Neural correlates of lexical-semantic memory: A voxel-based morphometry study in mild AD, aMCI and normal aging

Balthazar, Marcio L.F.; Yasuda, Clarissa L.; Lopes, Tátila M.; Pereira, Fabrício R.S.; Damasceno, Benito Pereira; Cendes, Fernando

doi:10.1590/S1980-57642011DN05020003

Abstract

Neuroanatomical correlations of naming and lexical-semantic memory are not yet fully understood. The most influential approaches share the view that semantic representations reflect the manner in which information has been acquired through perception and action, and that each brain area processes different modalities of semantic representations. Despite these anatomical differences in semantic processing, generalization across different features that have similar semantic significance is one of the main characteristics of human cognition.

Methods:

We evaluated the brain regions related to naming, and to the semantic generalization, of visually presented drawings of objects from the Boston Naming Test (BNT), which comprises different categories, such as animals, vegetables, tools, food, and furniture. In order to create a model of lesion method, a sample of 48 subjects presenting with a continuous decline both in cognitive functions, including naming skills, and in grey matter density (GMD) was compared to normal young adults with normal aging, amnestic mild cognitive impairment (aMCI) and mild Alzheimer's disease (AD). Semantic errors on the BNT, as well as naming performance, were correlated with whole brain GMD as measured by voxel-based morphometry (VBM).

Results:

The areas most strongly related to naming and to semantic errors were the medial temporal structures, thalami, superior and inferior temporal gyri, especially their anterior parts, as well as prefrontal cortices (inferior and superior frontal gyri).

Conclusion:

The possible role of each of these areas in the lexical-semantic networks was discussed, along with their contribution to the models of semantic memory organization.

Key words:
semantic memory; naming; voxel-based morphometry; Alzheimer's disease; mild cognitive impairment.

Resumo

As correlações neuroanatômicas de nomeação e memória lexical-semântica não são totalmente entendidas. As abordagens mais influentes compartilham a idéia de que representações refletem a maneira na qual a informação foi adquirida por meio da percepção e ação e que cada área do cérebro processa diferentes modalidades de representações semânticas. Apesar destas diferenças anatômicas no processamento semântico, a generalização de diferentes aspectos que tem significância semântica análoga é uma das principais características da cognição humana.

Métodos:

Nós avaliamos as regiões cerebrais relacionadas à nomeação e à generalização semântica de desenhos de objetos visualmente apresentados do Teste de Nomeação de Boston (TNB), que compreende diferentes categorias, como animais, vegetais, utensílios, comida e móveis. Para criar um modelo de método de lesão, nós investigamos uma amostra de 48 pessoas que demonstraram um declínio contínuo em funções cognitivas, incluindo habilidades de nomeação e em densidade de substância cinzenta (DSC) em relação a adultos jovens: envelhecimento normal, comprometimento cognitivo leve amnéstico (CCLa) e doença de Alzheimer (DA). Nós correlacionamos seus erros semânticos no TNB, assim como seus desempenhos de nomeação, com a DSC de todo o cérebro que foi medido por morfometria baseada em vóxel (MBV).

Resultados:

As áreas que mais se relacionaram à nomeação e aos erros semânticos foram as estruturas mediais temporais, tálamo, giro temporal superior e inferior, especialmente em suas partes anteriores e os córtices pré-frontais (giro frontal inferior e superior).

Conclusão:

Discutimos o provável papel de cada uma dessas áreas na rede lexical-semântica e sua contribuição para os modelos de organização semântica.

Palavras-chave:
memória semântica; nomeação; morfometria baseada em voxel; doença de Alzheimer; comprometimento cognitivo leve.

Texto completo disponível apenas em PDF.

Full text available only in PDF format.

References

Luria AR. The word and its semantic structure. In: Thought and language: the Luria's last conferences. Porto Alegre: Artes Médicas; 1986:27-28.
McClelland JL, Rumelhart DE. Distributed memory and the representation of general and specific information. J Exp Psychol Gen 1985;114:159-197.
Hart Jr, Kraut MA. Neural hybrid model of semantic object memory (version 1.1). In: Hart Jr J, Kraut MA (Eds). Neural basis of semantic memory. Cambridge: Ed. Cambridge University Press; 2007:331-353.
Hodges JR, Graham N, Patterson K. Charting the progression in semantic dementia: implications for the organisation of semantic memory. Memory 1995;3:463-495.
Patterson K, Nestor PJ, Rogers TT. Where do you know what you know? The representation of semantic knowledge in the human brain. Nat Rev Neurosci 2007;8:976-987.
Martin A, Chao LL. Semantic memory and the brain: structure and processes. Curr Opin Neurobiol 2001;11:194-201.
Albert MS, Heller HS, Milberg W. Changes in naming ability with age. Psychol Aging 1988;3:173-178.
LaBarge E, Edwards D, Knesevich JW. Performance of normal elderly on the Boston Naming Test. Brain Lang 1986;27:380-384.
Zec RF, Markwell SJ, Burkett NR, Larsen DL. A longitudinal study of confrontation naming in the "normal" elderly. J Int Neuropsychol Soc 2005;11:716-726.
Adlam AL, Bozeat S, Arnold R, Watson P, Hodges JR. Semantic knowledge in mild cognitive impairment and mild Alzheimer's disease. Cortex 2006;42:675-684.
Dudas RB, Clague F, Thompson SA, Graham KS, Hodges JR. Episodic and semantic memory in mild cognitive impairment. Neuropsychologia 2005;43:1266-1276.
Winblad B, Palmer K, Kivipelto M, et al. Mild cognitive impairment--beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Int Med 2004;256:240-246.
Kaplan EF, Goodglass H, Weintraub S. The Boston Naming Test. 2nd edition. Philadelphia: Lea and Febiger; 1983.
Morris JC. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 1993;43:2412-2414.
McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984;34:939-944.
Folstein MF, Folstein SE, McHugh PR. "Mini-mental state": a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189-198.
Brucki SM, Nitrini R, Caramelli P, Bertolucci PH, Okamoto IH. Suggestions for utilization of the mini-mental state examination in Brazil. Arq Neuropsiquiatr 2003;61:777-781.
Rey A. Clinical examination in psychology. Paris: Press Universitaire de France; 1964.
Roth M, Huppert FA, Tym E, Mountjoy CQ. CAMDEX: The Cambridge Examination for Mental Disorders of the Elderly. Cambridge: Cambridge University Press; 1988.
Christensen A-L. Luria's Neuropsychological Investigation. Copenhagen: Munksgaard; 1979:203.
Wechsler D. Manual for the Wechsler Memory Scale-Revised (WMS-R). San Antonio: The Psychological Corporation; 1987.
Alexopoulos GS, Abrams RC, Young RC, Shamoian CA. Cornell Scale for Depression in Dementia. Biological Psychiatry 1988;23:271-284.
Carthery-Goulart MT, Areza-Fegyveres R, Schultz RR, et al. Brazilian version of the Cornell depression scale in dementia. Arq Neuropsiquiatr 2007;65:912-915.
Ashburner J, Friston KJ. Unified segmentation. NeuroImage 2005;26:839-851.
Bergougnian L, Chupin M, Czechowska Y, et al. Can voxel based morphometry, manual segmentation and automated segmentation equally detect hippocampal volume differences in acute depression? Neuroimage 2009;45:29-37.
Rorden C, Fridriksson J, Karnath HO. An evaluation of traditional and novel tools for lesion behavior mapping. Neuroimage 2009;44:1355-1362.
Balthazar ML, Cendes F, Damasceno BP. Semantic error patterns on The Boston Naming Test in normal aging, amnestic mild cognitive impairment and mild Alzheimer's disease: is there semantic disruption? Neuropsychology 2008;22:703-709.
Tulving E. Multiple memory systems and consciousness. Hum Neurobiol 1987;6:67-80.
Squire LR, Knowlton B, Musen G. The structure and organization of memory. Ann Rev Psychol 1993;44:453-495.
Gabrieli JD, Cohen NJ, Corkin S. The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection. Brain Cog 1988;7:157-177.
Venneri A, McGeown WJ, Hietanen HM, Guerrini C, Ellis AW, Shanks MF. The anatomical bases of semantic retrieval deficits in early Alzheimer's disease. Neuropsychologia 2008;46:497-510.
Slotnick SD, Moo LR, Kraut MA, Lesser RP, Hart J Jr. Interactions between thalamic and cortical rhythms during semantic memory recall in human. Proc Natl Acad Sci USA 2002; 99:6440-6443.
Kraut MA, Calhoun V, Pitcock JA, Cusick C, Hart J Jr. Neural hybrid model of semantic object memory: implications from event-related timing using fMRI. J Int Neuropsychol Soc 2003;9:1031-1040.
Damasio H, Grabowski TJ, Tranel D, Hichwa RD, Damasio AR. A neural basis for lexical retrieval. Nature 1996;380:499-505.
Gorno-Tempini ML, Price CJ, Josephs O, et al. The neural systems sustaining face and proper-name processing. Brain 1998;121:2103-2118.
Damasio H, Tranel D, Grabowski T, Adolphs R, Damasio A. Neural systems behind word and concept retrieval. Cognition 2004;92:179-229.
Grossman M, McMillan C, Moore P, et al. What's in a name: voxel-based morphometric analyses of MRI and naming difficulty in Alzheimer's disease, frontotemporal dementia and corticobasal degeneration. Brain 2004;127:628-649.
Mummery CJ, Patterson K, Price CJ, Ashburner J, Frackowiak RS, Hodges JR. A voxel-based morphometry study of semantic dementia: relationship between temporal lobe atrophy and semantic memory. Ann Neurol 2000;47:36-45.
Gabrieli JD, Cohen NJ, Corkin S. The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection. Brain Cog 1988;7:157-177.
Devlin JT, Russell RP, Davis MH, et al. Is there an anatomical basis for category-specificity? Semantic memory studies in PET and fMRI. Neuropsychologia 2002;40:54-75.
Thompson-Schill SL, Swick D, Farah MJ, D'Esposito M, Kan IP, Knight RT. Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. Proc Natl Acad Sci USA 1998;95:15855-15860.
Vandenberghe R, Price C, Wise R, Josephs O, Frackowiak RS. Functional anatomy of a common semantic system for words and pictures. Nature 1996;383:254-256.
Thompson-Schill SL, D'Esposito M, Aguirre DK, Farah MJ. Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a re-evaluation. Proc Natl Acad Sci USA 1997;94: 14792-14797.
Baldo JV, Shimamura AP. Letter and category fluency in patients with frontal lobe lesions. Neuropsychology 1998;12: 259-267.
Fiez JA, Raichle ME, Miezin FM, Pettersen SE, Tallal P, Katz WF. PET studies of auditory and phonological processing: Effects of stimulus characteristics and task design. J Cog Neurosc 1995;7:357-375.
Poldrack RA, Wagner AD, Prull MW, Desmond JE, Glover GH, Gabrieli JD. Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex. Neuroimage 1999;10:15-35.
Gold BT, Balota DA, Kirchhoff BA, Buckner RL. Common and dissociable activation patterns associated with controlled semantic and phonological processing: evidence from FMRI adaptation. Cereb Cortex 2005;15:1438-1450.
Snyder HR, Feigenson K, Thompson-Schill SL. Prefrontal cortical response to conflict during semantic and phonological tasks. J Cog Neurosci 2007;19:761-775.

Publication Dates

Publication in this collection
Apr-Jun 2011

History

Received
08 Feb 2011
Accepted
22 Apr 2011

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] Luria AR. The word and its semantic structure. In: Thought and language: the Luria's last conferences. Porto Alegre: Artes Médicas; 1986:27-28.

[2] McClelland JL, Rumelhart DE. Distributed memory and the representation of general and specific information. J Exp Psychol Gen 1985;114:159-197.

[3] Hart Jr, Kraut MA. Neural hybrid model of semantic object memory (version 1.1). In: Hart Jr J, Kraut MA (Eds). Neural basis of semantic memory. Cambridge: Ed. Cambridge University Press; 2007:331-353.

[4] Hodges JR, Graham N, Patterson K. Charting the progression in semantic dementia: implications for the organisation of semantic memory. Memory 1995;3:463-495.

[5] Patterson K, Nestor PJ, Rogers TT. Where do you know what you know? The representation of semantic knowledge in the human brain. Nat Rev Neurosci 2007;8:976-987.

[6] Martin A, Chao LL. Semantic memory and the brain: structure and processes. Curr Opin Neurobiol 2001;11:194-201.

[7] Albert MS, Heller HS, Milberg W. Changes in naming ability with age. Psychol Aging 1988;3:173-178.

[8] LaBarge E, Edwards D, Knesevich JW. Performance of normal elderly on the Boston Naming Test. Brain Lang 1986;27:380-384.

[9] Zec RF, Markwell SJ, Burkett NR, Larsen DL. A longitudinal study of confrontation naming in the "normal" elderly. J Int Neuropsychol Soc 2005;11:716-726.

[10] Adlam AL, Bozeat S, Arnold R, Watson P, Hodges JR. Semantic knowledge in mild cognitive impairment and mild Alzheimer's disease. Cortex 2006;42:675-684.

[11] Dudas RB, Clague F, Thompson SA, Graham KS, Hodges JR. Episodic and semantic memory in mild cognitive impairment. Neuropsychologia 2005;43:1266-1276.

[12] Winblad B, Palmer K, Kivipelto M, et al. Mild cognitive impairment--beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Int Med 2004;256:240-246.

[13] Kaplan EF, Goodglass H, Weintraub S. The Boston Naming Test. 2nd edition. Philadelphia: Lea and Febiger; 1983.

[14] Morris JC. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 1993;43:2412-2414.

[15] McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984;34:939-944.

[16] Folstein MF, Folstein SE, McHugh PR. "Mini-mental state": a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189-198.

[17] Brucki SM, Nitrini R, Caramelli P, Bertolucci PH, Okamoto IH. Suggestions for utilization of the mini-mental state examination in Brazil. Arq Neuropsiquiatr 2003;61:777-781.

[18] Rey A. Clinical examination in psychology. Paris: Press Universitaire de France; 1964.

[19] Roth M, Huppert FA, Tym E, Mountjoy CQ. CAMDEX: The Cambridge Examination for Mental Disorders of the Elderly. Cambridge: Cambridge University Press; 1988.

[20] Christensen A-L. Luria's Neuropsychological Investigation. Copenhagen: Munksgaard; 1979:203.

[21] Wechsler D. Manual for the Wechsler Memory Scale-Revised (WMS-R). San Antonio: The Psychological Corporation; 1987.

[22] Alexopoulos GS, Abrams RC, Young RC, Shamoian CA. Cornell Scale for Depression in Dementia. Biological Psychiatry 1988;23:271-284.

[23] Carthery-Goulart MT, Areza-Fegyveres R, Schultz RR, et al. Brazilian version of the Cornell depression scale in dementia. Arq Neuropsiquiatr 2007;65:912-915.

[24] Ashburner J, Friston KJ. Unified segmentation. NeuroImage 2005;26:839-851.

[25] Bergougnian L, Chupin M, Czechowska Y, et al. Can voxel based morphometry, manual segmentation and automated segmentation equally detect hippocampal volume differences in acute depression? Neuroimage 2009;45:29-37.

[26] Rorden C, Fridriksson J, Karnath HO. An evaluation of traditional and novel tools for lesion behavior mapping. Neuroimage 2009;44:1355-1362.

[27] Balthazar ML, Cendes F, Damasceno BP. Semantic error patterns on The Boston Naming Test in normal aging, amnestic mild cognitive impairment and mild Alzheimer's disease: is there semantic disruption? Neuropsychology 2008;22:703-709.

[28] Tulving E. Multiple memory systems and consciousness. Hum Neurobiol 1987;6:67-80.

[29] Squire LR, Knowlton B, Musen G. The structure and organization of memory. Ann Rev Psychol 1993;44:453-495.

[30] Gabrieli JD, Cohen NJ, Corkin S. The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection. Brain Cog 1988;7:157-177.

[31] Venneri A, McGeown WJ, Hietanen HM, Guerrini C, Ellis AW, Shanks MF. The anatomical bases of semantic retrieval deficits in early Alzheimer's disease. Neuropsychologia 2008;46:497-510.

[32] Slotnick SD, Moo LR, Kraut MA, Lesser RP, Hart J Jr. Interactions between thalamic and cortical rhythms during semantic memory recall in human. Proc Natl Acad Sci USA 2002; 99:6440-6443.

[33] Kraut MA, Calhoun V, Pitcock JA, Cusick C, Hart J Jr. Neural hybrid model of semantic object memory: implications from event-related timing using fMRI. J Int Neuropsychol Soc 2003;9:1031-1040.

[34] Damasio H, Grabowski TJ, Tranel D, Hichwa RD, Damasio AR. A neural basis for lexical retrieval. Nature 1996;380:499-505.

[35] Gorno-Tempini ML, Price CJ, Josephs O, et al. The neural systems sustaining face and proper-name processing. Brain 1998;121:2103-2118.

[36] Damasio H, Tranel D, Grabowski T, Adolphs R, Damasio A. Neural systems behind word and concept retrieval. Cognition 2004;92:179-229.

[37] Grossman M, McMillan C, Moore P, et al. What's in a name: voxel-based morphometric analyses of MRI and naming difficulty in Alzheimer's disease, frontotemporal dementia and corticobasal degeneration. Brain 2004;127:628-649.

[38] Mummery CJ, Patterson K, Price CJ, Ashburner J, Frackowiak RS, Hodges JR. A voxel-based morphometry study of semantic dementia: relationship between temporal lobe atrophy and semantic memory. Ann Neurol 2000;47:36-45.

[39] Gabrieli JD, Cohen NJ, Corkin S. The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection. Brain Cog 1988;7:157-177.

[40] Devlin JT, Russell RP, Davis MH, et al. Is there an anatomical basis for category-specificity? Semantic memory studies in PET and fMRI. Neuropsychologia 2002;40:54-75.

[41] Thompson-Schill SL, Swick D, Farah MJ, D'Esposito M, Kan IP, Knight RT. Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. Proc Natl Acad Sci USA 1998;95:15855-15860.

[42] Vandenberghe R, Price C, Wise R, Josephs O, Frackowiak RS. Functional anatomy of a common semantic system for words and pictures. Nature 1996;383:254-256.

[43] Thompson-Schill SL, D'Esposito M, Aguirre DK, Farah MJ. Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a re-evaluation. Proc Natl Acad Sci USA 1997;94: 14792-14797.

[44] Baldo JV, Shimamura AP. Letter and category fluency in patients with frontal lobe lesions. Neuropsychology 1998;12: 259-267.

[45] Fiez JA, Raichle ME, Miezin FM, Pettersen SE, Tallal P, Katz WF. PET studies of auditory and phonological processing: Effects of stimulus characteristics and task design. J Cog Neurosc 1995;7:357-375.

[46] Poldrack RA, Wagner AD, Prull MW, Desmond JE, Glover GH, Gabrieli JD. Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex. Neuroimage 1999;10:15-35.

[47] Gold BT, Balota DA, Kirchhoff BA, Buckner RL. Common and dissociable activation patterns associated with controlled semantic and phonological processing: evidence from FMRI adaptation. Cereb Cortex 2005;15:1438-1450.

[48] Snyder HR, Feigenson K, Thompson-Schill SL. Prefrontal cortical response to conflict during semantic and phonological tasks. J Cog Neurosci 2007;19:761-775.

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