Hyperorality in Frontotemporal Dementia: How Psychiatric and Neural Correlates Change During the Disease Course

Christopher B Morrow; Chiadi Onyike; Alexander Pantelyat; Gwenn S Smith; Jeannie Leoutsakos; Andreia V Faria; Neill R Graff-Radford; R Ryan Darby; Nupur Ghoshal; Adam M Staffaroni; Katya Rascovsky; Toji Miyagawa; Akshata Balaji; Kyrana Tsapkini; Maria I Lapid; Mario F Mendez; Irene Litvan; Belen Pascual; ALLFTD consortium; Julio C Rojas; Zbigniew K Wszolek; Kimiko Domoto-Reilly; John Kornak; Vidyulata Kamath

doi:10.1176/appi.neuropsych.20240134

Hyperorality in Frontotemporal Dementia: How Psychiatric and Neural Correlates Change During the Disease Course

Christopher B Morrow, Chiadi Onyike, Alexander Pantelyat, Gwenn S Smith, Jeannie Leoutsakos, Andreia V Faria, Neill R Graff-Radford, R Ryan Darby, Nupur Ghoshal, Adam M Staffaroni, Katya Rascovsky, Toji Miyagawa, Akshata Balaji, Kyrana Tsapkini, Maria I Lapid, Mario F Mendez, Irene Litvan, Belen Pascual, ALLFTD consortium, Julio C RojasZbigniew K Wszolek, Kimiko Domoto-Reilly, John Kornak, Vidyulata Kamath

Research output: Contribution to journal › Article › peer-review

Abstract

OBJECTIVE: Hyperorality is a core feature of behavioral variant frontotemporal dementia (bvFTD); however, the cognitive, psychiatric, and neuroanatomical correlates of hyperorality across the bvFTD stages remain unclear. The authors explored these associations in early- and advanced-stage bvFTD.

METHODS: Participants with sporadic or genetic bvFTD were enrolled in the ARTFL LEFFTDS Longitudinal Frontotemporal Lobar Degeneration (ALLFTD) consortium study. Baseline cognitive and psychiatric symptoms of participants with or without hyperorality were compared after stratification by disease severity. Linear multivariable regressions adjusted for age and total intracranial volume were used to examine associations between regional gray matter volume (GMV) and hyperorality status. Five anatomical regions of interest were preselected for analysis on the basis of previously identified neuroanatomical correlates of hyperorality in bvFTD.

RESULTS: Hyperorality was present in 50% of early-stage bvFTD participants (N=136) and was associated with higher rates of ritualistic-compulsive behavior and difficulty detecting social-emotional expressions. Hyperorality was present in 63% of advanced-stage participants (N=208) and was associated with higher rates of apathy, ritualistic-compulsive behavior, and socially aberrant behavior. Regional GMV was similar for those with or without hyperorality among early-stage participants. Among advanced-stage participants, hyperorality was associated with lower GMV in the right dorsal and ventral striatum.

CONCLUSIONS: Hyperorality emerged early in bvFTD and was accompanied by deficits in social cognition and complex-ritualistic behavior before clinically significant GMV loss. These findings suggest that early identification and management of hyperorality could improve neuropsychiatric trajectories in bvFTD.

Original language	English (US)
Pages (from-to)	appineuropsych20240134
Journal	Journal of Neuropsychiatry and Clinical Neurosciences
DOIs	https://doi.org/10.1176/appi.neuropsych.20240134
State	E-pub ahead of print - Mar 26 2025

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10.1176/appi.neuropsych.20240134

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Morrow, C. B., Onyike, C., Pantelyat, A., Smith, G. S., Leoutsakos, J., Faria, A. V., Graff-Radford, N. R., Darby, R. R., Ghoshal, N., Staffaroni, A. M., Rascovsky, K., Miyagawa, T., Balaji, A., Tsapkini, K., Lapid, M. I., Mendez, M. F., Litvan, I., Pascual, B., ALLFTD consortium, ... Kamath, V. (2025). Hyperorality in Frontotemporal Dementia: How Psychiatric and Neural Correlates Change During the Disease Course. Journal of Neuropsychiatry and Clinical Neurosciences, appineuropsych20240134. Advance online publication. https://doi.org/10.1176/appi.neuropsych.20240134

Morrow, CB, Onyike, C, Pantelyat, A, Smith, GS, Leoutsakos, J, Faria, AV, Graff-Radford, NR, Darby, RR, Ghoshal, N, Staffaroni, AM, Rascovsky, K, Miyagawa, T, Balaji, A, Tsapkini, K, Lapid, MI, Mendez, MF, Litvan, I, Pascual, B, ALLFTD consortium, Rojas, JC, Wszolek, ZK, Domoto-Reilly, K, Kornak, J & Kamath, V 2025, 'Hyperorality in Frontotemporal Dementia: How Psychiatric and Neural Correlates Change During the Disease Course', Journal of Neuropsychiatry and Clinical Neurosciences, pp. appineuropsych20240134. https://doi.org/10.1176/appi.neuropsych.20240134

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title = "Hyperorality in Frontotemporal Dementia: How Psychiatric and Neural Correlates Change During the Disease Course",

abstract = "OBJECTIVE: Hyperorality is a core feature of behavioral variant frontotemporal dementia (bvFTD); however, the cognitive, psychiatric, and neuroanatomical correlates of hyperorality across the bvFTD stages remain unclear. The authors explored these associations in early- and advanced-stage bvFTD.METHODS: Participants with sporadic or genetic bvFTD were enrolled in the ARTFL LEFFTDS Longitudinal Frontotemporal Lobar Degeneration (ALLFTD) consortium study. Baseline cognitive and psychiatric symptoms of participants with or without hyperorality were compared after stratification by disease severity. Linear multivariable regressions adjusted for age and total intracranial volume were used to examine associations between regional gray matter volume (GMV) and hyperorality status. Five anatomical regions of interest were preselected for analysis on the basis of previously identified neuroanatomical correlates of hyperorality in bvFTD.RESULTS: Hyperorality was present in 50% of early-stage bvFTD participants (N=136) and was associated with higher rates of ritualistic-compulsive behavior and difficulty detecting social-emotional expressions. Hyperorality was present in 63% of advanced-stage participants (N=208) and was associated with higher rates of apathy, ritualistic-compulsive behavior, and socially aberrant behavior. Regional GMV was similar for those with or without hyperorality among early-stage participants. Among advanced-stage participants, hyperorality was associated with lower GMV in the right dorsal and ventral striatum.CONCLUSIONS: Hyperorality emerged early in bvFTD and was accompanied by deficits in social cognition and complex-ritualistic behavior before clinically significant GMV loss. These findings suggest that early identification and management of hyperorality could improve neuropsychiatric trajectories in bvFTD.",

author = "Morrow, {Christopher B} and Chiadi Onyike and Alexander Pantelyat and Smith, {Gwenn S} and Jeannie Leoutsakos and Faria, {Andreia V} and Graff-Radford, {Neill R} and Darby, {R Ryan} and Nupur Ghoshal and Staffaroni, {Adam M} and Katya Rascovsky and Toji Miyagawa and Akshata Balaji and Kyrana Tsapkini and Lapid, {Maria I} and Mendez, {Mario F} and Irene Litvan and Belen Pascual and {ALLFTD consortium} and Rojas, {Julio C} and Wszolek, {Zbigniew K} and Kimiko Domoto-Reilly and John Kornak and Vidyulata Kamath",

year = "2025",

month = mar,

day = "26",

doi = "10.1176/appi.neuropsych.20240134",

language = "English (US)",

pages = "appineuropsych20240134",

journal = "Journal of Neuropsychiatry and Clinical Neurosciences",

issn = "0895-0172",

publisher = "American Psychiatric Association",

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TY - JOUR

T1 - Hyperorality in Frontotemporal Dementia

T2 - How Psychiatric and Neural Correlates Change During the Disease Course

AU - Morrow, Christopher B

AU - Onyike, Chiadi

AU - Pantelyat, Alexander

AU - Smith, Gwenn S

AU - Leoutsakos, Jeannie

AU - Faria, Andreia V

AU - Graff-Radford, Neill R

AU - Darby, R Ryan

AU - Ghoshal, Nupur

AU - Staffaroni, Adam M

AU - Rascovsky, Katya

AU - Miyagawa, Toji

AU - Balaji, Akshata

AU - Tsapkini, Kyrana

AU - Lapid, Maria I

AU - Mendez, Mario F

AU - Litvan, Irene

AU - Pascual, Belen

AU - ALLFTD consortium

AU - Rojas, Julio C

AU - Wszolek, Zbigniew K

AU - Domoto-Reilly, Kimiko

AU - Kornak, John

AU - Kamath, Vidyulata

PY - 2025/3/26

Y1 - 2025/3/26

N2 - OBJECTIVE: Hyperorality is a core feature of behavioral variant frontotemporal dementia (bvFTD); however, the cognitive, psychiatric, and neuroanatomical correlates of hyperorality across the bvFTD stages remain unclear. The authors explored these associations in early- and advanced-stage bvFTD.METHODS: Participants with sporadic or genetic bvFTD were enrolled in the ARTFL LEFFTDS Longitudinal Frontotemporal Lobar Degeneration (ALLFTD) consortium study. Baseline cognitive and psychiatric symptoms of participants with or without hyperorality were compared after stratification by disease severity. Linear multivariable regressions adjusted for age and total intracranial volume were used to examine associations between regional gray matter volume (GMV) and hyperorality status. Five anatomical regions of interest were preselected for analysis on the basis of previously identified neuroanatomical correlates of hyperorality in bvFTD.RESULTS: Hyperorality was present in 50% of early-stage bvFTD participants (N=136) and was associated with higher rates of ritualistic-compulsive behavior and difficulty detecting social-emotional expressions. Hyperorality was present in 63% of advanced-stage participants (N=208) and was associated with higher rates of apathy, ritualistic-compulsive behavior, and socially aberrant behavior. Regional GMV was similar for those with or without hyperorality among early-stage participants. Among advanced-stage participants, hyperorality was associated with lower GMV in the right dorsal and ventral striatum.CONCLUSIONS: Hyperorality emerged early in bvFTD and was accompanied by deficits in social cognition and complex-ritualistic behavior before clinically significant GMV loss. These findings suggest that early identification and management of hyperorality could improve neuropsychiatric trajectories in bvFTD.

AB - OBJECTIVE: Hyperorality is a core feature of behavioral variant frontotemporal dementia (bvFTD); however, the cognitive, psychiatric, and neuroanatomical correlates of hyperorality across the bvFTD stages remain unclear. The authors explored these associations in early- and advanced-stage bvFTD.METHODS: Participants with sporadic or genetic bvFTD were enrolled in the ARTFL LEFFTDS Longitudinal Frontotemporal Lobar Degeneration (ALLFTD) consortium study. Baseline cognitive and psychiatric symptoms of participants with or without hyperorality were compared after stratification by disease severity. Linear multivariable regressions adjusted for age and total intracranial volume were used to examine associations between regional gray matter volume (GMV) and hyperorality status. Five anatomical regions of interest were preselected for analysis on the basis of previously identified neuroanatomical correlates of hyperorality in bvFTD.RESULTS: Hyperorality was present in 50% of early-stage bvFTD participants (N=136) and was associated with higher rates of ritualistic-compulsive behavior and difficulty detecting social-emotional expressions. Hyperorality was present in 63% of advanced-stage participants (N=208) and was associated with higher rates of apathy, ritualistic-compulsive behavior, and socially aberrant behavior. Regional GMV was similar for those with or without hyperorality among early-stage participants. Among advanced-stage participants, hyperorality was associated with lower GMV in the right dorsal and ventral striatum.CONCLUSIONS: Hyperorality emerged early in bvFTD and was accompanied by deficits in social cognition and complex-ritualistic behavior before clinically significant GMV loss. These findings suggest that early identification and management of hyperorality could improve neuropsychiatric trajectories in bvFTD.

U2 - 10.1176/appi.neuropsych.20240134

DO - 10.1176/appi.neuropsych.20240134

M3 - Article

C2 - 40134270

SN - 0895-0172

SP - appineuropsych20240134

JO - Journal of Neuropsychiatry and Clinical Neurosciences

JF - Journal of Neuropsychiatry and Clinical Neurosciences

ER -

Hyperorality in Frontotemporal Dementia: How Psychiatric and Neural Correlates Change During the Disease Course

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