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Dementia & Neuropsychologia

Print version ISSN 1980-5764

Dement. neuropsychol. vol.7 no.1 São Paulo Jan./Mar. 2013

http://dx.doi.org/10.1590/S1980-57642013DN70100014 

ORIGINAL ARTICLES

A tale of two hemispheres: Contrasting socioemotional dysfunction in right- versus left-lateralised semantic dementia

Um conto sobre dois hemisférios: contrastando a disfunção socioemocional na demência semântica com atrofia lateralizada à direita versus esquerda

Muireann Irish1 

Fiona Kumfor2 

John R. Hodges3 

Olivier Piguet4 

1School of Psychology, University of New South Wales, Sydney, Australia. Neuroscience Research Australia, Sydney, Australia, and School of Medical Sciences, University of New South Wales, Sydney, Australia. PhD, Research Fellow at the School of Psychology, University of New South Wales, Sydney, Australia.

2Masters, PhD, Candidate at Neuroscience Research Australia, Randwick, Sydney, Australia.

3Professor and Senior Principal Research Fellow at Neuroscience Research Australia, Randwick, Sydney, Australia.

4Associate Professor and Senior Research Fellow at Neuroscience Research Australia, Randwick, Sydney, Australia.

ABSTRACT

Objective:

Semantic dementia, a subtype of frontotemporal lobar degeneration, is characterised by cross-modal loss of conceptual knowledge attributable to progressive degeneration of the left anterior temporal lobe. Much less is known regarding the clinical presentation of SD patients with predominantly right-lateralised atrophy. Recent reports emphasise marked socioemotional and behavioural disturbances in such cases. Given the importance of the right anterior temporal lobes in social cognition, we hypothesised that socioemotional functioning would be disproportionately affected in right versus left-lateralised SD cases.

Methods:

We assessed well-characterised cases of predominantly right (n=10) and left (n=12) SD and 20 matched healthy controls on tests of emotion processing and interpersonal functioning.

Results:

Right SD cases showed disproportionate difficulties in the recognition of positive and negative facial emotions, specifically happiness and anger, compared with left SD cases. Deficits in anger recognition persisted in right SD despite covarying for facial and semantic processing. On a contextually rich task of emotion recognition using multimodal videos, no subgroup differences were evident. Finally, empathic concern was rated as significantly lower by caregivers of right versus left SD cases. Overall, the extent of socioemotional disturbance was associated with the degree of behavioural changes in SD.

Conclusion:

Our results reveal considerable overlap in the extent to which socioemotional processes are disrupted in left and right-lateralised cases of SD. Notably, however, right SD cases show disproportionate deficits for recognition of facial emotions and the capacity for empathic concern, supporting a specialised role for the right anterior temporal lobes in mediating these cognitive functions.

Key words: semantic dementia; emotion processing; frontotemporal dementia; hemispheric lateralisation

RESUMO

Objetivo:

A demência semântica (DS), um subtipo de degeneração lobar frontotemporal, é caracterizada por perda multimodal do conhecimento conceitual atribuída à degeneração progressiva do região anterior do lobo temporal esquerdo. Sabe-se menos sobre o quadro clínico de pacientes com DS em que a atrofia é localizada predominantemente à direita. Relatos recentes têm enfatizado marcantes distúrbios socioemocionais e comportamentais em tais casos. Dada a importância da região anterior do lobo temporal direito na cognição social, aventamos a hipótese de que o funcionamento socioemocional seria desproporcionalmente afetado nos casos de DS com atrofia lateralizada à direita.

Métodos:

Foram avaliados os desempenhos de casos bem caracterizados de DS com atrofia do lobo temporal predominantemente à direita (n=10) e à esquerda (n=12) e 20 controles saudáveis em testes de processamento de emoções e funcionamento interpessoal.

Resultados:

Casos de DS com atrofia predominante à direita apresentaram dificuldades desproporcionadas no reconhecimento de emoções faciais positivas e negativas, especificamente expressões de felicidade e raiva, em comparação com os casos de atrofia à esquerda. Os déficits no reconhecimento de raiva persistiram depois de excluídas as covariações com processamento facial e semântico. Em uma tarefa contextualmente rica de reconhecimento de emoções através de vídeos multimodais, não houve diferenças entre os subgrupos. Por fim, preocupação empática foi classificada por cuidadores como significativamente menor nos casos com atrofia à direita. Em geral, o grau de perturbação socioemocional foi associado com o grau de alterações comportamentais na DS.

Conclusão:

Nossos resultados revelam uma considerável sobreposição na medida em que os processos socioemocionais são rompidos tanto em casos com atrofia predominante à direita como à esquerda. Notavelmente, entretanto, os casos com DS com atrofia predominante à direita apresentam déficits desproporcionais no reconhecimento de emoções faciais e na capacidade de preocupação empática, dando suporte à hipótese de um papel especializado das regiões anteriores do lobo temporal direito na mediação dessas funções cognitivas.

Palavras-chave: demência semântica; processamento de emoção; demência frontotemporal; lateralização hemisférica

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REFERENCES

Hodges JR, Patterson K. Semantic dementia: a unique clinicopathological syndrome. Lancet Neurol 2007;6:1004-1014. [ Links ]

Mion M, Patterson K, Acosta-Cabronero J, et al. What the left and right anterior fusiform gyri tell us about semantic memory. Brain 2010; 133:3256-3268. [ Links ]

Chan D, Fox N, Scahill R, et al. Patterns of temporal lobe atrophy in semantic dementia and Alzheimer's disease. Ann Neurol 2001;49: 433-442. [ Links ]

Galton C, Patterson K, Graham K, et al. Differing patterns of temporal atrophy in Alzheimer's disease and semantic dementia. Neurology 2001;57:216-225. [ Links ]

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. [ Links ]

Irish M, Addis DR, Hodges JR, Piguet O. Considering the role of semantic memory in episodic future thinking: evidence from semantic dementia. Brain2012;135:2178-2191. [ Links ]

Edwards-Lee T, Miller BL, Benson DF, et al. The temporal variant of frontotemporal dementia. Brain1997;120:1027-1040. [ Links ]

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. [ Links ]

Gainotti G, Barbier A, Marra C. Slowly progressive defect in recognition of familiar people in a patient with right anterior temporal atrophy. Brain2003;126:792-803. [ Links ]

Thompson SA, Patterson K, Hodges JR.Left/right asymmetry of atrophy in semantic dementia: behavioral-cognitive implications. Neurology2003;61:1196-1203. [ Links ]

Gorno-Tempini ML, Rankin KP, Woolley JD, Rosen HJ, Phengrasamy L, Miller BL. Cognitive and behavioral profile in a case of right anterior temporal lobe neurodegeneration. Cortex 2004;40:631-644. [ Links ]

Chan D, Anderson V, Pijnenburg Y, et al. The clinical profile of right temporal lobe atrophy. Brain2009;132:1287-1298. [ Links ]

Henry ML, Wilson SM, Ogar JM, et al. Neuropsychological, behavioral, and anatomical evolution in right temporal variant frontotemporal dementia: A longitudinal and post-mortem single case analysis.. Neurocase In press. [ Links ]

Ross LA, Olson IR. Social cognition and the anterior temporal lobes. Neuroimage 2010;49:3452-3462. [ Links ]

Zahn R, Moll J, Krueger F, Huey ED, Garrido G, Grafman J. Social concepts are represented in the superior anterior temporal cortex. Proc Natl Acad Sci USA 2007;104:6430-6435. [ Links ]

Kumfor F, Miller L, Lah S, et al. Are you really angry? The effect of intensity on facial emotion recognition in frontotemporal dementia. Soc Neurosci 2011;6:502-514. [ Links ]

Miller LA, Hsieh S, Lah S, Savage S, Hodges JR, Piguet O. One size does not fit all: face emotion processing impairments in semantic dementia, behavioural-variant frontotemporal dementia and Alzheimer's disease are mediated by distinct cognitive deficits. Behav Neurol 2012;25:53-60. [ Links ]

Hsieh S, Hornberger M, Piguet O, Hodges JR. Braincorrelates of musical and facial emotion recognition: evidence from the dementias. Neuropsychologia 2012;50:1814-1822. [ Links ]

Hsieh S, Foxe D, Leslie F, Savage S, Piguet O, Hodges JR.Grief and joy: emotion word comprehension in the dementias. Neuropsychology 2012;26:624-630. [ Links ]

Rankin KP, Gorno-Tempini ML, Allison SC, et al. Structural anatomy of empathy in neurodegenerative disease. Brain2006;129:2945-2956. [ Links ]

Rankin KP, Kramer JH, Miller BL. Patterns of cognitive and emotional empathy in frontotemporal lobar degeneration. Cogn Behav Neurol2005;18:28-36. [ Links ]

Eslinger PJ, Moore P, Anderson C, Grossman M. Social cognition, executive functioning, and neuroimaging correlates of empathic deficits in frontotemporal dementia. J Neuropsychiatry Clin Neurosci 2011;23:74-82. [ Links ]

Gorno-Tempini ML, Hillis AE, Weintraub S, et al. Classification of primary progressive aphasia and its variants. Neurology2011;76:1006-1014. [ Links ]

Morris J. Clinical dementia rating: a reliable and valid diagnostic and staging measure for dementia of the Alzheimer type. Int Psychogeriatr 1997;9:173-176. [ Links ]

Mioshi E, Dawson K, Mitchell J, Arnold R, Hodges J. The Addenbrooke's Cognitive Examination Revised (ACE-R): a brief cognitive test battery for dementia screening. Int J Geriatr Psychiatry 2006;21:1078-1085. [ Links ]

Meyers J, Meyers K. The Meyers Scoring System for the Rey Complex Figure and the Recognition Trial: Professional Manual. Odessa, FL: Psychological Assessment Resources; 1995. [ Links ]

Savage, S., Hsieh, S., Leslie, F., Foxe, D., Piguet, O., Hodges, J.R. Distinguishing subtypes in primary progressive aphasia: Application of the Sydney Language Battery. Dem Ger Cogn Disord. In press, accepted 3/12/2012. [ Links ]

Reitan R. Validity of the Trail Making Test as an indicator of organic brain damage. Percept Mot Skills 1958;8:271-276. [ Links ]

Strauss E, Sherman EMS, Spreen O. A compendium of neuropsychological tests: Administration, norms, and commentary: Oxford University Press, USA; 2006. [ Links ]

Young AW, Perrett D, Calder AJ, Sprengelmeyer R, Ekman P. Facial Expressions of Emotion - Stimuli and Tests (FEEST): Thames Valley Test Company; 2002. [ Links ]

Ekman P, Friesen WV. Pictures of Facial Affect. San Francisco: CA: Consulting Psychologists Press; 1976. [ Links ]

McDonald S, Flanagan S, Rollins J, Kinch J. TASIT: A new clinical tool for assessing social perception after traumatic brain injury. J Head Trauma Rehabil 2003;18:219-238. [ Links ]

Davis MH. Measuring individual differences in empathy: Evidence for a multidimensional approach. J Pers Soc Psychol 1983;44:113-126. [ Links ]

Wedderburn C, Wear H, Brown J, et al. The utility of the Cambridge Behavioural Inventory in neurodegenerative disease. J Neurol Neurosurg Psychiatry 2008;79:500-503. [ Links ]

Rosen HJ, Perry RJ, Murphy J, et al. Emotion comprehension in the temporal variant of frontotemporal dementia. Brain2002;125:2286-2295. [ Links ]

Liu W, Miller BL, Kramer JH, et al. Behavioral disorders in the frontal and temporal variants of frontotemporal dementia. Neurology2004;62: 742-748. [ Links ]

Adolphs R, Tranel D, Damasio H. Emotion recognition from faces and prosody following temporal lobectomy. Neuropsychology2001;15: 396-404. [ Links ]

Mendez MF, Perryman KM. Disrupted facial empathy in drawings from artists with frontotemporal dementia. Neurocase2003;9:44-50. [ Links ]

Sollberger M, Stanley CM, Wilson SM, et al. Neural basis of interpersonal traits in neurodegenerative diseases. Neuropsychologia2009;47: 2812-2827. [ Links ]

Irish M, Piguet O, Hodges JR.Self-projection and the default network in frontotemporal dementia. Nat Rev Neurol 2012;8:152-161. [ Links ]

Duval C, Bejanin A, Piolino P, et al. Theory of mind impairments in patients with semantic dementia. Brain2012;135:228-241. [ Links ]

Seeley WW, Bauer AM, Miller BL, et al. The natural history of temporal variant frontotemporal dementia. Neurology2005;64:1384-1390. [ Links ]

Brambati SM, Rankin KP, Narvid J, et al. Atrophy progression in semantic dementia with asymmetric temporal involvement: a tensor-based morphometry study. Neurobiol Aging 2009;30:103-111. [ Links ]

Received: November 25, 2012; Accepted: February 02, 2013

Olivier Piguet. Neuroscience Research Australia, Barker Street, Randwick, Sydney, Australia, NSW 2031. E-mail: o.piguet@neura.edu.au

Disclosure: The authors report no conflicts of interest.

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