Mapping the brain network of the phonological loop

C. Papagno, A. Comi, M. Riva, A. Bizzi, M. Vernice, A. Casarotti, E. Fava, L. Bello

Research output: Contribution to journalArticle

Abstract

The cortical and subcortical neural correlates underlying item and order information in verbal short-term memory (STM) were investigated by means of digit span in 29 patients with direct electrical stimulation during awake surgery for removal of a neoplastic lesion. Stimulation of left Broca's area interfered with span, producing significantly more item than order errors, as compared to the stimulation of the supramarginal/angular gyrus, which also interfered with span but, conversely, produced more order than item errors. Similarly, stimulation of the third segment of the left superior longitudinal fasciculus (SLF-III), also known as anterior segment of the arcuate fascicle (AF), produced more order than item errors. Therefore, we obtained two crucial results: first, we were able to distinguish between content and order information storage. Second, we demonstrated that the SLF-III is involved in transferring order information from Geschwind's area to Broca's area. In a few patients, we demonstrated that also order information of nonverbal material was disrupted by left supramarginal gyrus stimulation. Order information is thus likely stored in the supramarginal gyrus, possibly independently from the nature of the material. Hum Brain Mapp 38:3011–3024, 2017. © 2017 Wiley Periodicals, Inc. © 2017 Wiley Periodicals, Inc.
Original languageEnglish
Pages (from-to)3011-3024
Number of pages14
JournalHuman Brain Mapping
Volume38
Issue number6
DOIs
Publication statusPublished - 2017

Fingerprint

Brain Mapping
Parietal Lobe
Information Storage and Retrieval
Short-Term Memory
Electric Stimulation
Brain
Broca Area

Keywords

  • arcuate
  • direct electric stimulation
  • inferior parietal lobule
  • memory short-term
  • neurosurgery
  • adolescent
  • adult
  • aged
  • angular gyrus
  • arcuate fasciculus
  • Article
  • brain mapping
  • Broca area
  • clinical article
  • electrostimulation
  • female
  • human
  • male
  • nuclear magnetic resonance scanner
  • phonetics
  • priority journal
  • short term memory
  • superior longitudinal fasciculus
  • supramarginal gyrus
  • tractography
  • verbal memory

Cite this

Papagno, C., Comi, A., Riva, M., Bizzi, A., Vernice, M., Casarotti, A., ... Bello, L. (2017). Mapping the brain network of the phonological loop. Human Brain Mapping, 38(6), 3011-3024. https://doi.org/10.1002/hbm.23569

Mapping the brain network of the phonological loop. / Papagno, C.; Comi, A.; Riva, M.; Bizzi, A.; Vernice, M.; Casarotti, A.; Fava, E.; Bello, L.

In: Human Brain Mapping, Vol. 38, No. 6, 2017, p. 3011-3024.

Research output: Contribution to journalArticle

Papagno, C, Comi, A, Riva, M, Bizzi, A, Vernice, M, Casarotti, A, Fava, E & Bello, L 2017, 'Mapping the brain network of the phonological loop', Human Brain Mapping, vol. 38, no. 6, pp. 3011-3024. https://doi.org/10.1002/hbm.23569
Papagno C, Comi A, Riva M, Bizzi A, Vernice M, Casarotti A et al. Mapping the brain network of the phonological loop. Human Brain Mapping. 2017;38(6):3011-3024. https://doi.org/10.1002/hbm.23569
Papagno, C. ; Comi, A. ; Riva, M. ; Bizzi, A. ; Vernice, M. ; Casarotti, A. ; Fava, E. ; Bello, L. / Mapping the brain network of the phonological loop. In: Human Brain Mapping. 2017 ; Vol. 38, No. 6. pp. 3011-3024.
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title = "Mapping the brain network of the phonological loop",
abstract = "The cortical and subcortical neural correlates underlying item and order information in verbal short-term memory (STM) were investigated by means of digit span in 29 patients with direct electrical stimulation during awake surgery for removal of a neoplastic lesion. Stimulation of left Broca's area interfered with span, producing significantly more item than order errors, as compared to the stimulation of the supramarginal/angular gyrus, which also interfered with span but, conversely, produced more order than item errors. Similarly, stimulation of the third segment of the left superior longitudinal fasciculus (SLF-III), also known as anterior segment of the arcuate fascicle (AF), produced more order than item errors. Therefore, we obtained two crucial results: first, we were able to distinguish between content and order information storage. Second, we demonstrated that the SLF-III is involved in transferring order information from Geschwind's area to Broca's area. In a few patients, we demonstrated that also order information of nonverbal material was disrupted by left supramarginal gyrus stimulation. Order information is thus likely stored in the supramarginal gyrus, possibly independently from the nature of the material. Hum Brain Mapp 38:3011–3024, 2017. {\circledC} 2017 Wiley Periodicals, Inc. {\circledC} 2017 Wiley Periodicals, Inc.",
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author = "C. Papagno and A. Comi and M. Riva and A. Bizzi and M. Vernice and A. Casarotti and E. Fava and L. Bello",
note = "Cited By :3 Export Date: 2 March 2018 CODEN: HBMAE Correspondence Address: Papagno, C.; Dipartimento di Psicologia, Universit{\`a} di Milano-Bicocca, Piazza dell'Ateneo Nuovo 1, Italy; email: costanza.papagno@unimib.it Tradenames: Siemens Verio, Siemens, Germany Manufacturers: Siemens, Germany References: Attout, L., Van Der Kaa, M.A., George, M., Majerus, S., (2011) The importance of distinguishing item and order memory for understanding short-term memory deficits in brain-damaged patients, , Poster presented at the 49, Academy of Aphasia, Montreal October 16–18; Awh, E., Smith, E.E., Jonides, J., Human rehearsal processes and the frontal lobes: PET evidence (1995) Ann NY Acad Sci, 769, pp. 97-117; Babikian, T., Boone, K.B., Lu, P., Arnold, G., Sensitivity and specificity of various digit span scores in the detection of suspect effort (2006) Clin Neuropsychol, 20, pp. 145-159; Baddeley, A.D., The development of the concept of working memory: Implications and contributions of neuropsychology (1990) Neuropsychological Impairments of Short-Term Memory, pp. 54-73. , In, Vallar G, Shallice T, editors., Cambridge, Cambridge University Press, pp; Baddeley, A.D., Exploring the central executive (1996) Q J Exp Psychol A Hum Exp Psychol, 49, pp. 5-28; Baddeley, A.D., (2007) Working Memory, Thought, and Action, p. 215. , Oxford, Oxford University Press, p; Baddeley, A.D., Working memory: Theories, models, and controversies (2012) Ann Rev Psychol, 63, pp. 1-29; Baddeley, A.D., Gathercole, S., Papagno, C., The Phonological loop as a language learning device (1998) Psychol Rev, 105, pp. 158-173; Baddeley, A.D., Papagno, C., Vallar, G., When long term learning depends on short-term storage (1988) J Mem Lang, 27, pp. 586-595; Baddeley, A.D., Salam{\'e}, P., The unattended speech effect: perception or memory? (1986) J Exp Psychol Learn Mem Cogn, 12, pp. 525-529; Baldo, J.V., Dronkers, N.F., The role of inferior parietal and inferior frontal cortex in working memory (2006) Neuropsychology, 20, pp. 529-538; Bello, L., Gambini, A., Castellano, A., Carrabba, G., Acerbi, F., Fava, E., Giussani, C., Falini, A., Motor and language DTI fiber tracking combined with intraoperative subcortical mapping for surgical removal of gliomas (2008) Neuroimage, 39, pp. 369-382; Bello, L., Riva, M., Fava, E., Ferpozzi, V., Castellano, A., Raneri, F., Pessina, F., Cerri, G., Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving the motor pathways (2014) Neuro-Oncol, 16, pp. 1110-1128; Bjork, E.L., Healy, A.F., Short-term order and item retention (1974) J Verb Learn Verb Behav, 13, pp. 80-97; Burgess, N., Hitch, J., Memory for serial order: a network model of the phonological loop and its timing (1999) Psychol Rev, 106, pp. 551-581; Cameron, A.C., Trivedi, P.K., (1998) Regression Analysis of Count Data, , Cambridge, UK, Cambridge University Press; Catani, M., Thiebaut de Schotten, M., A diffusion tensor imaging tractography atlas for virtual in vivo dissections (2008) Cortex, 44, pp. 1105-1132; Catani, M., Thiebaut de Schotten, M., (2012) Atlas of Human Connections, , Oxford, Oxford University Press; Catani, M., Jones, D.K., ffichte, D.H., Perisylvian language networks of the human brain (2005) Ann Neurol, 57, pp. 8-16; Catrical{\'a}, E., Della Rosa, P.A., Ginex, V., Mussetti, Z., Plebani, V., Cappa, S.F., An Italian battery for the assessment of semantic memory disorders (2013) Neurol Sci, 34, pp. 985-993; Cecchetto, C., Di Domenico, A., Garraffa, M., Papagno, C., (2012) Comprendo. 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year = "2017",
doi = "10.1002/hbm.23569",
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journal = "Human Brain Mapping",
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TY - JOUR

T1 - Mapping the brain network of the phonological loop

AU - Papagno, C.

AU - Comi, A.

AU - Riva, M.

AU - Bizzi, A.

AU - Vernice, M.

AU - Casarotti, A.

AU - Fava, E.

AU - Bello, L.

N1 - Cited By :3 Export Date: 2 March 2018 CODEN: HBMAE Correspondence Address: Papagno, C.; Dipartimento di Psicologia, Università di Milano-Bicocca, Piazza dell'Ateneo Nuovo 1, Italy; email: costanza.papagno@unimib.it Tradenames: Siemens Verio, Siemens, Germany Manufacturers: Siemens, Germany References: Attout, L., Van Der Kaa, M.A., George, M., Majerus, S., (2011) The importance of distinguishing item and order memory for understanding short-term memory deficits in brain-damaged patients, , Poster presented at the 49, Academy of Aphasia, Montreal October 16–18; Awh, E., Smith, E.E., Jonides, J., Human rehearsal processes and the frontal lobes: PET evidence (1995) Ann NY Acad Sci, 769, pp. 97-117; Babikian, T., Boone, K.B., Lu, P., Arnold, G., Sensitivity and specificity of various digit span scores in the detection of suspect effort (2006) Clin Neuropsychol, 20, pp. 145-159; Baddeley, A.D., The development of the concept of working memory: Implications and contributions of neuropsychology (1990) Neuropsychological Impairments of Short-Term Memory, pp. 54-73. , In, Vallar G, Shallice T, editors., Cambridge, Cambridge University Press, pp; Baddeley, A.D., Exploring the central executive (1996) Q J Exp Psychol A Hum Exp Psychol, 49, pp. 5-28; Baddeley, A.D., (2007) Working Memory, Thought, and Action, p. 215. , Oxford, Oxford University Press, p; Baddeley, A.D., Working memory: Theories, models, and controversies (2012) Ann Rev Psychol, 63, pp. 1-29; Baddeley, A.D., Gathercole, S., Papagno, C., The Phonological loop as a language learning device (1998) Psychol Rev, 105, pp. 158-173; Baddeley, A.D., Papagno, C., Vallar, G., When long term learning depends on short-term storage (1988) J Mem Lang, 27, pp. 586-595; Baddeley, A.D., Salamé, P., The unattended speech effect: perception or memory? (1986) J Exp Psychol Learn Mem Cogn, 12, pp. 525-529; Baldo, J.V., Dronkers, N.F., The role of inferior parietal and inferior frontal cortex in working memory (2006) Neuropsychology, 20, pp. 529-538; Bello, L., Gambini, A., Castellano, A., Carrabba, G., Acerbi, F., Fava, E., Giussani, C., Falini, A., Motor and language DTI fiber tracking combined with intraoperative subcortical mapping for surgical removal of gliomas (2008) Neuroimage, 39, pp. 369-382; Bello, L., Riva, M., Fava, E., Ferpozzi, V., Castellano, A., Raneri, F., Pessina, F., Cerri, G., Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving the motor pathways (2014) Neuro-Oncol, 16, pp. 1110-1128; Bjork, E.L., Healy, A.F., Short-term order and item retention (1974) J Verb Learn Verb Behav, 13, pp. 80-97; Burgess, N., Hitch, J., Memory for serial order: a network model of the phonological loop and its timing (1999) Psychol Rev, 106, pp. 551-581; Cameron, A.C., Trivedi, P.K., (1998) Regression Analysis of Count Data, , Cambridge, UK, Cambridge University Press; Catani, M., Thiebaut de Schotten, M., A diffusion tensor imaging tractography atlas for virtual in vivo dissections (2008) Cortex, 44, pp. 1105-1132; Catani, M., Thiebaut de Schotten, M., (2012) Atlas of Human Connections, , Oxford, Oxford University Press; Catani, M., Jones, D.K., ffichte, D.H., Perisylvian language networks of the human brain (2005) Ann Neurol, 57, pp. 8-16; Catricalá, E., Della Rosa, P.A., Ginex, V., Mussetti, Z., Plebani, V., Cappa, S.F., An Italian battery for the assessment of semantic memory disorders (2013) Neurol Sci, 34, pp. 985-993; Cecchetto, C., Di Domenico, A., Garraffa, M., Papagno, C., (2012) Comprendo. 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PY - 2017

Y1 - 2017

N2 - The cortical and subcortical neural correlates underlying item and order information in verbal short-term memory (STM) were investigated by means of digit span in 29 patients with direct electrical stimulation during awake surgery for removal of a neoplastic lesion. Stimulation of left Broca's area interfered with span, producing significantly more item than order errors, as compared to the stimulation of the supramarginal/angular gyrus, which also interfered with span but, conversely, produced more order than item errors. Similarly, stimulation of the third segment of the left superior longitudinal fasciculus (SLF-III), also known as anterior segment of the arcuate fascicle (AF), produced more order than item errors. Therefore, we obtained two crucial results: first, we were able to distinguish between content and order information storage. Second, we demonstrated that the SLF-III is involved in transferring order information from Geschwind's area to Broca's area. In a few patients, we demonstrated that also order information of nonverbal material was disrupted by left supramarginal gyrus stimulation. Order information is thus likely stored in the supramarginal gyrus, possibly independently from the nature of the material. Hum Brain Mapp 38:3011–3024, 2017. © 2017 Wiley Periodicals, Inc. © 2017 Wiley Periodicals, Inc.

AB - The cortical and subcortical neural correlates underlying item and order information in verbal short-term memory (STM) were investigated by means of digit span in 29 patients with direct electrical stimulation during awake surgery for removal of a neoplastic lesion. Stimulation of left Broca's area interfered with span, producing significantly more item than order errors, as compared to the stimulation of the supramarginal/angular gyrus, which also interfered with span but, conversely, produced more order than item errors. Similarly, stimulation of the third segment of the left superior longitudinal fasciculus (SLF-III), also known as anterior segment of the arcuate fascicle (AF), produced more order than item errors. Therefore, we obtained two crucial results: first, we were able to distinguish between content and order information storage. Second, we demonstrated that the SLF-III is involved in transferring order information from Geschwind's area to Broca's area. In a few patients, we demonstrated that also order information of nonverbal material was disrupted by left supramarginal gyrus stimulation. Order information is thus likely stored in the supramarginal gyrus, possibly independently from the nature of the material. Hum Brain Mapp 38:3011–3024, 2017. © 2017 Wiley Periodicals, Inc. © 2017 Wiley Periodicals, Inc.

KW - arcuate

KW - direct electric stimulation

KW - inferior parietal lobule

KW - memory short-term

KW - neurosurgery

KW - adolescent

KW - adult

KW - aged

KW - angular gyrus

KW - arcuate fasciculus

KW - Article

KW - brain mapping

KW - Broca area

KW - clinical article

KW - electrostimulation

KW - female

KW - human

KW - male

KW - nuclear magnetic resonance scanner

KW - phonetics

KW - priority journal

KW - short term memory

KW - superior longitudinal fasciculus

KW - supramarginal gyrus

KW - tractography

KW - verbal memory

U2 - 10.1002/hbm.23569

DO - 10.1002/hbm.23569

M3 - Article

VL - 38

SP - 3011

EP - 3024

JO - Human Brain Mapping

JF - Human Brain Mapping

SN - 1065-9471

IS - 6

ER -