Patterns of brain atrophy in frontotemporal dementia and semantic dementia
Abstract
Objective: To identify and compare the patterns of cerebral atrophy associated with two clinical variants of frontotemporal lobar degeneration (FTLD): frontotemporal dementia (FTD) and semantic dementia (SemD).
Methods: Twenty patients with FTLD were classified as having FTD (N = 8) or SemD (N = 12) based on current clinical criteria. Both groups showed a similar spectrum of behavioral abnormalities, as indicated by the neuropsychiatric inventory. T1-weighted MRI was obtained for each patient and 20 control subjects. The regions of focal gray matter tissue loss associated with both FTD and SemD, as well as those differing between the two groups were examined using voxel-based morphometry.
Results: Regions of significant atrophy seen in both groups were located in the ventromedial frontal cortex, the posterior orbital frontal regions bilaterally, the insula bilaterally, and the left anterior cingulate cortex. The FTD, but not the SemD, group showed atrophy in the right dorsolateral frontal cortex and the left premotor cortex. The SemD, but not the FTD, group showed tissue loss in the anterior temporal cortex and the amygdala/anterior hippocampal region bilaterally.
Conclusions: Although FTD and SemD are associated with different overall patterns of brain atrophy, regions of gray matter tissue loss in the orbital frontal, insular, and anterior cingulate regions are present in both groups. The authors suggest that pathology in the areas of atrophy associated with both FTD and SemD may underlie some the behavioral symptoms seen in the two disorders.
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References
1.
Brun A, Englund B, Gustafson L, et al. Clinical and neuropathological criteria for frontotemporal dementia. J Neurol Neurosurg Psychiatry . 1994; 57: 416–418.
2.
Neary D, Snowden JS, Gustafson L, et al. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology . 1998; 51: 1546–1554.
3.
Neary D, Snowden JS, Mann DM. The clinical pathological correlates of lobar atrophy. Dementia . 1993; 4: 154–159.
4.
Edwards-Lee T, Miller BL, Benson DF, et al. The temporal variant of frontotemporal dementia. Brain . 1997; 120: 1027–1040.
5.
Boone KB, Miller BL, Lee A, Berman N, Sherman D, Stuss DT. Neuropsychological patterns in right versus left frontotemporal dementia. J Int Neuropsychol Soc . 1999; 5: 616–622.
6.
Snowden JS, Goulding PJ, Neary D. Semantic dementia: a form of circumscribed cerebral atrophy. Behavioural Neurology . 1989; 2: 167–182.
7.
Hodges JR, Patterson K, Oxbury S, Funnell E. Semantic dementia. Progressive fluent aphasia with temporal lobe atrophy. Brain . 1992; 115: 1783–1806.
8.
Mummery C, Patterson K, Price C, Ashburner J, Frackowiak R, Hodges J. A voxel-based morphometry study of semantic dementia: relationship between temporal lobe atrophy and semantic memory. Ann Neurol . 2000; 47: 36–45.
9.
Galton CJ, Patterson K, Graham K, et al. Differing patterns of temporal atrophy in Alzheimer’s disease and semantic dementia. Neurology . 2001; 56: 216–225.
10.
Chan D, Fox NC, Scahill RI, et al. Patterns of temporal lobe atrophy in semantic dementia and Alzheimer’s disease. Ann Neurol . 2001; 49: 433–442.
11.
Perry RJ, Hodges JR. Differentiating frontal and temporal variant frontotemporal dementia from Alzheimer’s disease. Neurology 2000;54:2277–2284.
12.
Bozeat S, Gregory CA, Ralph MA, Hodges JR. Which neuropsychiatric and behavioural features distinguish frontal and temporal variants of frontotemporal dementia from Alzheimer’s disease? J Neurol Neurosurg Psychiatry 2000;69:178–186.
13.
Vandenberghe R, Price C, Wise R, Josephs O, Frackowiak RSJ. Functional anatomy of a common semantic system for words and pictures. Nature . 1996; 383: 254–256.
14.
Gorno–Tempini ML, Price CJ, Josephs O, et al. The neural systems sustaining face and proper-name processing. Brain . 1998; 121: 2103–2118.
15.
Fukui T, Kertesz A. Volumetric study of lobar atrophy in Pick complex and Alzheimer’s disease. Journal of Neurol Sci . 2000; 174: 111–121.
16.
Ashburner J, Friston KJ. Voxel-based morphometry–the methods. Neuroimage . 2000; 11: 805–821.
17.
Eslinger PJ. Orbital frontal cortex: historical and contemporary views about its behavioral and physiological significance. An introduction to special topic papers: part I. Neurocase . 1999; 5: 225–229.
18.
Galton CJ, Patterson K, Xuereb JH, Hodges JR. Atypical and typical presentations of Alzheimer’s disease: a clinical, neuropsychological, neuroimaging and pathological study of 13 cases. Brain 2000;123 Pt 3:484–498.
19.
Read SL, Miller BL, Mena I, Kim R, Itabashi H, Darby A. SPECT in dementia: clinical and pathological correlation. J Am Geriatr Soc . 1995; 43: 1243–1247.
20.
Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the mental state of patients for the clinician. J Psychiat Res . 1975; 12: 189–198.
21.
Delis DC, Lucas JA, Kopelman MD. Memory. In: Fogel BS, Schiffer RB, Rao SM, eds. Synopsis of neuropsychiatry. Philadelphia: Lippincott, Williams & Wilkins; 2000:169–191.
22.
Kaplan E, Goodglass H, Wintraub S. The Boston Naming Test. Philadelphia: Lea and Febiger, 1983.
23.
Reitan RM. Validity of the Trailmaking Test as an indication of organic brain damage. Percept Mot Skills . 1958; 8: 271–276.
24.
Cummings JL. The Neuropsychiatric Inventory. Assessing psychopathology in dementia patients. Neurology . 1997; 48: S10–16.
25.
Levy ML, Miller BL, Cummings JL, Fairbanks LA, Craig A. Alzheimer disease and frontotemporal dementias. Behavioral distinctions. Arch Neurol . 1996; 53: 687–690.
26.
Evans AC, Kamber M, Collins DL, Macdonald D. An MRI-based probabilistic atlas of neuroanatomy. In: Shorvon S, Fish D, Andermann F, Bydder GM, Stefan H, eds. Magnetic resonance scanning and epilepsy: Plenum Press; 1994:263–274.
27.
Ashburner J, Friston K. Multimodal image coregistration and partitioning–a unified framework. Neuroimage . 1997; 6: 209–217.
28.
Friston K, Holmes A, Worsley K, Poline J-P, Frith C, Frackowiak R. Statistical parametric map in functional imaging: a general linear approach. Hum Brain Mapp . 1995; 2: 189–210.
29.
Duvornoy HM. The human brain. Surface, three-dimensional sectional anatomy with MRI, and blood supply. New York: Springer-Verlag Wein; 1999.
30.
Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human brain: 3-Dimensional proportional system; an approach to cerebral imaging. Stuttgart: George Thieme Verlag; 1988.
31.
Rylander G. Personality changes after operations on the frontal lobes. Acta Psychiatr Scand (suppl) 1939; 20.
32.
Eslinger PJ, Damasio AR. Severe disturbance of higher cognition after bilateral frontal lobe ablation: patient EVR. Neurology . 1985; 35: 1731–1741.
33.
Damasio H, Grabowski T, Frank R, Galaburda AM, Damasio AR. The return of Phineas Gage: clues about the brain from the skull of a famous patient. Science . 1994; 264: 1102–1105.
34.
Rolls ET, Hornak J, Wade D, McGrath J. Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J Neurol Neurosurg Psychiatry . 1994; 57: 1518–1524.
35.
Bechara A, Tranel D, Damasio H, Damasio AR. Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. Cereb Cortex . 1996; 6: 215–225.
36.
Rolls ET. The orbitofrontal cortex and reward. Cereb Cortex . 2000; 10: 284–294.
37.
Saver JL, Damasio AR. Preserved access and processing of social knowledge in a patient with acquired sociopathy due to ventromedial frontal damage. Neuropsychologia . 1991; 29: 1241–1249.
38.
Miller BL, Darby A, Benson DF, Cummings JL, Miller MH. Aggressive, socially disruptive and antisocial behaviour associated with fronto-temporal dementia. Br J Psychiatry . 1997; 170: 150–154.
39.
Chui H, Willis L. Vascular diseases of the frontal lobes. In: Miller BL, Cummings JL, eds. The human frontal lobes. New York: Guilford; 1999: 370–401.
40.
Shima K, Tanji J. Role for cingulate motor area cells in voluntary movement selection based on reward. Science . 1998; 282: 1335–1338.
41.
Graybiel AM, Rauch SL. Toward a neurobiology of obsessive-compulsive disorder. Neuron . 2002; 28: 343–347.
42.
Mendez MF, Perryman KM, Miller BL, Swartz JR, Cummings JL. Compulsive behaviors as presenting symptoms of frontotemporal dementia. J Geriatr Psychiatry Neurol . 1997; 10: 154–157.
43.
Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 1996;22:229–244.
44.
Critchley HD, Elliott R, Mathias CJ, Dolan RJ. Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study. J Neurosci . 2000; 20: 3033–3040.
45.
Damasio AR. The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philosophical Transactions of the Royal Society of London, Series B. Biological Sciences . 1996; 351: 1413–1420.
46.
Dronkers NF. A new brain region for coordinating speech articulation. Nature . 1996; 384: 159–161.
47.
Lavenu I, Pasquier F, Lebert F, Petit H, Van der Linden M. Perception of emotion in frontotemporal dementia and Alzhei-mer disease. Alzheimer Dis Assoc Disord . 1999; 13: 96–101.
48.
Snowden JS, Bathgate D, Varma A, Blackshaw A, Gibbons ZC, Neary D. Distinct behavioural profiles in frontotemporal dementia and semantic dementia. J Neurol Neurosurg Psychiatry . 2001; 70: 323–332.
49.
Perry RJ, Rosen HR, Kramer JH, Beer JS, Levenson RL, Miller BL. Hemispheric dominance for emotions, empathy and social behaviour: evidence from right and left handers with frontotemporal dementia. Neurocase . 2001; 7: 145–160.
50.
Amaral DG, Price JL, Pitkanen A, Carmichael ST. Anatomical organization of the primate amygdaloid complex. In: Aggleton JP, ed. The amygdala: neurobiological aspects of emotion, memory and mental dysfunction. New York: Wiley-Liss; 1992: 1–66.
51.
Adolphs R, Tranel D, Hamann S, et al. Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia . 1999; 37: 1111–1117.
52.
Hornak J, Rolls ET, Wade D. Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia . 1996; 34: 247–261.
53.
Buchel C, Dolan RJ, Armony JL, Friston KJ. Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging. J Neurosci . 1999; 19: 10869–10876.
54.
Buchel C, Dolan RJ. Classical fear conditioning in functional neuroimaging. Curr Opin Neurobiol . 2000; 10: 219–223.
55.
Phillips ML, Young AW, Scott SK, et al. Neural responses to facial and vocal expressions of fear and disgust. Proceedings of the Royal Society of London Series B. Biological Sciences . 1998; 265: 1809–1817.
56.
Gorno–Tempini ML, Pradelli S, Serafini M, et al. Explicit and incidental facial expression processing: an fMRI study. Neuroimage . 2001; 14: 465–473.
57.
Franzen EA, Myers RE. Neural control of social behavior: prefrontal and anterior temporal cortex. Neuropsychologia . 1972; 11: 141–157.
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Received: May 4, 2001
Accepted: September 27, 2001
Published online: January 22, 2002
Published in print: January 22, 2002
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