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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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“It has been proposed that dorsolateral posterior aspects of PFC mediate subvocal rehearsal in verbal working memory [Paulesu et al., 1993, 1996).”
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“…areas are connected also play a specific role in acoustic and phonological analyses and the storage and manipulation of speech stimuli (E. Paulesu et al., 1993; P. Paulesu et al., 1993; Awh et al., 1995; Schumacher et al., 1996; Zatorre et al., 1996; Poldrack et al., 1999; Burton et al.,…”
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“This is consistent with findings that show parietal involvement in sensory working memory (e.g. Paulesu et al. 1993; Klingberg et al. 1996, 1997; Chafee and Goldman-Rakic 1998).”
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“Also, temporoparietal regions including the superior temporal, supramarginal, and angular gyri as well as occipitotemporal areas have been associated with phonological processes (Church et al., 2008; Paulesu et al., 1993; Pugh et al., 1996; Rumsey et al., 1997; Shaywitz and Shaywitz, 2005).”
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“This behavioural effect may be mediated by interference with processes occurring in Broca’s area, a region identified as possibly mediating the phonological loop rehearsal processes in Baddeley’s working memory model (Baddeley, 1995 ; Paulesu et al., 1993).”
BackgroundHirano, J., Takamiya, A., Yamagata, B., Hotta, S., Miyasaka, Y., Pu, S., Iwanami, A., Uchida, H., & Mimura, M. (2017) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2017.02.018 · Cited by 59
“The left lower frontal gyrus (Broca’s area, Brodmann’s area 44) is thought to be involved in the phonological loop, including articulatory rehearsal (Paulesu et al., 1993; Henson et al., 2000; Vallar et al., 1997).”
BackgroundSulcal depth in prefrontal cortex: a novel predictor of working memory performance
Yao, J. K., Voorhies, W. I., Miller, J. A., Bunge, S. A., & Weiner, K. S. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac173 · Cited by 65
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“The third ROI was located in the left inferior temporal gyrus ( 56, 32, 16, lower panel): The difference between noncanonical and canonical sentences was more pronounced in the ambiguous sentences (see also Table III). r 946 r et al., 1998; Paulesu et al., 1993].”
Kübler, A., Murphy, K., Kaufman, J. N., Stein, E. A., & Garavan, H. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00400-2 · Cited by 60
“Parietal cortex is often considered the seat of storage and maintenance processes in verbal and spatial working memory tasks (Bunge et al., 2000; Hartley and Speer, 2000; Honey et al., 2000; Jonides et al., 1998; Paulesu et al., 1993; Salmon et al., 1996; Smith et al., 1998).”
BackgroundFunctional Neuroanatomy of Segmenting Speech and Nonspeech
Burton, M. W., & Small, S. L. (2006) · Cortex · doi:10.1016/s0010-9452(08)70400-3 · Cited by 62
“…temporal regions appear to be associated with early acoustic/phonetic processing (e.g., Zatorre et al., 1992), the parietal region with short-term storage of phonological information (e.g., Paulesu et al., 1993), and the frontal regions with articulatory recoding of speech (Zatorre et al., 1996).”
BackgroundCortical Areas Activated by Bilateral Galvanic Vestibular Stimulation
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“…gyrus has been often involved in phonological processes (e.g. mapping orthography to phonology, phonological recoding, rhyme detection etc., see Paulesu et al., 1993; Demonet et al., 1994; Seghier et al., 2004), while the angular gyrus has been involved in semantic processing (Binder et al.,…”
BackgroundVerbal storage in a premotor–parietal network: evidence from fMRI-guided magnetic stimulation
Herwig, U., Abler, B., Schönfeldt‐Lecuona, C., Wunderlich, A. P., Grothe, J., Spitzer, M., & Walter, H. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00368-9 · Cited by 61
“Phonological storage has been found to involve parietal areas (Paulesu et al., 1993; Awh et al., 1996; Jonides et al., 1998).”
Is Broca's area involved in the processing of passive sentences? An event-related fMRI study
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“Phonological working memory (Baddeley, 1992 ) is composed of a phonological store, localized in the left SMG, and an articulatory control process, located in the left IFG (Paulesu, Frith, & Frackowiak, 1993 ).”
BackgroundA slow wave investigation of working memory biases in mood disorders.
Deldin, P. J., Deveney, C. M., Kim, A. S., Casas, B. R., & Best, J. L. (2001) · Journal of Abnormal Psychology · doi:10.1037//0021-843x.110.2.267 · Cited by 59
Neural basis for sentence comprehension deficits in frontotemporal dementia
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“This region has been associated with WM for letters, possibly a frontal rehearsal component that helps maintain verbal information in WM (Awh et al., 1996; Jonides et al., 1997; Paulesu, Frith, & Frackowiak, 1993; Smith & Jonides, 1999).”
BackgroundMoores, K. A., Clark, C. R., Hadfield, J. L. M., Brown, G. C., Taylor, D. J. F., Fitzgibbon, S. P., Lewis, A. C., Weber, D. L., & Greenblatt, R. E. (2002) · Human Brain Mapping · doi:10.1002/hbm.10073 · Cited by 59
“Lastly, activity in this region has also been observed in verbal working memory tasks on the left [Beuregard et al., 1997; Paulesu et al., 1993, 1995; Salmon et al., 1996] and bilaterally [Chee et al., 1999; Coull et al., 1996; Honey et al., 2000].”
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Prefrontal Neuronal Responses during Audiovisual Mnemonic Processing
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“, 2010; Lee and Noppeney, 2011), but also when they are stored in memory for further manipulation, which suggests IFG plays a role in working memory (WM) of communication stimuli (Paulesu et al., 1993; Schumacher et al., 1996; Crottaz-Herbette et al., 2004; Rämä and Courtney, 2005).”
BackgroundRangaswamy, M., Porjesz, B., Ardekani, B. A., Choi, S. J., Tanabe, J., Lim, K. O., & Begleiter, H. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.09.018 · Cited by 58
“Inferior frontal gyrus (BA 44/6) activation has been reported in studies on verbal working memory and in particular for phonological processing (Awh et al., 1996; Jonides et al., 1998; McDermott et al., 2003; Paulesu et al., 1993).”
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Working memory load modulates the auditory “What” and “Where” neural networks
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“Previous studies have shown that the left supramarginal gyrus and the left IPL were neural correlates of the phonological storage component responsible for holding verbal information in Baddeley's (1986) working memory model (e.g., Awh et al., 1996; Paulesu et al., 1993; Ravizza et al., 2004; Salmon et al., 1996).”
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“The actual memory representations are thought to be temporarily stored based on their spatial or verbal features, with the verbal features being processed by a so-called phonological loop that maintains language-related memory representations, and has been strongly linked to activity in the superior temporal/supramarg…”
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Visual word stem completion priming within and across modalities
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“For example, an utterance can be perceived as sadder if it expresses passivity phonological store to the left supramarginal gyrus (Paulesu et al., 1993).”
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“, 2012) emerged from supramarginal gyrus, a brain region often found to be actively involved in short-term memory (Gaab et al., 2003; Paulesu et al., 1993).”
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“, 1988) and in particular during a rhyming task which engages subvocal rehearsal (Ruchkin et al., 1990, 1997; Paulesu et al., 1993).”
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“Finally, Broca’s area has been implicated during attention to sensory stimuli (Curtis & D’Esposito, 2003; Kaas et al., 2012; Paulesu et al., 1993) probably related to body-part semantics (Braitenberg & Pulvermüller, 1992), and visuo-spatial body representation (Hauk & Pulvermüller, 2011; Van Elk &…”
BackgroundPaulesu, E., Shallice, T., Danelli, L., Sberna, M., Frackowiak, R. S. J., & Frith, C. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00231 · Cited by 56
“The multi-component nature of the phonological loop has also been supported by functional anatomical models in normal subjects of the mid 90s (Paulesu et al., 1993; Demonet et al., 1994; for discussions see Demonet et al., 1996; Paulesu et al., 1996a; Dolan et al., 1997).”
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The Role of the Cerebellum in Cognition
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Age-Related Changes in Task Related Functional Network Connectivity
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Automatic audiovisual integration in speech perception
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“Broca’s area, which is known to be involved in encoding phonological representations in terms of mouth articulation gestures (Demonet et al. 1992; Paulesu et al. 1993; Zatorre et al. 1992) is activated also by imitation of face movements (Carr et al.”
BackgroundShallice, T., & Papagno, C. (2018) · Cortex · doi:10.1016/j.cortex.2018.10.004 · Cited by 56
The effect of rehearsal rate and memory load on verbal working memory
Fegen, D., Buchsbaum, B. R., & D'Esposito, M. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.034 · Cited by 56
“…are consistent with the proposed roles for these regions, with IFG (BA 44) thought to be involved in articulatory motor planning (Awh et al., 1996; Paulesu et al., 1993), PM (BA 6) thought to play an important role in the selection of phoneme- and syllable-level representations during speech…”
Cortical lateralization during verb generation: a combined ERP and fMRI study
Rowan, A., Liegeois, F. J., Vargha‐Khadem, F., Gadian, D. G., Connelly, A., & Baldeweg, T. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.01.034 · Cited by 53
Cupini, L. M., Matteis, M., Troisi, E., et al. (1996) · Brain · doi:10.1093/brain/119.4.1249 · Cited by 56
“This finding is at variance with the results from previous studies in man (Paulesu et al., 1993) in which a significant activation of the left hemisphere was observed with PET analysis during a letter verbal task.”
BackgroundMethodResultInfluentialNeural correlates of working memory performance in adolescents and young adults with dyslexia
Vasić, N., Lohr, C., Steinbrink, C., Martin, C., & Wolf, R. C. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2007.09.002 · Cited by 58
Right parietal contributions to verbal working memory: Spatial or executive?
Ravizza, S. M., Behrmann, M., & Fiez, J. A. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2005.03.014 · Cited by 60
“Given that the cerebellum is often implicated in imaging studies of verbal working memory, potentially by aiding articulatory rehearsal (Paulesu et al., 1993), we would predict that central presentation should have less impact on this patient’s performance compared to RB.”
BackgroundMethodInfluentialCallan, D. E., & Schweighofer, N. (2010) · Human Brain Mapping · doi:10.1002/hbm.20894 · Cited by 55
“The frontal operculum is involved in a variety of other verbal and nonverbal functions, such as acoustic-articulatory processing [Fiez et al., 1995; Paulesu et al., 1993], syllable sequence production [Bohland and Guenther, 2006], implicit priming [Wagner et al.”
BackgroundInfluentialPierpont, E. I., Richmond, E. K., Abbeduto, L., Kover, S. T., & Brown, W. T. (2011) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-011-9095-2 · Cited by 55
“These types of phonological memory tasks typically result in the activation of a brain network that includes the left inferior frontal and premotor cortex, supplementary motor areas, and cerebellum (Lycke et al. 2008; Paulesu et al. 1993; Awh et al. 1996).”
BackgroundHara, T., Abo, M., Kobayashi, K., Watanabe, M., Kakuda, W., & Senoo, A. (2015) · Translational Stroke Research · doi:10.1007/s12975-015-0417-7 · Cited by 55
When meaningless symbols become letters: Neural activity change in learning new phonograms
Callan, A. M., Callan, D. E., & Masaki, S. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.06.031 · Cited by 55
The role of the ventral and dorsal pathways in reading Chinese characters and English words
Sun, Y., Yang, Y., Desroches, A. S., Liu, L., & Peng, D. (2011) · Brain and Language · doi:10.1016/j.bandl.2011.03.012 · Cited by 55
“Previous studies have suggested that the middle frontal gyrus mediates spatial and verbal working memory processes, such the maintenance of a limited amount of spatial and verbal information (McCarthy et al., 1994; Owen et al., 1996; Paulesu et al., 1996; Courtney et al., 1998).”
BackgroundPhonological agraphia following a focal anterior insulo-opercular infarction
Mariën, P., Pickut, B. A., Engelborghs, S., Martin, J. J., & Deyn, P. P. D. (2001) · Neuropsychologia · doi:10.1016/s0028-3932(01)00006-9 · Cited by 56
The prefrontal cortex: insights from functional neuroimaging using cognitive activation tasks
Goethals, I., Audenaert, K., de Wiele, C. V., & Dierckx, R. A. J. O. (2003) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-003-1382-z · Cited by 57
Acquired focal brain lesions in childhood: Effects on development and reorganization of language
Chilosi, A. M. (2008) · Brain and Language · doi:10.1016/j.bandl.2007.12.010 · Cited by 55
Neural Correlates of Successful and Unsuccessful Verbal Memory Encoding
Casasanto, D. J., Killgore, W. D. S., Maldjian, J. A., Glosser, G., Alsop, D. C., Cooke, A., Grossman, M., & Detre, J. A. (2002) · Brain and Language · doi:10.1006/brln.2001.2584 · Cited by 55
Chan, W., Yang, G., Chia, M., Woon, P., Lee, J., Keefe, R. S. E., Sitoh, Y., Nowinski, W. L., & Sim, K. (2010) · Bipolar Disorders · doi:10.1111/j.1399-5618.2010.00829.x · Cited by 54
Spironelli, C., & Angrilli, A. (2007) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2007.02.002 · Cited by 54
Karlsgodt, K. H., Bachman, P., Winkler, A. M., Bearden, C. E., & Glahn, D. C. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.08.016 · Cited by 58
“Given the evidence that during WMem performance the frontal and parietal regions show synchronized neural activity and function as an integrated circuit [17,20,21,131] there is interest not just in the cortical regions themselves, but the connections between them such as the SLF, and in particular, to what extent WMem…”
BackgroundKelly, C. A. M., Hester, R., Foxe, J. J., Shpaner, M., & Garavan, H. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.01.008 · Cited by 54
“…been associated with working memory maintenance (dlPFC—see Curtis and D'Esposito, 2003), rehearsal (ventrolateral, premotor—e.g., Awh et al., 1995; Paulesu et al., 1993; Smith et al., 1998) and interference control (dorso/ ventrolateral—e.g., Bunge et al., 2001; D'Esposito et al., 1999; Jonides…”
BackgroundGuo, Z., Wu, X., Li, W., Jones, J. A., Yan, N., Sheft, S., Liu, P., & Liu, H. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1329-17.2017 · Cited by 54
“These brain regions have been identified both in the verbal WM tasks (Paulesu et al., 1993; Buchsbaum et al., 2005) and in the generation of vocal compensation for pitch feedback errors (Zarate et al., 2010; Behroozmand et al., 2015).”
BackgroundIngram, R. U., Halai, A. D., Pobric, G., Sajjadi, S. A., Patterson, K. E., & Ralph, M. A. L. (2020) · Brain · doi:10.1093/brain/awaa245 · Cited by 55
“mary systems with different brain areas: phonological processing and working memory with posterior superior temporal lobe and supra-marginal gyrus (Paulesu et al., 1993); semantic representation with anterior temporal lobe (ATL) (Patterson et al.”
BackgroundVerbal memory impairment after left insular cortex infarction
Manes, F. F., Springer, J., Jorge, R. E., & Robinson, R. G. (1999) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.67.4.532 · Cited by 54
The role of transcranial magnetic stimulation in the study of cerebellar cognitive function
Oliveri, M., Torriero, S., Koch, G., et al. (2007) · The Cerebellum · doi:10.1080/14734220701213421 · Cited by 54
Kim, J., Kim, M. S., Lee, J. S., Lee, D. S., Lee, M. C., & Kwon, J. S. (2002) · NeuroImage · doi:10.1006/nimg.2001.1025 · Cited by 54
“Previous imaging studies have indicated that brain activations accompanying verbal WM are found not only in the dorsolateral prefrontal cortex but also in other regions such as the inferior frontal area, supplementary motor area, premotor area, and parietal cortices (Paulesu et al., 1993; Petrides et al., 1993b; Andre…”
BackgroundResultInfluentialDistributed neural systems for temporal production: A functional MRI study
Basso, G., Nichelli, P., Wharton, C. M., Peterson, M., & Grafman, J. (2003) · Brain Research Bulletin · doi:10.1016/s0361-9230(02)00941-3 · Cited by 53
Age-Related Changes in the Anatomy of Language Regions in Autism Spectrum Disorder
Knaus, T. A., Silver, A. M., Dominick, K. C., Schuring, M. D., Shaffer, N., Lindgren, K. A., Joseph, R. M., & Tager-Flusberg, H. B. (2008) · Brain Imaging and Behavior · doi:10.1007/s11682-008-9048-x · Cited by 53
“Broca’s area has been shown to be involved in the organization of articulatory sequences and inner speech (Stuss and Benson 1986, cited in Demonet et al. 1992), in subvocal rehearsal ( Paulesu et al. 1993 ), and in the initiation of speech (Alexander et al. 1990).”
Modality- and Task-specific Brain Regions Involved in Chinese Lexical Processing
Liu, L., Deng, X., Peng, D., Cao, F., Ding, G., Jin, Z. H., Zeng, Y., Li, K., Lei, Z., Fan, N., et al. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21141 · Cited by 53
“Some have argued it is involved in the conversion between orthography and phonology (Booth et al., 2002; Xu et al., 2001; Lurito, Kareken, Lowe, Chen, & Mathews, 2000; Pugh et al., 1996), and others have suggested that it is part of the phonological loop ( Paulesu, Frith, & Frackowiak, 1993 ) or is involved in verbal…”
BackgroundMottaghy, F. M., Döring, T., Müller‐Gärtner, H., Töpper, R., & Krause, B. J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02209.x · Cited by 51
“Activations in the left SMG (Paulesu et al., 1993) were attributed to the phonological buffer (Baddeley & Hitch, 1974) but this area has been discussed in the context of motor attention, the control of limb movements and number processing (Deiber et al.”
BackgroundMethodInfluentialRavizza, S. M., Hazeltine, E., Ruiz, S., & Zhu, D. C. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.12.021 · Cited by 51
“3: Barch and Csernansky, 2007; Gruber and Von Cramon, 2001; Paulesu et al., 1993; Ravizza et al., 2004; Salmon et al., 1996).”
InfluentialMemory networks in the prefrontal cortex
Fuster, J. M. (2000) · Progress in Brain Research · doi:10.1016/s0079-6123(08)62147-0 · Cited by 51
Lœvenbruck, H., Baciu, M., Segebarth, C., & Abry, C. (2005) · Journal of Neurolinguistics · doi:10.1016/j.jneuroling.2004.12.002 · Cited by 42
Ylinen, S., Nora, A., Leminen, A., Hakala, T., Huotilainen, M., Shtyrov, Y., Mäkelä, J. P., & Service, E. (2015) · Cerebral Cortex · doi:10.1093/cercor/bht351 · Cited by 42
Maintenance of non-consciously presented information engages the prefrontal cortex
Bergström, F., & Eriksson, J. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00938 · Cited by 42
Fletcher, L., & Carruthers, P. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2011.0413 · Cited by 83
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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