Abstract
The relationship between verbal-auditory short-term memory (STM) and language is an open area of debate and contrasting hypotheses have been proposed, suggesting either that STM would strongly rely on language-related processes, or that it depends on a dedicated system related to language, but independent from it. In this study we examined 103 patients undergoing surgery for glioma resection in the left or right hemisphere, and we conducted a VLSM analysis on their behavioral performance on auditory-verbal STM, as well as on more general verbal and nonverbal tasks. The aim was to investigate whether the anatomical correlates of auditory-verbal STM were part of the language system or they were spatially segregated from it. VLSM results showed that digit span scores were linked to lesions in both the left supramarginal gyrus and superior-posterior temporal areas, as reported in the literature on patients with a selective deficit of auditory-verbal STM. Conversely, other verbal tasks involved areas only partly overlapping with those found for digit span, with repetition being affected by lesions in more anterior regions in the parietal, temporal, and frontal lobes, and word comprehension by lesions in a network including cortical and subcortical pathways in the temporal lobe. The present results, thus, show that auditory-verbal STM neural correlates are only partially overlapping with those supporting comprehension and production: while the left posterior–superior temporal cortex, involved in speech perception, takes part in both functions, the left supramarginal gyrus has a consistent and specific role only in STM, supporting the hypothesis of interacting but segregated networks.
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References
Ashburner J, Friston KJ (1999) Nonlinear spatial normalization using basis functions. Hum Brain Map 266:1–26
Awh E, Smith EE, Jonides J (1995) Human rehearsal processes and the frontal lobes: PET evidence. Ann N Y Acad Sci 769:97–118. https://doi.org/10.1111/j.1749-6632.1995.tb38134.x
Baddeley AD (1990) The development of the concept of working memory: implications and contributions of neuropsychology. In: Vallar G, Shallice T (eds) Neuropsychological impairments of short-term memory. Cambridge University Press, New York, pp 54–73
Baddeley AD, Hitch G (1974) Working memory. Psychol Learn Motiv 8:47–89
Baldo JV, Schwartz S, Wilkins D, Dronkers NF (2006) Role of frontal versus temporal cortex in verbal fluency as revealed by voxel-based lesion symptom mapping. J Int Neuropsychol Soc 12:896–900
Buchsbaum BR, D’Esposito M (2008) The search for the phonological store: from loop to convolution. J Cognit Neurosci 20:762–778. https://doi.org/10.1162/jocn.2008.20501
Buchsbaum BR, D'Esposito M (2019) A sensorimotor view of verbal working memory. Cortex 112:134–148
Buchsbaum BR, Baldo J, Okada K et al (2011) Conduction aphasia, sensory-motor integration, and phonological short-term memory—an aggregate analysis of lesion and fMRI data. Brain Lang 119:119–128. https://doi.org/10.1016/j.bandl.2010.12.001
Campanella F, Shallice T, Ius T et al (2014) Impact of brain tumour location on emotion and personality: a voxel-based lesion-symptom mapping study on mentalization processes. Brain 137:2532–2545. https://doi.org/10.1093/brain/awu183
Carlesimo GA, Caltagirone C, Gainotti G et al (1996) The mental deterioration battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. Eur Neurol 36:378–384
Cecchetto C, Di Domenico A, Garraffa M, Papagno C (2012) Comprendo. Batteria per la Comprensione di frasi negli adulti. Raffaele, Cortina
Chouiter L, Holmberg J, Manuel AL et al (2016) Partly segregated cortico-subcortical pathways support phonolgic and semantic verbal fluency: a lesion study. Neuroscience 329:275–283. https://doi.org/10.1016/j.neuroscience.2016.05.029
Crinion J, Ashburner J, Leff A et al (2007) Spatial normalization of lesioned brains: performance evaluation and impact on fMRI analyses. Neuroimage 37:866–875. https://doi.org/10.1016/j.neuroimage.2007.04.065
D’Esposito M, Postle BR (2015) The cognitive neuroscience of working memory. Annu Rev Psychol 66:115–142. https://doi.org/10.1146/annurev-psych-010814-015031
Damasio H, Damasio AR (1980) The anatomical basis of conduction aphasia. Brain 103:337–350. https://doi.org/10.1093/brain/103.2.337
De Renzi E, Faglioni P (1965) The comparative efficiency of intelligence and vigilance tests in detecting hemispheric cerebral damage. Cortex 1(4):410–433
De Renzi E, Faglioni P (1978) Normative data and screening power of a shortened version of the Token Test. Cortex 14:41–49
Duffau H, Denvil D, Capelle L (2002) Long term reshaping of language, sensory, and motor maps after glioma resection: a new parameter to integrate in the surgical strategy. J Neurol Neurosurg Psychiatry 72:511–516
Gorno-Tempini ML, Brambati SM, Ginex V et al (2008) The logopenic/phonological variant of primary progressive aphasia. Neurology 71:1227–1234. https://doi.org/10.1212/01.wnl.0000320506.79811.da
Henry JD, Crawford JR (2004) A meta-analytic review of verbal fluency performance following focal cortical lesions. Neuropsychology 18:284–295. https://doi.org/10.1037/0894-4105.18.2.284
Henson RNA, Burgess N, Frith CD (2000) Recoding, storage, rehersal, and grouping in verbal short-term memory: an fMRI study. Neuropsychologia 38:426–440. https://doi.org/10.1016/S0028-3932(99)00098-6
Hurlstone MJ, Hitch GJ, Baddeley AD (2014) Memory for serial order across domains: an overview of the literature and directions for future research. Psychol Bull 140:339–373. https://doi.org/10.1037/a0034221
Karnath H-O, Rennig J (2017) Investigating structure and function in the healthy human brain: validity of acute versus chronic lesion-symptom mapping. Brain Struct Funct 222:2059–2070. https://doi.org/10.1007/s00429-016-1325-7
Karnath H-O, Steinbach JP (2011) Do brain tumours allow valid conclusions on the localisation of human brain functions? Objections. Cortex 47:1004–1006. https://doi.org/10.1016/j.cortex.2010.08.006
Kinkingnéhun S, Volle E, Pélégrini-Issac M et al (2007) A novel approach to clinical-radiological correlations: anatomo-Clinical Overlapping Maps (AnaCOM): method and validation. Neuroimage 37:1237–1249. https://doi.org/10.1016/j.neuroimage.2007.06.027
Koenigs M, Acheson DJ, Barbey AK et al (2011) Areas of left perisylvian cortex mediate auditory-verbal short-term memory. Neuropsychologia 49:3612–3619. https://doi.org/10.1016/j.neuropsychologia.2011.09.013
Leff AP, Schofield TM, Crinion JT et al (2009) The left superior temporal gyrus is a shared substrate for auditory short-term memory and speech comprehension: evidence from 210 patients with stroke. Brain 132:3401–3410. https://doi.org/10.1093/brain/awp273
Martin N, Saffran EM (1997) Language and auditory-verbal short-term memory impairments: evidence for common underlying processes. Cognit Neuropsychol 14:641–682. https://doi.org/10.1080/026432997381402
Mattavelli G, Pisoni A, Casarotti A et al (2019) Consequences of brain tumour resection on emotion recognition. J Neuropsychol 13:1–21. https://doi.org/10.1111/jnp.12130
Miceli G, Laudanna A, Burani C, Capasso R (1994) Batteria per l’analisi dei deficit afasici. Cepsag, Roma
Monaco M, Costa A, Caltagirone C, Carlesimo GA (2013) Forward and backward span for verbal and visuo-spatial data: standardization and normative data from an Italian adult population. Neurol Sci 34:749–754. https://doi.org/10.1007/s10072-012-1130-x
Newhart M, Trupe LA, Gomez Y et al (2012) Ischemia in Broca’s area versus angular gyrus. Cortex 48:1288–1297. https://doi.org/10.1016/j.cortex.2011.09.009.Asyntactic
Newton AM, De Villiers JG (2007) While talking thinking. Psychol Sci 18:574–579. https://doi.org/10.1111/j.1467-9280.2007.01942.x
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113. https://doi.org/10.1016/0028-3932(71)90067-4
Orsini A, Grossi D, Capitani E, Laiacona M (1987) Verbal and spatial immediate memory span: normative data from 1335 item sand 112 children. Ital J Neurol Sci 8:537–548
Papagno C, Cecchetto C (2019) Is STM involved in sentence comprehension? Cortex 112:80–90. https://doi.org/10.1016/j.cortex.2018.08.028
Papagno C, Miracapillo C, Casarotti A et al (2011) What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain 134:405–414. https://doi.org/10.1093/brain/awq283
Papagno C, Comi A, Riva M, Bello L (2012) Measuring clinical outcomes in neuro-oncology. A battery to evaluate low-grade gliomas (LGG). J Neuro-oncol 108:269–275. https://doi.org/10.1007/s11060-012-0824-5
Papagno C, Comi A, Riva M et al (2017) Mapping the brain network of the phonological loop. Hum Brain Map 38:3011–3024. https://doi.org/10.1002/hbm.23569
Paulesu E, Frith CD, Frackowiak RSJ (1993) The neural correlates of the verbal component of the working memory. Nature 362:342–345
Petrides M, Alivisatos B, Meyer E, Evans AC (1993) Functional activation of the human frontal cortex during the performance of verbal working memory tasks. Proc Nat Acad Sci 90(3):878–882
Pettigrew C, Hillis AE (2014) Role for memory capacity in sentence comprehension: evidence from acute stroke. Aphasiology 28:1258–1280. https://doi.org/10.1080/02687038.2014.919436
Pisoni A, Mattavelli G, Casarotti A et al (2018) Object-action dissociation: a voxel-based lesion-symptom mapping study on 102 patients after glioma removal. NeuroImage Clin 18:986–995. https://doi.org/10.1016/j.nicl.2018.03.022
Poeppel D (1996) A critical review of PET studies of phonological processing. Brain Lang 55:317–385. https://doi.org/10.1006/brln.1996.0108
Romero L, Walsh V, Papagno C (2006) The neural correlates of phonological short-term memory: a repetitive transcranial magnetic stimulation study. J Cognit Neurosci 18:1147–1155. https://doi.org/10.1162/jocn.2006.18.7.1147
Rorden C, Fridriksson J, Karnath HO (2009) An evaluation of traditional and novel tools for lesion behavior mapping. Neuroimage 44:1355–1362. https://doi.org/10.1016/j.neuroimage.2008.09.031
Shallice T, Papagno C (2019) Impairments of auditory-verbal short-term memory: do selective deficits of the input phonological buffer exist? Cortex 112:107–121. https://doi.org/10.1016/j.cortex.2018.10.004
Smith JS, Chang EF, Lamborn KR et al (2008) Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:1338–1345. https://doi.org/10.1200/JCO.2007.13.9337
Vallar G, Papagno C (2002) Neuropsychological impairments of short-term memory. In: Baddeley AD, Kopelman M, Wilson B (eds) Handbook of memory disorders. Wiley, Chichester, pp 249–270
Vallar G, DiBetta AM, Silveri C (1997) The phonological short-term storage-rehearsal system: patterns of impairment and neural correlates. Neuropsychologia 35:795–812
Warrington EK, Logue V, Pratt RTC (1971) The anatomical localisation of selective impairment of auditory verbal short-term memory. Neuropsychologia 9:377–387. https://doi.org/10.1016/0028-3932(71)90002-9
Yue Q, Martin RC, Hamilton AC, Rose NS (2018) Non-perceptual regions in the left inferior parietal lobe support phonological short-term memory: evidence for a buffer account? Cereb Cortex 29:1398–1413. https://doi.org/10.1093/cercor/bhy037
Zamora L, Corina D, Ojemann G (2016) Human temporal cortical single neuron activity during working memory maintenance. Neuropsychologia 86:1–12. https://doi.org/10.1016/j.neuropsychologia.2016.04.004
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Alberto Pisoni and Giulia Mattavelli equally contributed to the paper.
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Pisoni, A., Mattavelli, G., Casarotti, A. et al. The neural correlates of auditory-verbal short-term memory: a voxel-based lesion-symptom mapping study on 103 patients after glioma removal. Brain Struct Funct 224, 2199–2211 (2019). https://doi.org/10.1007/s00429-019-01902-z
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DOI: https://doi.org/10.1007/s00429-019-01902-z