Repetitive prefrontal tDCS activates VTA dopaminergic neurons, resulting in attenuation of Alzheimer’s Disease-like deficits in Tg2576 mice

Abstract Background Emerging evidence implicates early dysfunction of dopaminergic neurons in the Ventral Tegmental Area (VTA) as a key contributor to Alzheimer’s Disease (AD) pathophysiology. Specifically, the VTA dopaminergic neurodegeneration and the consequent reduction of dopamine (DA) in mesoc...

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Main Authors: Maria Luisa De Paolis, Gilda Loffredo, Paraskevi Krashia, Livia La Barbera, Annalisa Nobili, Emma Cauzzi, Lucy Babicola, Matteo Di Segni, Roberto Coccurello, Stefano Puglisi-Allegra, Emanuele Claudio Latagliata, Marcello D’Amelio
Format: Article
Language:English
Published: BMC 2025-04-01
Series:Alzheimer’s Research & Therapy
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Online Access:https://doi.org/10.1186/s13195-025-01736-4
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author Maria Luisa De Paolis
Gilda Loffredo
Paraskevi Krashia
Livia La Barbera
Annalisa Nobili
Emma Cauzzi
Lucy Babicola
Matteo Di Segni
Roberto Coccurello
Stefano Puglisi-Allegra
Emanuele Claudio Latagliata
Marcello D’Amelio
author_facet Maria Luisa De Paolis
Gilda Loffredo
Paraskevi Krashia
Livia La Barbera
Annalisa Nobili
Emma Cauzzi
Lucy Babicola
Matteo Di Segni
Roberto Coccurello
Stefano Puglisi-Allegra
Emanuele Claudio Latagliata
Marcello D’Amelio
author_sort Maria Luisa De Paolis
collection DOAJ
description Abstract Background Emerging evidence implicates early dysfunction of dopaminergic neurons in the Ventral Tegmental Area (VTA) as a key contributor to Alzheimer’s Disease (AD) pathophysiology. Specifically, the VTA dopaminergic neurodegeneration and the consequent reduction of dopamine (DA) in mesocorticolimbic targets are associated with the onset of cognitive impairments and neuropsychiatric-like manifestations in AD animal models. Moreover, decreased midbrain volume and functional VTA disconnection are identified as predictors of accelerated progression from Mild Cognitive Impairment to AD-dementia in clinical populations. Given these findings, interventions capable of directly modulating VTA activity and augmenting DA release, despite the ongoing neurodegeneration, may hold therapeutic potential for mitigating DA-related deficits in AD. This study aims at evaluating the therapeutic potential of prefrontal transcranial Direct Current Stimulation (tDCS) in the Tg2576 mouse model of AD, exhibiting early VTA dopaminergic neurodegeneration. Methods Repeated tDCS was applied to assess its ability to activate VTA DA neurons. We also evaluated tDCS effects on synaptic plasticity, cognitive and non-cognitive behaviours and AD-related pathology. Hippocampal DA release and Nucleus Accumbens (NAc) DA transporter (DAT) expression were measured. With immunohistochemistry we examined microglial density and morphological complexity at different disease stages. Additionally, intracellular amyloid-β (Aβ) levels and plaque burden were evaluated to determine the impact of tDCS on AD pathology. Results Prefrontal tDCS enhanced the activity of VTA dopaminergic neurons, leading to increased hippocampal DA release and higher DAT levels in the NAc. The enhanced DA outflow is associated with restored CA3-CA1 synaptic plasticity and improvements in recognition memory and motivational behaviours. tDCS reduced microglial numbers and morphological complexity in Tg2576 mice at both pre-plaque stage (7-months) and at an advanced stage characterized by plaque accumulation (12-months). Notably, tDCS also decreased Aβ plaque burden, although no changes in intracellular Aβ levels were observed in younger Tg2576 mice. Conclusions These findings highlight the multifaceted therapeutic potential of prefrontal tDCS in targeting key AD pathophysiological hallmarks, including dopaminergic dysfunction, synaptic impairments, neuroinflammation and plaque deposition. As a non-invasive neuromodulatory approach, prefrontal tDCS emerges as a promising early intervention strategy to complement existing AD treatments, with the potential to improve patient outcomes and quality of life.
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spelling doaj-art-dbd5aac94d754fb1a9df60710d0d0b742025-08-20T01:47:33ZengBMCAlzheimer’s Research & Therapy1758-91932025-04-0117112010.1186/s13195-025-01736-4Repetitive prefrontal tDCS activates VTA dopaminergic neurons, resulting in attenuation of Alzheimer’s Disease-like deficits in Tg2576 miceMaria Luisa De Paolis0Gilda Loffredo1Paraskevi Krashia2Livia La Barbera3Annalisa Nobili4Emma Cauzzi5Lucy Babicola6Matteo Di Segni7Roberto Coccurello8Stefano Puglisi-Allegra9Emanuele Claudio Latagliata10Marcello D’Amelio11Department of Medicine and Surgery, Università Campus Bio-Medico Di RomaDepartment of Medicine and Surgery, Università Campus Bio-Medico Di RomaDepartment of Sciences and Technologies for Sustainable Development and One Health, Università Campus Bio-Medico Di RomaDepartment of Medicine and Surgery, Università Campus Bio-Medico Di RomaDepartment of Medicine and Surgery, Università Campus Bio-Medico Di RomaDepartment of Medicine and Surgery, Università Campus Bio-Medico Di RomaDepartment of Experimental Neurosciences, IRCCS Santa Lucia FoundationChild Psychopathology Unit, IRCCS Eugenio MedeaDepartment of Experimental Neurosciences, IRCCS Santa Lucia FoundationIstituto Di Ricovero E Cura a Carattere Scientifico (IRCCS) NeuromedDepartment of Experimental Neurosciences, IRCCS Santa Lucia FoundationDepartment of Medicine and Surgery, Università Campus Bio-Medico Di RomaAbstract Background Emerging evidence implicates early dysfunction of dopaminergic neurons in the Ventral Tegmental Area (VTA) as a key contributor to Alzheimer’s Disease (AD) pathophysiology. Specifically, the VTA dopaminergic neurodegeneration and the consequent reduction of dopamine (DA) in mesocorticolimbic targets are associated with the onset of cognitive impairments and neuropsychiatric-like manifestations in AD animal models. Moreover, decreased midbrain volume and functional VTA disconnection are identified as predictors of accelerated progression from Mild Cognitive Impairment to AD-dementia in clinical populations. Given these findings, interventions capable of directly modulating VTA activity and augmenting DA release, despite the ongoing neurodegeneration, may hold therapeutic potential for mitigating DA-related deficits in AD. This study aims at evaluating the therapeutic potential of prefrontal transcranial Direct Current Stimulation (tDCS) in the Tg2576 mouse model of AD, exhibiting early VTA dopaminergic neurodegeneration. Methods Repeated tDCS was applied to assess its ability to activate VTA DA neurons. We also evaluated tDCS effects on synaptic plasticity, cognitive and non-cognitive behaviours and AD-related pathology. Hippocampal DA release and Nucleus Accumbens (NAc) DA transporter (DAT) expression were measured. With immunohistochemistry we examined microglial density and morphological complexity at different disease stages. Additionally, intracellular amyloid-β (Aβ) levels and plaque burden were evaluated to determine the impact of tDCS on AD pathology. Results Prefrontal tDCS enhanced the activity of VTA dopaminergic neurons, leading to increased hippocampal DA release and higher DAT levels in the NAc. The enhanced DA outflow is associated with restored CA3-CA1 synaptic plasticity and improvements in recognition memory and motivational behaviours. tDCS reduced microglial numbers and morphological complexity in Tg2576 mice at both pre-plaque stage (7-months) and at an advanced stage characterized by plaque accumulation (12-months). Notably, tDCS also decreased Aβ plaque burden, although no changes in intracellular Aβ levels were observed in younger Tg2576 mice. Conclusions These findings highlight the multifaceted therapeutic potential of prefrontal tDCS in targeting key AD pathophysiological hallmarks, including dopaminergic dysfunction, synaptic impairments, neuroinflammation and plaque deposition. As a non-invasive neuromodulatory approach, prefrontal tDCS emerges as a promising early intervention strategy to complement existing AD treatments, with the potential to improve patient outcomes and quality of life.https://doi.org/10.1186/s13195-025-01736-4Transcranial Direct Current StimulationNeuromodulation techniquesMesocorticolimbic systemDementiaHippocampusCognitive decline
spellingShingle Maria Luisa De Paolis
Gilda Loffredo
Paraskevi Krashia
Livia La Barbera
Annalisa Nobili
Emma Cauzzi
Lucy Babicola
Matteo Di Segni
Roberto Coccurello
Stefano Puglisi-Allegra
Emanuele Claudio Latagliata
Marcello D’Amelio
Repetitive prefrontal tDCS activates VTA dopaminergic neurons, resulting in attenuation of Alzheimer’s Disease-like deficits in Tg2576 mice
Alzheimer’s Research & Therapy
Transcranial Direct Current Stimulation
Neuromodulation techniques
Mesocorticolimbic system
Dementia
Hippocampus
Cognitive decline
title Repetitive prefrontal tDCS activates VTA dopaminergic neurons, resulting in attenuation of Alzheimer’s Disease-like deficits in Tg2576 mice
title_full Repetitive prefrontal tDCS activates VTA dopaminergic neurons, resulting in attenuation of Alzheimer’s Disease-like deficits in Tg2576 mice
title_fullStr Repetitive prefrontal tDCS activates VTA dopaminergic neurons, resulting in attenuation of Alzheimer’s Disease-like deficits in Tg2576 mice
title_full_unstemmed Repetitive prefrontal tDCS activates VTA dopaminergic neurons, resulting in attenuation of Alzheimer’s Disease-like deficits in Tg2576 mice
title_short Repetitive prefrontal tDCS activates VTA dopaminergic neurons, resulting in attenuation of Alzheimer’s Disease-like deficits in Tg2576 mice
title_sort repetitive prefrontal tdcs activates vta dopaminergic neurons resulting in attenuation of alzheimer s disease like deficits in tg2576 mice
topic Transcranial Direct Current Stimulation
Neuromodulation techniques
Mesocorticolimbic system
Dementia
Hippocampus
Cognitive decline
url https://doi.org/10.1186/s13195-025-01736-4
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