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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 (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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“2003), in contradiction to the idea that this brain region has a pivotal role in human working memory (Paulesu et al. 1993; Smith and Jonides 1997; 1998).”
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“The phonological loop is thought to be based on a cortical network comprising the left inferior parietal lobe and the premotor cortex (Paulesu et al., 1993; Baddeley, 2000); however, for the episodic buffer there is evidence that, among other neural networks, theMTL plays at least a supportive role (Berlingeri et al.”
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“Previous functional imaging studies have described sustained activity in the medial wall during working memory tasks (e.g. Paulesu et al., 1993; Courtney et al., 1996; Fiez et al., 1996; D'Esposito et al., 1998).”
BackgroundSelf-citationEvaluating models of working memory through the effects of concurrent irrelevant information.
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“Although previous research treats Broca’s area as the most likely site of subvocal rehearsal (e.g., Awh et al., 1996; Henson, 2001; Paulesu et al., 1993; E. E. Smith & Jonides, 1999), the ventral portions of this region may be more appropriately interpreted as a site of representation for novel…”
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“The fact, that both the analyses of verbal WM and abstract WM demonstrated extended identical cerebellar activation patterns does not support a role of the cerebellum solely in the context of the articulatory control system ofWM, as proposed by a number of studies (Awh et al., 1996; Desmond et al., 1997; Desmond and F…”
BackgroundInfluentialResolving sentence ambiguity with planning and working memory resources: Evidence from fMRI
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“Left IPC appears to support a component of WM (Awh et al., 1996; Chein and Fiez, 2001; Jonides et al., 1998; Marshuetz et al., 2000; Paulesu et al., 1993; Smith and Jonides, 2002).”
BackgroundPhonological Neighborhood Effects in Spoken Word Production: An fMRI Study
Peramunage, D., Blumstein, S. E., Myers, E. B., Goldrick, M., & Baese‐Berk, M. M. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21489 · Cited by 87
“Activation of the SMG extending into the posterior STG is consistent, with recent work showing activation in these areas in the perception of the phonological sound shape of words (Hickok & Poeppel, 2000; Paulesu et al., 1993) and in the perception of auditorily presented words under conditions of phonological competi…”
Executive working memory processes in dyslexia: Behavioral and fMRI evidence
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Neural modeling and functional neuroimaging
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The nature of working memory in linguistic, arithmetic and spatial integration processes
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“, 1991; Vallar & Shallice, 1990); and (4) neuroimaging studies suggesting that different neural substrates underlie verbal memory tasks and spatial memory tasks (Jonides et al., 1993; Paulesu et al., 1993).”
Current perspectives on the cerebellum and reading development
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“Several studies have reported activation of the left PFC when subjects are instructed to focus on phonological aspects of speech stimuli, in addition to left parietal lobe areas and occasionally the left supramarginal gyrus ( Paulesu et al., 1993; Zatorre et al., 1996).”
BackgroundNeural bases of focusing attention in working memory: An fMRI study based on group differences
Osaka, M., KOMORI, M., MORISHITA, M., & Osaka, N. (2007) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.7.2.130 · Cited by 89
“The retention of verbal information in the phonological loop is associated with activation in the left ventrolateral prefrontal cortex (VLPFC), and the retention of visuospatial information with activation in the right homologues (Awh et al., 1996; Jonides et al., 1993; Owen et al., 1998; Paulesu, Frith, & Frackowiak,…”
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Segregation of Lexical and Sub-Lexical Reading Processes in the Left Perisylvian Cortex
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“Moreover, several functional imaging studies have suggested that the left temporo-parietal junction is the key region that subserves the phonological store [46–48].”
BackgroundNeural Correlates of Sublexical Processing in Phonological Working Memory
McGettigan, C., Warren, J. E., Eisner, F., Marshall, C. R., Shanmugalingam, P., & Scott, S. K. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21491 · Cited by 89
“At both two and four syllables, Klein et al., using PET, also manipulated “articulatory difficulty” through addition of consonant clusters, whereas Papoutsi et al., who used fMRI, employed two levels of phonotactic frequency.”
BackgroundInfluentialState estimation in posterior parietal cortex: Distinct poles of environmental and bodily states
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How Does Learning to Read Affect Speech Perception?
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“Indeed, studies of verbal working memory commonly implicate these regions (Paulesu et al., 1993; Romero et al., 2006; Koelsch et al., 2009).”
BackgroundWorking memory and FDG–PET dissociate early and late onset Alzheimer disease patients
Kalpouzos, G., Eustache, F., Sayette, V. D. L., Viader, F., Chételat, G., & Desgranges, B. (2005) · Journal of Neurology · doi:10.1007/s00415-005-0685-3 · Cited by 85
“Indeed, the most significant hypometabolic peak was located in the left supramarginal gyrus (BA40), which is a crucial region for phonological loop processes [2, 12, 25, 31, 43, 46, 56].”
Hierarchical functional connectivity between the core language system and the working memory system
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“…been traditionally conceptualized as operations on information actively maintained in the phonological loop, which is primarily subserved by the anterior language system of the bilateral premotor and dorsal inferior frontal cortex rather than the hippocampus (Baddeley, 1992; Paulesu et al., 1993).”
BackgroundBilateral slowing of mentally simulated actions after stroke
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Frontal Lobe Functioning in Man: The Riddle Revisited
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“and globally broadcast in the usual way ( Paulescu et al., 1993; Kosslyn, 1994; Shergill et al.,”
BackgroundMeyer, L., Obleser, J., Anwander, A., & Friederici, A. D. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.05.052 · Cited by 86
“…studies encompassed various regions, including left superior temporal gyrus (STG) (Kim et al., 2002), SMG (Awh et al., 1996; Clark et al., 2000; Paulesu et al., 1993) and left inferior and posterior parietal cortices (Awh et al., 1995; Becker et al., 1996; Bushara et al., 1999; Clark et al.,…”
Reading, hearing, and the planum temporale
Buchsbaum, B. R., Olsen, R. K., Koch, P. F., Kohn, P. D., Kippenhan, J. S., & Berman, K. F. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.08.025 · Cited by 89
“…tasks (Postle et al., 1999; Sakai and Passingham, 2003)—although far more studies of verbal working memory have not found evidence for superior temporal lobe participation in so-called bphonological storageQ (e.g., Paulesu et al., 1993; Fiez et al., 1996; Awh et al., 1996; Jonides et al., 1998).”
InfluentialNeural basis for generalized quantifier comprehension
McMillan, C. T., Clark, R., Moore, P., DeVita, C., & Grossman, M. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2005.02.012 · Cited by 85
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“See Paulescu et al., 1993; Shergill et al., 2002.)”
BackgroundSeparable Neuronal Circuitries for Manipulable and Non-manipulable Objects in Working Memory
Mecklinger, A. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.11.1115 · Cited by 86
“In verbal working memory tasks, Broca's area has been associated with subvocal rehearsal processes (Paulesu et al., 1993; Cohen et al., 1997).”
BackgroundResultInfluentialAtypical Brain Activation During Simple & Complex Levels of Processing in Adult ADHD: An fMRI Study
Sigi Hale, T., Bookheimer, S., McGough, J. J., Phillips, J. M., & McCracken, J. T. (2007) · Journal of Attention Disorders · doi:10.1177/1087054706294101 · Cited by 84
Kim, J., Whyte, J., Wang, J., Rao, H., Tang, K. Z., & Detre, J. A. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.11.035 · Cited by 86
“It is known from previous PET studies that there are significantly smaller CBF changes during cognitive activation tasks compared to those during simple sensory–motor tasks (Colebatch et al., 1991; Jonides et al., 1997; Paulesu et al., 1993; Ramsey et al., 1996).”
ResultVerbal and spatial memory spans in Alzheimer's and multi-infarct dementia
Carlesimo, G. A., Fadda, L., Lorusso, S., & Caltagirone, C. (2009) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1994.tb01648.x · Cited by 85
Fulbright, R. K., Manson, S. C., Skudlarski, P., Lacadie, C., & Gore, J. C. (2003) · PubMed Central · Cited by 82
Ruchkin, D. S., Berndt, R. S., Johnson, R., Ritter, W., Grafman, J. H., & Canoune, H. L. (1997) · Cognitive Brain Research · doi:10.1016/s0926-6410(97)00021-9 · Cited by 83
Neural correlates of auditory temporal predictions during sensorimotor synchronization
Pecenka, N., Engel, A., & Keller, P. E. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00380 · Cited by 88
“…area that has been more typically observed during verbal compared to nonverbal working-memory tasks (and particularly identity comparisons; cf. Owen et al., 2005) and has been revealed as a key structure for subvocal rehearsal (e.g., Paulesu et al., 1993; Smith and Jonides, 1998; Baddeley, 2003).”
BackgroundModality Specific Cerebro-Cerebellar Activations in Verbal Working Memory: An fMRI Study
Kirschen, M. P., Chen, S. A., & Desmond, J. E. (2010) · Behavioural Neurology · doi:10.1155/2010/587450 · Cited by 85
Videsott, G., Herrnberger, B., Hoenig, K., Schilly, E., Grothe, J., Wiater, W., Spitzer, M., & Kiefer, M. (2010) · Brain and Language · doi:10.1016/j.bandl.2010.01.006 · Cited by 80
The neural response to changing semantic and perceptual complexity during language processing
Sharp, D. J., Awad, M., Warren, J. E., Wise, R. J. S., Vigliocco, G., & Scott, S. K. (2009) · Human Brain Mapping · doi:10.1002/hbm.20871 · Cited by 81
“…that the supramarginal gyrus within the inferior parietal lobe forms part of a fronto-parietal circuit supporting the encoding, maintenance, and selection of phonological information held in working memory [Braver et al., 1997; Paulesu et al., 1993; Shallice and Vallar, 1990; Zatorre et al., 1996].”
BackgroundResultIndividual Differences in Sentence Memory
Roberts, R., & Gibson, E. A. F. (2002) · Journal of Psycholinguistic Research · doi:10.1023/a:1021213004302 · Cited by 81
“…verbal information using a phonological code 3 (Awh et al., 1996; Baddeley, 1996; Basso, Spinnler, Vallar, & Zanobio, 1982; Fiez et al., 1996; Paulesu, Frith, & Frackowiak, 1993; Vallar, Betta, & Silveri, 1997); and the central executive (CE), used for allocating attention, planning,…”
Jeong, H., Sugiura, M., Sassa, Y., et al. (2006) · Human Brain Mapping · doi:10.1002/hbm.20269 · Cited by 81
“Several studies [Awh et al., 1996; Baddeley, 1986; Paulesu et al., 1993] have emphasized the relationship between the right cerebellum and the left IFG.”
Dissociating semantic and phonological maintenance using fMRI
Shivde, G., & Thompson‐Schill, S. L. (2004) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.4.1.10 · Cited by 81
Campbell, J. L., Langdon, D. W., Cercignani, M., & Rashid, W. (2016) · Neural Plasticity · doi:10.1155/2016/4292585 · Cited by 88
“24 Functional MRI (fMRI) and position emission tomography (PET) studies have better defined these anatomical areas involved in working memory [147-150].”
BackgroundMendrek, A., Kiehl, K. A., Smith, A., Irwin, D., Forster, B. B., & Liddle, P. F. (2005) · Psychological Medicine · doi:10.1017/s0033291704003228 · Cited by 85
“Several studies have provided evidence that the PFC is responsible for the central executive and phonological loop component of a workingmemory function, while the posterior parietal cortex appears to serve as a phonological storage of information (Paulesu et al. 1993; Awh et al. 1996; Cohen et al. 1997).”
BackgroundBright, P., Moss, H. E., Stamatakis, E. A., & TYLER, L. K. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.02.019 · Cited by 81
“... arise if atrophy extends into the LIFG (Shapiro & Caramazza, 2003; Stamatakis, Marslen-Wilson, Tyler, & Fletcher, 2005; Tyler, deMornay-Davies, et al., 2002; Tyler, Marslen-Wilson, & Stamatakis, 2005a, 2005b; Tyler, Randall, & Marslen-Wilson, 2002; Tyler, Stamatakis, Post, Randall, & Marslen-Wilson, 2005), and pho…”
The prefrontal cortex: from monkey to man
Lévy, R. (2023) · Brain · doi:10.1093/brain/awad389 · Cited by 88
Adaptive influence of long term high altitude residence on spatial working memory: An fMRI study
Yan, X., Zhang, J., Gong, Q., & Weng, X. (2011) · Brain and Cognition · doi:10.1016/j.bandc.2011.06.002 · Cited by 82
Mottaghy, F. M., Gangitano, M., Krause, B. J., & Pascual‐Leone, Á. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00010-7 · Cited by 82
“Their functionality has been attributed to the subvocal rehearsal system (e.g., Paulesu et al., 1993; Smith et al., 1998).”
BackgroundMethodFunctional MRI study of PASAT in normal subjects
Audoin, B., Ibarrola, D., Duong, M. V. A., Pelletier, J., Sylviane Confort-gouny, A., Irina Malikova, A., Ali‐Chérif, A., Cozzone, P. J., & Ranjeva, J. (2005) · Magnetic Resonance Materials in Physics Biology and Medicine · doi:10.1007/s10334-004-0098-9 · Cited by 80
“Regions including the left supramarginalis gyrus (BA 40) and the posterior part of the left superior temporal gyrus (BA 22) have been associated with phonological store [18].”
BackgroundMorin, A., & Hamper, B. (2012) · The Open Neuroimaging Journal · doi:10.2174/1874440001206010078 · Cited by 80
“It has been proposed that the LIFG serves additional functions besides covert speech per se, including cognitive control [38], working memory [39], language unification [40], selection among competing alternatives [41, 42], response inhibition [43], and action understanding [44].”
BackgroundMaruishi, M., Miyatani, M., Nakao, T., & Muranaka, H. (2006) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2006.097345 · Cited by 83
White, D. A., Gragert, M. N., Mandernach, T., Huntington, K., & Steiner, R. D. (2002) · Journal of the International Neuropsychological Society · doi:10.1017/s135561770102001x · Cited by 80
“…studies of healthy adults have shown that the prefrontal cortex is activated during the performance of working memory tasks involving verbal (Awh et al., 1996; Fiez et al., 1996; Paulesu et al., 1993; Petrides et al., 1993) and nonverbal (Jonides et al., 1993; Smith et al., 1995) materials.”
BackgroundCo-localizing linguistic and musical syntax with intracranial EEG
Sammler, D., Koelsch, S., Tonio Ball, A., Brandt, A., Grigutsch, M., Huppertz, H., Knösche, T. R., Wellmer, J., Widman, G., Elger, C. E., et al. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.09.035 · Cited by 80
“Note that these differences are desired consequences of our baseline filter (see Material and methods and Discussion) to avoid offset effects (Steinhauer and Drury, 2012).”
BackgroundInnateness, autonomy, universality? Neurobiological approaches to language
Müller, R. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00043296 · Cited by 79
Cognitive neuroscience perspective on memory: overview and summary
Sridhar, S., Khamaj, A., & Asthana, M. K. (2023) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2023.1217093 · Cited by 80
“The left inferior frontal gyrus (Broca’s area) and the left posterior superior temporal gyrus (Wernicke’s area) has been proposed to play a critical role in supporting phonological and verbal working memory tasks, specifically the subvocal rehearsal system of the articulatory loop (Paulesu et al., 1993; Buchsbaum et a…”
BackgroundMajerus, S., Bastin, C., Poncelet, M., der Linden, M. V., Salmon, É., Collette, F., & Maquet, P. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.12.008 · Cited by 79
Gentilucci, M., Bernardis, P., Crisi, G., & Volta, R. D. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.7.1059 · Cited by 80
“On the other hand, Broca’s area has been proposed to be involved in encoding phonological representations in terms of mouth articulation gestures ( Paulesu, Frith, & Frackowiak, 1993; Demonet et al., 1992; Zatorre, Evans, Meyer, & Gjedde, 1992).”
BackgroundMapping of verbal working memory in nonfluent Chinese–English bilinguals with functional MRI
Xue, G., Dong, Q., Jin, Z. H., & Chen, C. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.01.013 · Cited by 80
“…including Broca’s area (BA44) and the premotor and supplementary motor areas (BA6), and an executive component in the dorsolateral PFC (BA9/46) (Awh et al., 1996; Honey et al., 2002; Jonides et al., 1997; Paulesu et al., 1993; Smith et al., 1996; see also, Smith and Jonides, 1998, for a review).”
BackgroundThe underlying mechanisms of verbal fluency deficit in frontotemporal dementia and semantic dementia
Laisney, M., Matuszewski, V., Mézenge, F., Belliard, S., Sayette, V. D. L., Eustache, F., & Desgranges, B. (2009) · Journal of Neurology · doi:10.1007/s00415-009-5073-y · Cited by 84
“It has been claimed that the left parietal cortex is the verbal short-term store [30, 45], whereas the right parietal cortex has been found to be involved in task switching [6, 74].”
BackgroundYarkoni, T., Speer, N. K., Balota, D. A., McAvoy, M. P., & Zacks, J. M. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.04.258 · Cited by 78
“Other effects are novel but follow naturally from existing models, e.g., the relatively selective time-on-task effect of naming latencies on bilateral IFG activation, consistent with a role for this region in subvocal articulation or rehearsal (Henson et al., 2000; Paulesu et al., 1993 ).”
Activation of Multi‐modal Cortical Areas Underlies Short‐term Memory
Klingberg, T., Kawashima, R., & Roland, P. E. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01340.x · Cited by 79
Metadata
- 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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