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November 17, 2020; 95 (20) Article

Neural correlates of naming errors across different neurodegenerative diseases

An FDG-PET study

Eleonora Catricalà, Cristina Polito, Luca Presotto, Valentina Esposito, View ORCID ProfileArianna Sala, Francesca Conca, Celeste Gasparri, Valentina Berti, View ORCID ProfileMassimo Filippi, Alberto Pupi, Sandro Sorbi, Sandro Iannaccone, Giuseppe Magnani, Stefano F. Cappa, Daniela Perani
First published October 1, 2020, DOI: https://doi.org/10.1212/WNL.0000000000010967
Eleonora Catricalà
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Cristina Polito
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Luca Presotto
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Valentina Esposito
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Arianna Sala
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Francesca Conca
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Celeste Gasparri
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Valentina Berti
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Massimo Filippi
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Alberto Pupi
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Sandro Sorbi
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Sandro Iannaccone
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Giuseppe Magnani
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Stefano F. Cappa
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Daniela Perani
From the Faculty of Psychology (E.C., F.C., C.G., S.F.C.), Institute for Advanced Studies, IUSS, Pavia; Nuclear Medicine Unit (C.P., V.B., A.P.), Department of Experimental and Clinical Biomedical Sciences, and NEUROFARBA, Department of Neuroscience, Psychology, Drug Research and Child Health (S.S.), University of Florence; Nuclear Medicine Unit (L.P., A.S., D.P.), IRCCS San Raffaele Hospital, Milan; Faculty of Psychology (V.E., A.S., D.P.), Vita-Salute San Raffaele University, Milan; Department of Neurology and INSPE (M.F., G.M.), San Raffaele Scientific Institute, Milan; Clinical Neuroscience Department (S.I.), San Raffaele Turro Hospital, Milan; IRCCS Fondazione Don Carlo Gnocchi (S.S.), Florence, and IRCCS Fondazione Istituto Neurologico Casimiro Mondino (S.F.C.), Pavia, Italy.
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Citation
Neural correlates of naming errors across different neurodegenerative diseases
An FDG-PET study
Eleonora Catricalà, Cristina Polito, Luca Presotto, Valentina Esposito, Arianna Sala, Francesca Conca, Celeste Gasparri, Valentina Berti, Massimo Filippi, Alberto Pupi, Sandro Sorbi, Sandro Iannaccone, Giuseppe Magnani, Stefano F. Cappa, Daniela Perani
Neurology Nov 2020, 95 (20) e2816-e2830; DOI: 10.1212/WNL.0000000000010967

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Abstract

Objective To investigate the types of errors produced in a picture naming task by patients with neurodegenerative dementia due to different etiologies and their neural correlates.

Methods The same standardized picture naming test was administered to a consecutive sample of patients (n = 148) who had been studied with [18F] FDG-PET. The errors were analyzed in 3 categories (visual, semantic, and phonologic). The PET data were analyzed using an optimized single-subject procedure, and the statistical parametric mapping multiple regression design was used to explore the correlation between each type of error and brain hypometabolism in the whole group. Metabolic connectivity analyses were run at the group level on 7 left hemisphere cortical areas corresponding to an a priori defined naming network.

Results Semantic errors were predominant in most patients, independent of clinical diagnosis. In the whole group analysis, visual errors correlated with hypometabolism in the right inferior occipital lobe and in the left middle occipital lobe. Semantic errors correlated with hypometabolism in the left fusiform gyrus, the inferior and middle temporal gyri, and the temporal pole. Phonologic errors were associated with hypometabolism in the left superior and middle temporal gyri. Both positive (occipital–posterior fusiform) and negative (anterior fusiform gyrus and the superior anterior temporal lobe) connectivity changes were associated with semantic errors.

Conclusions Naming errors reflect the dysfunction of separate stages of the naming process and are specific markers for different patterns of brain involvement. These correlations are not limited to primary progressive aphasia but extend to other neurodegenerative dementias.

Glossary

AAL=
Automated Anatomical Labelling;
AD=
Alzheimer disease;
ATL=
anterior temporal lobe;
bvFTD=
behavioral variant of frontotemporal dementia;
CBS=
corticobasal syndrome;
DLB=
dementia with Lewy bodies;
FDR=
false discovery rate;
FTD=
frontotemporal dementia;
FWE=
familywise error;
IFG=
inferior frontal gyrus;
lvPPA=
logopenic variant of primary progressive aphasia;
nfvPPA=
nonfluent variant of primary progressive aphasia;
PCA=
posterior cortical atrophy;
PPA=
primary progressive aphasia;
PSP=
progressive supranuclear palsy;
ROI=
region of interest;
sATL=
superior anterior temporal lobe;
SPM=
statistical parametric mapping;
svPPA=
semantic variant of primary progressive aphasia

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • ↵* These authors contributed equally to this work.

  • Editorial, page 897

  • Received April 18, 2020.
  • Accepted in final form July 23, 2020.
  • © 2020 American Academy of Neurology
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