Transcranial magnetic stimulation of the precuneus enhances memory and neural activity in prodromal Alzheimer's disease

Memory loss is one of the first symptoms of typical Alzheimer's disease (AD), for which there are no effective therapies available. The precuneus (PC) has been recently emphasized as a key area for the memory impairment observed in early AD, likely due to disconnection mechanisms within large-s...

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Published in:	NeuroImage (Orlando, Fla.) Vol. 169; pp. 302 - 311
Main Authors:	Koch, Giacomo, Bonnì, Sonia, Pellicciari, Maria Concetta, Casula, Elias P., Mancini, Matteo, Esposito, Romina, Ponzo, Viviana, Picazio, Silvia, Di Lorenzo, Francesco, Serra, Laura, Motta, Caterina, Maiella, Michele, Marra, Camillo, Cercignani, Mara, Martorana, Alessandro, Caltagirone, Carlo, Bozzali, Marco
Format:	Journal Article
Language:	English
Published:	United States Elsevier Inc 01.04.2018 Elsevier Limited
Subjects:	Aged Alzheimer Disease - physiopathology Alzheimer's disease Beta Rhythm - physiology Cognitive ability Cortex (parietal) Dementia EEG Family medical history Female Functional Neuroimaging - methods Humans Magnetic fields Male Medical imaging Memory Memory Disorders - physiopathology Memory, Episodic Neural networks Neurodegenerative diseases Oscillations Parietal Lobe - physiopathology Patients Precuneus Prodromal Symptoms Studies Transcranial magnetic stimulation Transcranial Magnetic Stimulation - methods Italy PPC MRI Memory MNI LTP FDI sLORETA DSST SD GMFP MMSE CSF Precuneus ISI AD Transcranial magnetic stimulation DMN EEG FAB ERSP RAVLT IAF TF PC TEPs RMT ADCS-PACC ITC rTMS
ISSN:	1053-8119, 1095-9572, 1095-9572
Online Access:	Get full text
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Abstract	Memory loss is one of the first symptoms of typical Alzheimer's disease (AD), for which there are no effective therapies available. The precuneus (PC) has been recently emphasized as a key area for the memory impairment observed in early AD, likely due to disconnection mechanisms within large-scale networks such as the default mode network (DMN). Using a multimodal approach we investigated in a two-week, randomized, sham-controlled, double-blinded trial the effects of high-frequency repetitive transcranial magnetic stimulation (rTMS) of the PC on cognition, as measured by the Alzheimer Disease Cooperative Study Preclinical Alzheimer Cognitive Composite in 14 patients with early AD (7 females). TMS combined with electroencephalography (TMS-EEG) was used to detect changes in brain connectivity. We found that rTMS of the PC induced a selective improvement in episodic memory, but not in other cognitive domains. Analysis of TMS-EEG signal revealed an increase of neural activity in patients' PC, an enhancement of brain oscillations in the beta band and a modification of functional connections between the PC and medial frontal areas within the DMN. Our findings show that high-frequency rTMS of the PC is a promising, non-invasive treatment for memory dysfunction in patients at early stages of AD. This clinical improvement is accompanied by modulation of brain connectivity, consistently with the pathophysiological model of brain disconnection in AD. •The precuneus is a key area for memory impairment in Alzheimer’s disease (AD).•We investigated the effects of precuneus-rTMS on memory in patients with early AD.•Precuneus-rTMS induced a selective improvement in episodic memory.•Precuneus-rTMS enhance precuneus activity and connectivity with frontal areas.•Precuneus-rTMS is a promising treatment for memory dysfunction in early AD patients.
AbstractList	Memory loss is one of the first symptoms of typical Alzheimer's disease (AD), for which there are no effective therapies available. The precuneus (PC) has been recently emphasized as a key area for the memory impairment observed in early AD, likely due to disconnection mechanisms within large-scale networks such as the default mode network (DMN). Using a multimodal approach we investigated in a two-week, randomized, sham-controlled, double-blinded trial the effects of high-frequency repetitive transcranial magnetic stimulation (rTMS) of the PC on cognition, as measured by the Alzheimer Disease Cooperative Study Preclinical Alzheimer Cognitive Composite in 14 patients with early AD (7 females). TMS combined with electroencephalography (TMS-EEG) was used to detect changes in brain connectivity. We found that rTMS of the PC induced a selective improvement in episodic memory, but not in other cognitive domains. Analysis of TMS-EEG signal revealed an increase of neural activity in patients' PC, an enhancement of brain oscillations in the beta band and a modification of functional connections between the PC and medial frontal areas within the DMN. Our findings show that high-frequency rTMS of the PC is a promising, non-invasive treatment for memory dysfunction in patients at early stages of AD. This clinical improvement is accompanied by modulation of brain connectivity, consistently with the pathophysiological model of brain disconnection in AD. •The precuneus is a key area for memory impairment in Alzheimer’s disease (AD).•We investigated the effects of precuneus-rTMS on memory in patients with early AD.•Precuneus-rTMS induced a selective improvement in episodic memory.•Precuneus-rTMS enhance precuneus activity and connectivity with frontal areas.•Precuneus-rTMS is a promising treatment for memory dysfunction in early AD patients. Memory loss is one of the first symptoms of typical Alzheimer's disease (AD), for which there are no effective therapies available. The precuneus (PC) has been recently emphasized as a key area for the memory impairment observed in early AD, likely due to disconnection mechanisms within large-scale networks such as the default mode network (DMN). Using a multimodal approach we investigated in a two-week, randomized, sham-controlled, double-blinded trial the effects of high-frequency repetitive transcranial magnetic stimulation (rTMS) of the PC on cognition, as measured by the Alzheimer Disease Cooperative Study Preclinical Alzheimer Cognitive Composite in 14 patients with early AD (7 females). TMS combined with electroencephalography (TMS-EEG) was used to detect changes in brain connectivity. We found that rTMS of the PC induced a selective improvement in episodic memory, but not in other cognitive domains. Analysis of TMS-EEG signal revealed an increase of neural activity in patients' PC, an enhancement of brain oscillations in the beta band and a modification of functional connections between the PC and medial frontal areas within the DMN.Our findings show that high-frequency rTMS of the PC is a promising, non-invasive treatment for memory dysfunction in patients at early stages of AD. This clinical improvement is accompanied by modulation of brain connectivity, consistently with the pathophysiological model of brain disconnection in AD. Memory loss is one of the first symptoms of typical Alzheimer's disease (AD), for which there are no effective therapies available. The precuneus (PC) has been recently emphasized as a key area for the memory impairment observed in early AD, likely due to disconnection mechanisms within large-scale networks such as the default mode network (DMN). Using a multimodal approach we investigated in a two-week, randomized, sham-controlled, double-blinded trial the effects of high-frequency repetitive transcranial magnetic stimulation (rTMS) of the PC on cognition, as measured by the Alzheimer Disease Cooperative Study Preclinical Alzheimer Cognitive Composite in 14 patients with early AD (7 females). TMS combined with electroencephalography (TMS-EEG) was used to detect changes in brain connectivity. We found that rTMS of the PC induced a selective improvement in episodic memory, but not in other cognitive domains. Analysis of TMS-EEG signal revealed an increase of neural activity in patients' PC, an enhancement of brain oscillations in the beta band and a modification of functional connections between the PC and medial frontal areas within the DMN. Our findings show that high-frequency rTMS of the PC is a promising, non-invasive treatment for memory dysfunction in patients at early stages of AD. This clinical improvement is accompanied by modulation of brain connectivity, consistently with the pathophysiological model of brain disconnection in AD.Memory loss is one of the first symptoms of typical Alzheimer's disease (AD), for which there are no effective therapies available. The precuneus (PC) has been recently emphasized as a key area for the memory impairment observed in early AD, likely due to disconnection mechanisms within large-scale networks such as the default mode network (DMN). Using a multimodal approach we investigated in a two-week, randomized, sham-controlled, double-blinded trial the effects of high-frequency repetitive transcranial magnetic stimulation (rTMS) of the PC on cognition, as measured by the Alzheimer Disease Cooperative Study Preclinical Alzheimer Cognitive Composite in 14 patients with early AD (7 females). TMS combined with electroencephalography (TMS-EEG) was used to detect changes in brain connectivity. We found that rTMS of the PC induced a selective improvement in episodic memory, but not in other cognitive domains. Analysis of TMS-EEG signal revealed an increase of neural activity in patients' PC, an enhancement of brain oscillations in the beta band and a modification of functional connections between the PC and medial frontal areas within the DMN. Our findings show that high-frequency rTMS of the PC is a promising, non-invasive treatment for memory dysfunction in patients at early stages of AD. This clinical improvement is accompanied by modulation of brain connectivity, consistently with the pathophysiological model of brain disconnection in AD.
Author	Cercignani, Mara Esposito, Romina Di Lorenzo, Francesco Bonnì, Sonia Martorana, Alessandro Caltagirone, Carlo Mancini, Matteo Bozzali, Marco Ponzo, Viviana Picazio, Silvia Serra, Laura Motta, Caterina Koch, Giacomo Casula, Elias P. Marra, Camillo Pellicciari, Maria Concetta Maiella, Michele
Author_xml	– sequence: 1 givenname: Giacomo surname: Koch fullname: Koch, Giacomo email: g.koch@hsantalucia.it organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 2 givenname: Sonia surname: Bonnì fullname: Bonnì, Sonia organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 3 givenname: Maria Concetta surname: Pellicciari fullname: Pellicciari, Maria Concetta organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 4 givenname: Elias P. surname: Casula fullname: Casula, Elias P. organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 5 givenname: Matteo surname: Mancini fullname: Mancini, Matteo organization: Neuroimaging Laboratory, Santa Lucia Foundation, IRCCS, Rome, 00179, Italy – sequence: 6 givenname: Romina surname: Esposito fullname: Esposito, Romina organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 7 givenname: Viviana surname: Ponzo fullname: Ponzo, Viviana organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 8 givenname: Silvia surname: Picazio fullname: Picazio, Silvia organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 9 givenname: Francesco surname: Di Lorenzo fullname: Di Lorenzo, Francesco organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 10 givenname: Laura surname: Serra fullname: Serra, Laura organization: Neuroimaging Laboratory, Santa Lucia Foundation, IRCCS, Rome, 00179, Italy – sequence: 11 givenname: Caterina surname: Motta fullname: Motta, Caterina organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 12 givenname: Michele surname: Maiella fullname: Maiella, Michele organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 13 givenname: Camillo surname: Marra fullname: Marra, Camillo organization: Memory Clinic, Neurology Department, Catholic University of Rome, Italy – sequence: 14 givenname: Mara surname: Cercignani fullname: Cercignani, Mara organization: Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, Brighton BN1 9RR, East Sussex, UK – sequence: 15 givenname: Alessandro surname: Martorana fullname: Martorana, Alessandro organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 16 givenname: Carlo surname: Caltagirone fullname: Caltagirone, Carlo organization: Non Invasive Brain Stimulation Unit/Department of Behavioral and Clinical Neurology, Santa Lucia Foundation IRCCS, Via Ardeatina 354, 00179, Rome, Italy – sequence: 17 givenname: Marco surname: Bozzali fullname: Bozzali, Marco email: m.bozzali@bsms.ac.uk organization: Neuroimaging Laboratory, Santa Lucia Foundation, IRCCS, Rome, 00179, Italy
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Snippet	Memory loss is one of the first symptoms of typical Alzheimer's disease (AD), for which there are no effective therapies available. The precuneus (PC) has been...
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SubjectTerms	Aged Alzheimer Disease - physiopathology Alzheimer's disease Beta Rhythm - physiology Cognitive ability Cortex (parietal) Dementia EEG Family medical history Female Functional Neuroimaging - methods Humans Magnetic fields Male Medical imaging Memory Memory Disorders - physiopathology Memory, Episodic Neural networks Neurodegenerative diseases Oscillations Parietal Lobe - physiopathology Patients Precuneus Prodromal Symptoms Studies Transcranial magnetic stimulation Transcranial Magnetic Stimulation - methods
Title	Transcranial magnetic stimulation of the precuneus enhances memory and neural activity in prodromal Alzheimer's disease
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