Dissociation of numbers and objects in corticobasal degeneration and semantic dementia
Abstract
Background: Semantic memory is thought to consist of category-specific representations of knowledge that may be selectively compromised in patients with neurodegenerative diseases, but this has been difficult to demonstrate reliably across object categories.
Methods: The authors evaluated performance on several simple measures requiring number representations (including addition and magnitude judgments of single digits), and on a task that requires object representations (an object naming task) in patients with corticobasal degeneration (CBD; n = 13) and semantic dementia (SD; n = 15). They also examined regional cortical atrophy using voxel-based morphometric analyses of high resolution structural MRI in subgroups of five CBD patients and three SD patients.
Results: CBD patients were consistently more impaired on simple addition and magnitude judgment tasks requiring number representations compared to object representations. Impaired performance with numbers in CBD was associated with cortical atrophy in right parietal cortex. By comparison, SD patients demonstrated a greater impairment on a naming task requiring object representations relative to their performance on measures involving number representations. This was associated with left anterior temporal cortical atrophy.
Conclusion: The cognitive and neuroanatomic dissociations between CBD and SD are consistent with the hypothesis that number and object representations constitute distinct domains in semantic memory, and these domains appear to be associated with distinct neural substrates.
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References
1.
Grossman M, Koenig P. Semantic memory. In: Ramachandran VS, ed. Encyclopedia of cognitive science. San Diego: Academic Press, 2001.
2.
Humphreys GW, Forde EME. Hierarchies, similarity, and interactivity in object recognition: “category-specific” neuropsychological deficits. Behav Brain Sci. 2001; 24: 453–509.
3.
Saffran E, Schwartz MF. Of cabbages and things: semantic memory from a neuropsychological perspective—A tutorial review. In: Umilta C, Moscovitch M, eds. Attention and performance XV: conscious and nonconscious information processing. Cambridge: MIT Press, 1994; 507–536.
4.
Caramazza A. The organization of conceptual knowledge in the brain. In: Gazzaniga MS, ed. The new cognitive neurosciences. Cambridge: MIT Press, 2000; 1037–1046.
5.
Tyler LK, Moss HE. Towards a distributed account of conceptual knowledge. Trends Cogn Sci. 2001; 5: 244–252.
6.
Hodges JR, Patterson K, Oxbury S, Funnell E. Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain. 1992; 115: 1783–1806.
7.
Snowden JS, Goulding PJ, Neary D. Semantic dementia: a form of circumscribed cerebral atrophy. Behav Neurol. 1989; 2: 167–182.
8.
Barbarotto R, Capitani E, Spinnler H, Trivelli C. Slowly progressive semantic impairment with category specificity. Neurocase. 1995; 1: 107–119.
9.
Basso A, Capitani E, Laiacona M. Progressive language impairment without dementia: a case with isolated category-specific semantic impairment. J Neurol Neurosurg Psychiatry. 1988; 51: 1201–1207.
10.
Breedin SD, Saffran EM, Coslett HB. Reversal of a concreteness effect in a patient with semantic dementia. Cogn Neuropsychol. 1995; 11: 617–660.
11.
Warrington EK. The selective impairment of semantic memory. Q J Exp Psychol. 1975; 27: 635–657.
12.
Galton CJ, Patterson K, Graham KS, et al. Differing patterns of temporal atrophy in Alzheimer’s disease and semantic dementia. Neurology. 2001; 57: 216–225.
13.
Mummery CJ, Patterson K, Price CJ, Hodges JR. A voxel-based morphometry study of semantic dementia: relationship between temporal lobe atrophy and semantic memory. Ann Neurol. 2000; 47: 36–45.
14.
Butterworth B. The mathematical brain. London: Macmillan, 1999.
15.
Dehaene S. The number sense. New York, NY: Oxford University Press, 1997.
16.
Cappelletti M, Butterworth B, Kopelman MD. Spared numerical abilities in a case of semantic dementia. Neuropsychologia. 2001; 39: 1224–1239.
17.
Diesfeldt HFA. Progressive decline of semantic memory with preservation of number processing and calculation. Behav Neurol. 1993; 6: 239–242.
18.
Cipolotti L, Butterworth B, Denes G. A specific deficit for numbers in a case of dense acalculia. Brain. 1991; 114: 2619–2637.
19.
Dehaene S, Cohen L. Cerebral pathways for calculation: double dissociation between rote verbal and quantitative knowledge of arithmetic. Cortex. 1997; 33: 219–250.
20.
Rossor MN, Warrington EK, Cipolotti L. The isolation of calculation skills. J Neurol. 1995; 242: 78–81.
21.
Thioux M, Pillon A, Samson D, De Partz M-P, Noel M-P, Seron X. The isolation of numerals at the semantic level. Neurocase. 1998; 4: 371–389.
22.
Halpern C, Clark R, McMillan C, Dennis K, Moore P, Grossman M. Calculation difficulty in neurodegenerative diseases. J Neurol Sci. 2003; 208: 31–38.
23.
Kompoliti K, Goetz CG, Boeve BF, et al. Clinical presentation and pharmacologic therapy in corticobasal degeneration. Arch Neurol. 1998; 55: 957–961.
24.
Stover NP, Watts RL. Corticobasal degeneration. Semin Neurol. 2001; 21: 49–58.
25.
Pillon B, Blin J, Vidailhet M, et al. The neuropsychological pattern of corticobasal degeneration: comparison with progressive supranuclear palsy and Alzheimer’s disease. Neurology. 1995; 45: 1477–1483.
26.
Riley DE, Lang AE, Lewis A, et al. Cortico-basal ganglionic degeneration. Neurology. 1990; 40: 1203–1212.
27.
Caselli RJ, Jack CR. Asymmetric cortical degeneration syndromes: a proposed clinical classification. Arch Neurol. 1992; 49: 770–779.
28.
Savoiardo M, Grisoli M, Girotti F. Magnetic resonance imaging in CBD, related atypical parkinsonian disorders, and dementias. In: Litvan I, Goetz CG, Lang AE, eds. Corticobasal degeneration and related disorders. Philadelphia, PA: Lippincott Williams & Wilkins, 2000; 197–208.
29.
Cohen L, Dehaene S, Chochon F, Lehericy S, Naccache L. Language and calculation within the parietal lobe: a combined cognitive, anatomical and fMRI study. Neuropsychologia. 2001; 38: 1426–1440.
30.
Dellatolas G, Deloche G, Basso A, Claros-Salinas D. Assessment of calculation and number processing using the EC301 battery: cross-cultural normative data and application to left- and right-brain damaged patients. J Int Neuropsychol Soc. 2001; 7: 840–859.
31.
Chochon F, Cohen L, van de Moortele P-F, Dehaene S. Differential contributions of the left and right inferior parietal lobules to number processing. J Cogn Neurosci. 1999; 11: 617–630.
32.
Stanescu-Cosson R, Pinel P, van de Moortele P-F, Le Bihan D, Cohen L, Dehaene S. Understanding dissociations in dyscalculia: a brain imaging study of the impact of number size on the cerebral networks for exact and approximate calculation. Brain. 2000; 123: 2240–2255.
33.
Folstein MF, Folstein SF, 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.
34.
Riley DE, Lang AE. Clinical diagnostic criteria. In: Litvan I, Goetz CG, Lang AE, eds. Corticobasal degeneration and related disorders. Philadelphia: Lippincott Williams & Wilkins, 2000; 29–34.
35.
Forman MS, Zhukareva V, Bergeron CB, et al. Signature tau neuropathology in gray and white matter of corticobasal degeneration. Am J Pathol. 2002; 160: 2045–2053.
36.
The Lund and Manchester Groups. Clinical and neuropathological criteria for frontotemporal dementia. J Neurol Neurosurg Psychiatry. 1994; 57: 416–418.
37.
McKhann G, Trojanowski JQ, Grossman M, Miller BL, Dickson D, Albert M. Clinical and pathological diagnosis of frontotemporal dementia: report of a work group on frontotemporal dementia and Pick’s disease. Arch Neurol. 2001; 58: 1803–1809.
38.
Neary D, Snowden JS, Gustafson L, et al. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology. 1998; 51: 1546–1554.
39.
Lambon Ralph MA, McClelland JL, Patterson K, Galton CJ, Hodges JR. No right to speak? The relationship between object naming and semantic impairment: neuropsychological evidence and a computational model. J Cogn Neurosci. 2001; 13: 341–356.
40.
Snodgrass JG, Vanderwart M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. J Exp Psychol Hum Learning Memory. 1980; 6: 174–214.
41.
Evans AC, Collins DL, Mills SR, Brown ED, Kelly RL, Peters TM. 3D statistical neuroanatomical models from 305 MRI volumes. In: Klaisner LA, ed. Nuclear Science Symposium and Medical Imaging Conference, Volumes 1–3, IEEE Conference Record. San Francisco, CA, 31 October–6. November 1993. Piscataway, NJ: IEEE Service-Center, 1993; 1813–1817.
42.
Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ, Mazziotta JC. Human brain function. San Diego: Academic Press, 1997.
43.
Talairach J, Tournaux P. Co-planar stereotaxic atlas of the human brain. New York: Thieme, 1988.
44.
Rebeiz JJ, Kolodny EH, Richardson EP. Corticodentatonigral degeneration with neuronal achromasia. Arch Neurol. 1968; 18: 20–33.
45.
Frisoni GB, Pizzolato G, Zanetti O, Bianchetti A, Chierichetti F, Trabucchi M. Corticobasal degeneration: neuropsychological assessment and dopamine D2 receptor SPECT analysis. Eur Neurol. 1995; 35: 50–54.
46.
Soliveri P, Monza D, Paridi D. Cognitive and magnetic imaging aspects of corticobasal degeneration and progressive supranuclear palsy. Neurology. 1999; 53: 502–507.
47.
Wenning GK, Litvan I, Jankovic J. Natural history and survival of 14 patients with corticobasal degeneration confirmed at postmortem examination. J Neurol Neurosurg Psychiatry. 1998; 64: 184–189.
48.
Anderson J, Reder L, Lebiere C. Working memory: activation limits on retrieval. Cogn Psychol. 1996; 30: 221–256.
49.
Logie R, Gilhooly KJ, Wynn V. Counting on working memory in arithmetic problem solving. Mem Cogn. 1994; 22: 395–410.
50.
Massman PJ, Kreiter KT, Jankovic J, Doody RS. Neuropsychological functioning in cortical-basal ganglionic degeneration: differentiation from Alzheimer’s disease. Neurology. 1996; 46: 720–726.
51.
Gibb WRG, Luthert PJ, Marsden CD. Corticobasal degeneration. Brain. 1989; 112: 1171–1193.
52.
Rinne JO, Lee MS, Thompson PD, Marsden CD. Corticobasal degeneration: a clinical study of 36 cases. Brain. 1994; 117: 1183–1196.
53.
Kertesz A, Hudson L, Mackenzie IR, Munoz DG. The pathology and nosology of primary progressive aphasia. Neurology. 1994; 44: 2065–2072.
54.
Sakurai Y, Hashida H, Uesugi H. A clinical profile of corticobasal degeneration presenting as primary progressive aphasia. Eur Neurol. 1996; 36: 134–137.
55.
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 (in press).
56.
Luria AR. Higher cortical functions in man. New York: Basic Books, 1966.
57.
Pesenti M, Thioux M, Seron X, de Volder A. Neuroanatomical substrates of arabic number processing, numerical comparison, and simple addition: a PET study. J Cogn Neurosci. 2000; 12: 461–479.
58.
Rickard TC, Romero SG, Basso G, Wharton C, Flitman S, Grafman J. The calculating brain: an fMRI study. Neuropsychologia. 2000; 38: 325–335.
59.
Litvan I, Agid Y, Goetz CG, Jankovic J, Wenning GK, Brandel JP. Accuracy of the clinical diagnosis of corticobasal degeneration: a clinicopathologic study. Neurology. 2001; 48: 119–125.
60.
Ashburner J, Friston K. Voxel-based morphometry: the methods. Neuroimage. 2000; 11: 805–821.
61.
Good CD, Johnsrude IS, Ashburner J, Henson RNA, Friston K, Frackowiak RSJ. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage. 2001; 14: 21–36.
62.
Elfgren C, Brun A, Gustafson L, et al. Neuropsychological tests as discriminators between dementia of Alzheimer type and frontotemporal dementia. Int J Geriatr Psychiatry. 1994; 9: 635–642.
63.
Pachana N, Boone K, Miller BL, Cummings JL, Berman N. Comparison of neuropsychological functioning in Alzheimer’s disease and frontotemporal dementia. J Int Neuropsychol Soc. 1996; 2: 505–510.
64.
Chan D, Fox NC, Scahill RI. Patterns of temporal lobe atrophy in semantic dementia and Alzheimer’s disease. Ann Neurol. 2001; 49: 433–442.
65.
Mummery CJ, Patterson K, Wise RJS, Vandenbergh R, Price CJ, Hodges JR. Disrupted temporal lobe connections in semantic dementia. Brain. 1999; 122: 61–73.
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Received: July 10, 2003
Accepted: December 2, 2003
Published online: April 12, 2004
Published in print: April 13, 2004
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