selemon, L. D. (1997) · Schizophrenia Bulletin · doi:10.1093/schbul/23.3.437 · Cited by 668 · see citing works
“…et al. 1996; Courtney et al. 19%; McCarthy et al. 1996), and semantic encoding and retrieval as well as other verbal processes engage still more inferior, insular, and anterior prefrontal regions (Paulesu et al. 1993; Raichle et al. 1994; Demb et al. 1995; Fiez et al. 1996; Price et al. 1996).”
BackgroundDistributed Neural Systems Underlying the Timing of Movements
Rao, S. M., Harrington, D. L., Haaland, K. Y., Bobholz, J. A., Cox, R. W., & Binder, J. R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05528.1997 · Cited by 665 · see citing works
“which the silent rehearsal of letter strings produced bilateral activation of the STG and IFG (Paulesu et al., 1993).”
BackgroundResultThe neurological basis of developmental dyslexia: An overview and working hypothesis
Habib, M. (2000) · Brain · doi:10.1093/brain/123.12.2373 · Cited by 655 · see citing works
“These authors used the same experimental paradigm as in a previous study (Paulesu et al., 1993) comparing a rhyming and a memory condition.”
MethodChafee, M. V., & Goldman, P. S. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.6.2919 · Cited by 655 · see citing works
DTI Tractography of the Human Brain's Language Pathways
Glasser, M. F., & Rilling, J. K. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn011 · Cited by 654 · see citing works
Distinct Brain Systems for Processing Concrete and Abstract Concepts
Binder, J. R., Westbury, C. F., McKiernan, K. A., Possing, E. T., & Medler, D. A. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/0898929054021102 · Cited by 643 · see citing works
“These regions have been strongly linked with phonological processes, verbal short-term memory, and lexical retrieval (Fiez, Balota, Raichle, & Petersen, 1999; Warburton et al., 1996; Paulesu, Frith, & Frackowiak, 1993; De ´monet et al., 1992).”
BackgroundHaidt, J., & Joseph, C. (2008) · The Innate Mind, Volume 3 · doi:10.1093/acprof:oso/9780195332834.003.0019 · Cited by 650 · see citing works
Shin, L. M., McNally, R. J., Kosslyn, S. M., Thompson, W. L., Rauch, S. L., Alpert, N. M., Metzger, L. J., Lasko, N. B., Orr, S. P., & Pitman, R. K. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.4.575 · Cited by 647 · see citing works
“In general, the left inferior frontal gyrus appears to be involved in speech production (40, 41), subvocal rehearsal (42), and inner speech (43).”
BackgroundArchitecture of the Prefrontal Cortex and the Central Executive
Goldman, P. S. (1995) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1995.tb38132.x · Cited by 640 · see citing works
The Neural Bases of Distraction and Reappraisal
McRae, K., Hughes, B., Chopra, S., Gabrieli, J. D. E., Gross, J. J., & Ochsner, K. N. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21243 · Cited by 642 · see citing works
“McRae et al. 253 2003; Paulesu, Frith, & Frackowiak, 1993 ) and regions of right inferior pFC associated with inhibition of motor responses (Aron, Robbins, & Poldrack, 2004) and other verbal strategies that can be used to down-regulate negative affective responses (Lieberman et al., 2007; Ochsner, Ray, et al., 2004).”
Cenquizca, L. A., & Swanson, L. W. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.002 · Cited by 640 · see citing works
Is developmental dyslexia a disconnection syndrome?
Paulesu, E., Uta Frith, A., Snowling, M. J., Gallagher, A., Morton, J., Frackowiak, R. S. J., & Frith, C. (1996) · Brain · doi:10.1093/brain/119.1.143 · Cited by 621 · see citing works
“The stereotactic coordinates of Broca's area reported in our earlier study (Paulesu et al., 1993) suggested that the activation focus fell in between BAs 44 and 6.”
BackgroundMethodResultInfluentialSelf-citationBrain imaging of the central executive component of working memory
Collette, F., & Van der Linden, M. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00063-x · Cited by 617 · see citing works
“This was made in order to be close to the procedure used by Paulesu, Frith and Frackowiak [93].”
MethodDuffau, H. (2005) · Brain · doi:10.1093/brain/awh423 · Cited by 619 · see citing works
Recovery from wernicke's aphasia: A positron emission tomographic study
Weiller, C., Isensee, C., Rijntjes, M., Huber, W., Müller, S. P., Bier, D. D., Dutschka, K., Woods, R. P., Noth, J., & Diener, H. (1995) · Annals of Neurology · doi:10.1002/ana.410370605 · Cited by 612 · see citing works
Selective Deficits in Prefrontal Cortex Function in Medication-Naive Patients With Schizophrenia
Barch, D. M., Carter, C. S., Braver, T. S., Sabb, F. W., MacDonald, A. W., Noll, D. C., & Cohen, J. D. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.3.280 · Cited by 615 · see citing works
“Considerable controversy exists about what functions specific regions of PFC carry out in support of WM.”
BackgroundResultInfluentialPremotor Cortex Activation during Observation and Naming of Familiar Tools
Grafton, S. T., Fadiga, L., Arbib, M. A., & Rizzolatti, G. (1997) · NeuroImage · doi:10.1006/nimg.1997.0293 · Cited by 606 · see citing works
“An alternative possibility is that the phonological encoding of words describing the objects and their use occurs at this site (Demonet et al., 1992; Paulesu et al., 1993; Zatorre et al., 1992).”
BackgroundA cultural effect on brain function
Paulesu, E., McCrory, E., Fazio, F., Menoncello, L., Brunswick, N., Cappa, S. F., Cotelli, M., Cossu, G., Corte, F., Lorusso, M., et al. (2000) · Nature Neuroscience · doi:10.1038/71163 · Cited by 602 · see citing works
“Italian readers showed comparatively stronger activation of the left planum temporale (at the temporoparietal junction), a brain region that has been linked to phonological processin”
BackgroundSelf-citationWorking memory and executive control
Baddeley, A., & Sala, S. D. (1996) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1996.0123 · Cited by 606 · see citing works
Anatomical variability in the cortical representation of first and second language
Dehaene, S., Emmanuel Dupoux, A., Mehler, J., Cohen, L., Paulesu, E., Perani, D., de Moortele, P. V., Lehéricy, S., & Bihan, D. L. (1997) · Neuroreport · doi:10.1097/00001756-199712010-00030 · Cited by 588 · see citing works
Self-citationActivation of the prefrontal cortex in a nonspatial working memory task with functional MRI
Cohen, J. D., Forman, S. D., Braver, T. S., Casey, B. J., Servan‐Schreiber, D., & Noll, D. C. (1994) · Human Brain Mapping · doi:10.1002/hbm.460010407 · Cited by 576 · see citing works
Cortex and memory: emergence of a new paradigm
Fuster, J. M. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21280 · Cited by 559 · see citing works
Coull, J. T., Frith, C. D., Frackowiak, R. S. J., & Grasby, P. M. (1996) · Neuropsychologia · doi:10.1016/0028-3932(96)00029-2 · Cited by 566 · see citing works
Self-citationAttention: the mechanisms of consciousness.
Posner, M. I. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.16.7398 · Cited by 846 · see citing works
False recognition in younger and older adults: Exploring the characteristics of illusory memories
Norman, K. A., & Schacter, D. L. (1997) · Memory & Cognition · doi:10.3758/bf03211328 · Cited by 570 · see citing works
The Role of Parietal Cortex in Verbal Working Memory
Jonides, J. J., Schumacher, E. H., Smith, E. E., Koeppe, R. A., Awh, E., Reuter‐Lorenz, P. A., Marshuetz, C., & Willis, C. R. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-13-05026.1998 · Cited by 568 · see citing works
“This argument is consistent with previous research that has also implicated parietal (Paulesu et al., 1993; Smith et al., 1996; Jonides et al., 1997) and frontal (Cohen et al., 1997) mechanisms in the storage of information in working memory.”
BackgroundResultInfluentialA Meta-analysis of Executive Components of Working Memory
Nee, D. E., Brown, J. W., Askren, M. K., Berman, M. G., Demiralp, E., Krawitz, A., & Jonides, J. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs007 · Cited by 544 · see citing works
“attributed activations in this region to phonological storage (Paulesu et al. 1993) equating the region with Wernicke’s area.”
BackgroundExplicit and implicit processing of words and pseudowords by adult developmental dyslexics
Brunswick, N., McCrory, E., Price, C. J., Frith, C. D., & Frith, U. (1999) · Brain · doi:10.1093/brain/122.10.1901 · Cited by 553 · see citing works
Self-citationCortical Networks Underlying Mechanisms of Time Perception
Harrington, D. L., Haaland, K. Y., & Knight, R. T. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-03-01085.1998 · Cited by 561 · see citing works
“However, different frontal areas have been associated with working memory (Pardo et al., 1991; Paulesu et al., 1993), and cytoarchitectonic maps of some areas (9 and 46) vary considerably (Rajkowska and Goldman-Rakic, 1995a).”
BackgroundFuster, J. M. (2000) · Experimental Brain Research · doi:10.1007/s002210000401 · Cited by 558 · see citing works
Isolating the neural mechanisms of age-related changes in human working memory
Rypma, B., & D’Esposito, M. (2000) · Nature Neuroscience · doi:10.1038/74889 · Cited by 549 · see citing works
Demonstrating the implicit processing of visually presented words and pseudowords
Price, C. J., Wise, R. J. S., & Frackowiak, R. S. J. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.1.62 · Cited by 544 · see citing works
Self-citationIntegration of diverse information in working memory within the frontal lobe
Prabhakaran, V., Narayanan, K., Zhao, Z., & Gabrieli, J. D. E. (2000) · Nature Neuroscience · doi:10.1038/71156 · Cited by 539 · see citing works
PET studies of encoding and retrieval: The HERA model
Nyberg, L. H., Cabeza, R. E. L., & Tulving, E. (1996) · Psychonomic Bulletin & Review · doi:10.3758/bf03212412 · Cited by 544 · see citing works
Load-Dependent Roles of Frontal Brain Regions in the Maintenance of Working Memory
Rypma, B., Prabhakaran, V., Desmond, J. E., Glover, G. H., & Gabrieli, J. D. E. (1999) · NeuroImage · doi:10.1006/nimg.1998.0404 · Cited by 545 · see citing works
An fMRI investigation of syllable sequence production
Bohland, J. W., & Guenther, F. H. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.04.173 · Cited by 545 · see citing works
“The latter area has been associated with the “phonological store” portion of Baddeley’s (1986) phonological loop model (Paulesu et al., 1993; Awh et al., 1996; Jonides et al., 1998); in Baddeley’s model this module contains phonological representations which can be temporarily activated by incoming verbal information.”
Background
- Authors
- Paulesu, E., Frith, C. D., & Frackowiak, R. S. J.
- Affiliations
- Hammersmith Hospital (GB)
- Venue
- Nature
- Published
- 1993-03-25
- Volume
- 362
- Issue
- 6418
- Pages
- 342-345
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2002007413
- Semantic Scholar
- e8a97ed48aa1080587f488566102cd9b169a5a1c
- Cited by
- 2,230
- References
- 25
- Citations by year
- 2026: 17 · 2025: 19 · 2024: 23 · 2023: 18 · 2022: 27 · 2021: 40 · 2020: 34 · 2019: 42 · 2018: 46 · 2017: 50 · 2016: 46 · 2015: 73 · 2014: 72 · 2013: 75 · 2012: 68
- FWCI
- 36.34
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Abilities and Testing
- Social Sciences › Psychology › Developmental and Educational Psychology › Reading and Literacy Development
- Keywords
- working memory, verbal short-term memory, phonological loop, phonological store, subvocal rehearsal, regional cerebral blood flow, Broca's area, neural correlates, visual word recognition
- MeSH terms
- Brain Mapping, Cerebrovascular Circulation, Frontal Lobe, Humans, Male, Memory, Short-Term, Models, Neurological, Parietal Lobe, Verbal Behavior
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