Handedness and language learning disability differentially distribute in progressive aphasia variants

Zachary A. Miller, Maria Luisa Mandelli, Katherine P. Rankin, Maya L. Henry, Miranda C. Babiak, Darvis T. Frazier, Iryna V. Lobach, Brianne M. Bettcher, Teresa Q. Wu, Gil D. Rabinovici, Neill R Graff Radford, Bruce L. Miller, Maria Luisa Gorno-Tempini

Research output: Contribution to journalArticle

50 Citations (Scopus)

Abstract

Primary progressive aphasia is a neurodegenerative clinical syndrome that presents in adulthood with an isolated, progressive language disorder. Three main clinical/anatomical variants have been described, each associated with distinctive pathology. A high frequency of neurodevelopmental learning disability in primary progressive aphasia has been reported. Because the disorder is heterogeneous with different patterns of cognitive, anatomical and biological involvement, we sought to identify whether learning disability had a predilection for one or more of the primary progressive aphasia subtypes. We screened the University of California San Francisco Memory and Aging Center's primary progressive aphasia cohort (n = 198) for history of languagerelated learning disability as well as hand preference, which has associations with learning disability. The study included logopenic (n = 48), non-fluent (n = 54) and semantic (n = 96) variant primary progressive aphasias. We investigated whether the presence of learning disability or non-right-handedness was associated with differential effects on demographic, neuropsychological and neuroimaging features of primary progressive aphasia. We showed that a high frequency of learning disability was present only in the logopenic group (X 2 = 15.17, P< 0.001) and (X2 = 11.51, P< 0.001) compared with semantic and nonfluent populations. In this group, learning disability was associated with earlier onset of disease, more isolated language symptoms, and more focal pattern of left posterior temporoparietal atrophy. Non-right-handedness was instead over-represented in the semantic group, at nearly twice the prevalence of the general population (X2 = 6.34, P = 0.01). Within semantic variant primary progressive aphasia the right-handed and non-right-handed cohorts appeared homogeneous on imaging, cognitive profile, and structural analysis of brain symmetry. Lastly, the non-fluent group showed no increase in learning disability or non-right-handedness. Logopenic variant primary progressive aphasia and developmental dyslexia both manifest with phonological disturbances and posterior temporal involvement. Learning disability might confer vulnerability of this network to earlyonset, focal Alzheimer's pathology. Left-handedness has been described as a proxy for atypical brain hemispheric lateralization. As non-right-handedness was increased only in the semantic group, anomalous lateralization mechanisms might instead be related to frontotemporal lobar degeneration with abnormal TARDBP. Taken together, this study suggests that neurodevelopmental signatures impart differential trajectories towards neurodegenerative disease.

Original languageEnglish (US)
Pages (from-to)3461-3473
Number of pages13
JournalBrain
Volume136
Issue number11
DOIs
StatePublished - Nov 2013

Fingerprint

Primary Progressive Aphasia
Functional Laterality
Learning Disorders
Aphasia
Language
Semantics
Association Learning
Frontotemporal Lobar Degeneration
Pathology
Language Disorders
Handedness
Learning Disability
Language-learning Disabilities
Progressive Aphasia
Dyslexia
San Francisco
Brain
Proxy
Neuroimaging
Neurodegenerative Diseases

Keywords

  • Alzheimer's disease
  • Case control study
  • Dementia aphasia
  • Frontotemporal dementia
  • Risk factors in epidemiology

ASJC Scopus subject areas

  • Clinical Neurology
  • Arts and Humanities (miscellaneous)

Cite this

Miller, Z. A., Mandelli, M. L., Rankin, K. P., Henry, M. L., Babiak, M. C., Frazier, D. T., ... Gorno-Tempini, M. L. (2013). Handedness and language learning disability differentially distribute in progressive aphasia variants. Brain, 136(11), 3461-3473. https://doi.org/10.1093/brain/awt242

Handedness and language learning disability differentially distribute in progressive aphasia variants. / Miller, Zachary A.; Mandelli, Maria Luisa; Rankin, Katherine P.; Henry, Maya L.; Babiak, Miranda C.; Frazier, Darvis T.; Lobach, Iryna V.; Bettcher, Brianne M.; Wu, Teresa Q.; Rabinovici, Gil D.; Graff Radford, Neill R; Miller, Bruce L.; Gorno-Tempini, Maria Luisa.

In: Brain, Vol. 136, No. 11, 11.2013, p. 3461-3473.

Research output: Contribution to journalArticle

Miller, ZA, Mandelli, ML, Rankin, KP, Henry, ML, Babiak, MC, Frazier, DT, Lobach, IV, Bettcher, BM, Wu, TQ, Rabinovici, GD, Graff Radford, NR, Miller, BL & Gorno-Tempini, ML 2013, 'Handedness and language learning disability differentially distribute in progressive aphasia variants', Brain, vol. 136, no. 11, pp. 3461-3473. https://doi.org/10.1093/brain/awt242
Miller ZA, Mandelli ML, Rankin KP, Henry ML, Babiak MC, Frazier DT et al. Handedness and language learning disability differentially distribute in progressive aphasia variants. Brain. 2013 Nov;136(11):3461-3473. https://doi.org/10.1093/brain/awt242
Miller, Zachary A. ; Mandelli, Maria Luisa ; Rankin, Katherine P. ; Henry, Maya L. ; Babiak, Miranda C. ; Frazier, Darvis T. ; Lobach, Iryna V. ; Bettcher, Brianne M. ; Wu, Teresa Q. ; Rabinovici, Gil D. ; Graff Radford, Neill R ; Miller, Bruce L. ; Gorno-Tempini, Maria Luisa. / Handedness and language learning disability differentially distribute in progressive aphasia variants. In: Brain. 2013 ; Vol. 136, No. 11. pp. 3461-3473.
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abstract = "Primary progressive aphasia is a neurodegenerative clinical syndrome that presents in adulthood with an isolated, progressive language disorder. Three main clinical/anatomical variants have been described, each associated with distinctive pathology. A high frequency of neurodevelopmental learning disability in primary progressive aphasia has been reported. Because the disorder is heterogeneous with different patterns of cognitive, anatomical and biological involvement, we sought to identify whether learning disability had a predilection for one or more of the primary progressive aphasia subtypes. We screened the University of California San Francisco Memory and Aging Center's primary progressive aphasia cohort (n = 198) for history of languagerelated learning disability as well as hand preference, which has associations with learning disability. The study included logopenic (n = 48), non-fluent (n = 54) and semantic (n = 96) variant primary progressive aphasias. We investigated whether the presence of learning disability or non-right-handedness was associated with differential effects on demographic, neuropsychological and neuroimaging features of primary progressive aphasia. We showed that a high frequency of learning disability was present only in the logopenic group (X 2 = 15.17, P< 0.001) and (X2 = 11.51, P< 0.001) compared with semantic and nonfluent populations. In this group, learning disability was associated with earlier onset of disease, more isolated language symptoms, and more focal pattern of left posterior temporoparietal atrophy. Non-right-handedness was instead over-represented in the semantic group, at nearly twice the prevalence of the general population (X2 = 6.34, P = 0.01). Within semantic variant primary progressive aphasia the right-handed and non-right-handed cohorts appeared homogeneous on imaging, cognitive profile, and structural analysis of brain symmetry. Lastly, the non-fluent group showed no increase in learning disability or non-right-handedness. Logopenic variant primary progressive aphasia and developmental dyslexia both manifest with phonological disturbances and posterior temporal involvement. Learning disability might confer vulnerability of this network to earlyonset, focal Alzheimer's pathology. Left-handedness has been described as a proxy for atypical brain hemispheric lateralization. As non-right-handedness was increased only in the semantic group, anomalous lateralization mechanisms might instead be related to frontotemporal lobar degeneration with abnormal TARDBP. Taken together, this study suggests that neurodevelopmental signatures impart differential trajectories towards neurodegenerative disease.",
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N2 - Primary progressive aphasia is a neurodegenerative clinical syndrome that presents in adulthood with an isolated, progressive language disorder. Three main clinical/anatomical variants have been described, each associated with distinctive pathology. A high frequency of neurodevelopmental learning disability in primary progressive aphasia has been reported. Because the disorder is heterogeneous with different patterns of cognitive, anatomical and biological involvement, we sought to identify whether learning disability had a predilection for one or more of the primary progressive aphasia subtypes. We screened the University of California San Francisco Memory and Aging Center's primary progressive aphasia cohort (n = 198) for history of languagerelated learning disability as well as hand preference, which has associations with learning disability. The study included logopenic (n = 48), non-fluent (n = 54) and semantic (n = 96) variant primary progressive aphasias. We investigated whether the presence of learning disability or non-right-handedness was associated with differential effects on demographic, neuropsychological and neuroimaging features of primary progressive aphasia. We showed that a high frequency of learning disability was present only in the logopenic group (X 2 = 15.17, P< 0.001) and (X2 = 11.51, P< 0.001) compared with semantic and nonfluent populations. In this group, learning disability was associated with earlier onset of disease, more isolated language symptoms, and more focal pattern of left posterior temporoparietal atrophy. Non-right-handedness was instead over-represented in the semantic group, at nearly twice the prevalence of the general population (X2 = 6.34, P = 0.01). Within semantic variant primary progressive aphasia the right-handed and non-right-handed cohorts appeared homogeneous on imaging, cognitive profile, and structural analysis of brain symmetry. Lastly, the non-fluent group showed no increase in learning disability or non-right-handedness. Logopenic variant primary progressive aphasia and developmental dyslexia both manifest with phonological disturbances and posterior temporal involvement. Learning disability might confer vulnerability of this network to earlyonset, focal Alzheimer's pathology. Left-handedness has been described as a proxy for atypical brain hemispheric lateralization. As non-right-handedness was increased only in the semantic group, anomalous lateralization mechanisms might instead be related to frontotemporal lobar degeneration with abnormal TARDBP. Taken together, this study suggests that neurodevelopmental signatures impart differential trajectories towards neurodegenerative disease.

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