The Relation between Amygdala Atrophy and Other Selected Brain Structures and Emotional Agnosia in Alzheimer Disease


Authors: K. Bechyně 1,5;  A. Varjassyová 1;  D. Lodinská 1;  M. Vyhnálek 1;  M. Bojar 1;  J. Brabec 2;  P. Petrovický 2;  Z. Seidl 4;  I. Schenk 5;  J. Hort 1
Authors‘ workplace: Neurologická klinika 2. LF UK a FN v Motole, Praha 1;  Anatomický ústav 1. LF UK v Praze 2;  Neurochirurgická klinika ÚVN Praha 3;  Radiodiagnostická klinika 1. LF UK a VFN v Praze 4;  Neurologické oddělení Nemocnice Písek 5
Published in: Cesk Slov Neurol N 2008; 71/104(6): 675-681
Category: Original Paper

Poděkování: Rádi bychom poděkovali pacientům a jejich rodinám za jejich čas a spolupráci. Tento projekt byl podpořen grantem GAČR 309/05/0693 a IGA MZ ČR 2006, NR 8931-4.

Overview

Introduction:
The amygdala and other structures of the limbic system are responsible for the analysis of signals carrying an emotional charge. The affection of the limbic system by a neurodegenerative process may cause a change in emotional perception or even emotional agnosia. The article evaluates the relation between in vivo measured volumes of the amygdala, hippocampus, anterior cingular cortex, temporal lobe pole and emotional agnosia in patients with Alzheimer’s disease as compared with the control population.

Material and method:
26 patients with Alzheimer’s disease and 17 members of the control group were subject to a magnetic resonance exam and a neuropsychological exam including an emotion recognition test using facial expression. Magnetic resonance volumetry was used to measure the amygdala, hippocampus, anterior cingular cortex and temporal pole volumes.

Results:
All regional volume values obtained by the measurement and the results of neuropsychological tests were significantly worse in patients with AD as compared with the control group. Comparison of regional volumes with the results of the emotion recognition test showed significant correlation between: left amygdala volume and the capacity to recognise joy (r = 0.54, p < 0.01) and sadness (r = 0.49, p < 0.05), right amygdala volume and the capacity to recognise fear (r = 0.34, p < 0.05) and sadness (r = 0.56, p < 0.01), the volume of both hippocampi and the capacity to recognise anger (r = 0.55 – right, and r = 0.58 – left, p < 0.01).

Conclusion:
The relation observed between a lower amygdala volume and a reduced capacity to recognise some emotions in patients with AD corroborates the hypothesis that emotional agnosia in AD patients is linked with atrophy of the amygdala and other limbic system structures.

Key words:
Alzheimer disease – emotional agnosia – amygdala – MR volumetry


Sources

1. Anderson AK, Phelps EA. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 2001; 411(6835): 305–309.

2. McGaugh JL, Ferry B, Vazdarjanova A, Roozendaal B. Amygdala: role in modulation of memory storage. In: Aggleton JP (ed). The Amygdala: A Functional Analysis. New York: Oxford University Press 2000: 391–424.

3. Damasio AR. On some functions of the human prefrontal cortex. Ann N Y Acad Sci 1995; 769: 241–251.

4. Markowitsch HJ, Calabrese P, Würker M, Durwen HF, Kessler J, Babinsky R et al. The amygdala‘s contribution to memory – a study on two patients with Urbach-Wiethe disease. Neuroreport 1994; 5(11): 1349–1352.

5. Morris JS, Ohman A, Dolan RJ. Conscious and unconscious emotional learning in the human amygdala. Nature 1998; 393(6684): 467–470.

6. Anderson AK, Phelps EA. Expression without recognition: contributions of the human amygdala to emotional communication. Psychol Sci 2000; 11(2): 106–111.

7. Mori E, Ikeda M, Hirono N, Kitagaki H, Imamura T, Shimomura R. Amygdalar volume and emotional memory in Alzheimer‘s disease. Am J Psychiatry 1999; 156(2): 216–222.

8. Blair RJ, Morris JS, Frith CD, Perrett DI, Dolan RJ. Dissociable neural responses to facial expressions of sadness and anger. Brain 1999; 122(5): 883–893.

9. Dolan RJ, Fletcher P, Morris J, Kapur N, Deakin JF, Frith CD. Neural activation during covert processing of positive emotional facial expressions. Neuroimage 1996; 4(3): 194–200.

10. Hesslinger B, Tebartz van Elst L, Thiel T, Haegele K, Henning J, Ebert D. Frontoorbital volume reductions in adult patients with attention deficit hyperactivity disorder. Neurosci Lett 2002; 328(3): 319–321.

11. Rosen HJ, Perry RJ, Murphy J, Kramer JH, Mychack P, Schuff N et al. Emotion comprehension in the temporal variant of frontotemporal dementia. Brain 2002; 125(10): 2286–2295.

12. Keane J, Calder AJ, Hodges JR, Zouny AW. Face and emotion processing in frontal variant frontotemporal dementia. Neuropsychologia 2002; 40(6): 655–665.

13. Olson IR, Plotzker A, Ezzyat Y. The Enigmatic temporal pole: a review of findings on social and emotional processing. Brain 2007; 130(7): 1718–1731.

14. Gloor P, Olivier A, Quesney LF, Andermann F, Horowitz S. The role of the limbic system in experiential phenomena of temporal lobe epilepsy. Ann Neurol 1982; 12(2): 129–144.

15. Zola-Morgan S, Squire LR, Alvarez-Royo P, Clower RP. Independence of memory functions and emotional behavior: separate contributions of the hippocampal formation and the amygdala. Hippocampus 1991; 1(2): 207–220.

16. Horínek D, Varjassyová A, Hort J. Magnetic resonance analysis of amygdalar volume in Alzheimer‘s disease. Curr Opin Psychiatry 2007; 20(3): 273–277.

17. Horínek D, Petrovický P, Hort J, Krásenský J, Brabec J, Bojar M et al. Amygdalar volume and psychiatric symptoms in Alzheimer‘s disease: an MR analysis. Acta Neurol Scand 2006; 113(1): 40–45.

18. Mori E, Ikeda M, Hirono N, Kitagaki H, Imamura T, Shimomura R. Amygdalar volume and emotional memory in Alzheimer’s disease. Am J Psychiatry 1999; 156(2): 216–222.

19. Lavenu I, Pasquier F, Lebert F, Petit H, Van der Linden M. Perception of emotion in frontotemporal dementia and Alzheimer disease. Alzheimer Dis Assoc Disord 1999; 13(2): 96–101.

20. Szeszko PR, Robinson D, Alvir JMJ, Binder RM, Lencz T, Ashtari M et al. Orbital frontal and amygdala volume reductions in obsessive-compulsive disorder. Arch Gen Psychiatry 1999; 56(10): 913–919.

21. 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 the Department of Health and Human Services Task Force on Alzheimer’s disease. Neurology 1984; 34(7): 939–944.

22. Rasova K, Krasensky J, Havrdova E, Obenberger J, Seidl Z, Dolezal O et al. Is it possible to actively and purposely make use of plasticity and adaptability in the neurorehabilitation treatment of multiple sclerosis patients? A pilot project. Clin Rehabil 2005; 19(2): 170–181.

23. Laakso MP, Soininen H, Partanen K, Lehtovirta M, Hallikainen M, Hänninen T et al. MRI of the hippocampus in Alzheimer‘s disease: sensitivity, specificity, an analysis of the incorrectly classified subjects. Neurobiol Aging 1998; 19(1): 23–31.

24. Brabec J. Jednoduchá metoda stanovení velikosti striata pro klinické diagnostické účely. Cesk Slov Neurol N 2005; 68/101(3): 179–182.

25. Hořínek D, Hort J, Brabec J, Bojar M, Krásenský J, Seidl Z et al. Objem amygdaly je snížen u nemocných s Alzheimerovou chorobou. Cesk Slov Neurol N 2005; 68/101(4): 235–240.

26. Amaral DG, Insausti R. The human hippocampal formation. In: Paxinos G (ed). The Human Nervous System. San Diego: Academic Press 1990: 711–755.

27. Folstein MF, Folstein SE, McHugh PR. „Mini‑mental State“. A practical method for the grading the cognitive state of patients for the clinician. J Psychiat Res 1975(3); 12: 189–198.

28. Buschke H. Cued recall in amnesia. J Clin Neuropsychol 1984; 6(4): 433–440.

29. Benton AL. Revised Visual Retention Test: clinical and experimental applications. Iowa City: State University of Iowa 1955.

30. Ekman P, Friesen WV. Pictures of facial affect. Palo Alto CA: Consulting Psychologists Press 1976.

31. Gray JM, Young AW, Barker WA, Curtis A, Gibson D. Impaired recognition of disgust in Huntington‘s disease gene carriers. Brain 1997; 120(11): 2029–2038.

32. Tisserand DJ, Pruessner JC, Sanz Arigita EJ, van Boxtel MP, Evans AC, Jolles J et al. Regional frontal cortical volumes decrease differentially in aging: An MRI study to compare volumetric approaches and voxel‑based morphometry. Neuroimage 2002; 17(2): 657–669.

33. Paus T, Tomaiuolo F, Otaky N, MacDonald D, Petrides M, Atlas J et al. Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map. Cereb Cortex 1996; 6(2): 207–214.

34. Jack CR jr, Petersen RC, Xu YC, O’Brien PC, Smith GE, Ivnik RJ et al. Prediction of AD with MRI‑based hippocampal volume in mild cognitive impairment. Neurology 1999; 52(7): 1397–1403.

35. Gorno–Tempini ML, Price CJ, Josephs O, Vandenberghe R, Cappa SF, Kapur N et al. The neural systems sustaining face and proper–name processing. Brain 1998; 121(11): 2103–2118.

36. Leveroni CL, Seidenberg M, Mayer AR, Mead LA, Binder JR, Rao SM. Neural systems underlying the recognition of familiar and newly learned faces. J Neurosci 2000; 20(2): 878–886.

37. Schneider F, Grodd W, Weiss U, Klose U, Mayer KR, Nägele T et al. Functional MRI reveals left amygdala activation during emotion. Psychiatry Res 1997; 76(2–3): 75–82

38. Canli T. Hemispheric asymmetry in the experience of emotion: a perspective from functional imaging. Neuroscientist 1999; 5: 201–207.

39. Pitkänen A. Connectivity of the rat amygdaloid complex. In: Aggleton JP (ed). The Amygdala: A Functional Analysis. Oxford: Oxford University Press 2000: 31–115.

40. Richardson MP, Strange B, Dolan RJ. Encoding of emotional memories depends on the amygdala and hippocampus and their interactions. Nat Neurosci 2004; 7(3): 278–285.

41. Rosen HJ, Perry RJ, Murphy J, Kramer JH, Mychack P, Schuff N et al. Emotion comprehension in the temporal variant of frontotemporal dementia. Brain 2002; 125(10): 2286–2295.

42. Burnham H, Hogervorst E. Recognition of facial expressions of emotion by patients with dementia of the Alzheimer type. Dement Geriatr Cogn Disord 2004; 18(1): 75–79.

43. Whitwell JL, Sampson EL, Watt HC, Harvey RJ, Rossor MN, Fox NC. A volumetric magnetic resonance imaging study of the amygdala in frontotemporal lobar degeneration and Alzheimer‘s disease. Dement Geriatr Cogn Disord 2005; 20(4): 238–244.

44. Boccardi M, Sabattoli F, Laakso MP, Testa C, Rossi R, Beltramello A et al. Frontotemporal dementia as a neural system disease. Neurobiol Aging 2005; 26(1): 37–44.

45. Killgore WD, Yurgelun-Todd DA. Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces. Neuroimage 2004; 21(4): 1215–1223.

Labels
Paediatric neurology Neurosurgery Neurology

Article was published in

Czech and Slovak Neurology and Neurosurgery

Issue 6

2008 Issue 6

Most read in this issue

This topic is also in:


Login
Forgotten password

Don‘t have an account?  Create new account

Forgotten password

Enter the email address that you registered with. We will send you instructions on how to set a new password.

Login

Don‘t have an account?  Create new account