Cognitive performance in aged rats is associated with differences in distinctive neuronal populations in the ventral tegmental area and altered synaptic plasticity in the hippocampus
IntroductionDeterioration of cognitive functions is commonly associated with aging, although there is wide variation in the onset and manifestation. Albeit heterogeneity in age-related cognitive decline has been studied at the cellular and molecular level, there is poor evidence for electrophysiolog...
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| Format: | Article |
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Frontiers Media S.A.
2024-02-01
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| Series: | Frontiers in Aging Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnagi.2024.1357347/full |
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| author | Claudia Sagheddu Tamara Stojanovic Shima Kouhnavardi Shima Kouhnavardi Artem Savchenko Artem Savchenko Ahmed M. Hussein Ahmed M. Hussein Ahmed M. Hussein Marco Pistis Marco Pistis Marco Pistis Francisco J. Monje Roberto Plasenzotti Mohammed Aufy Christian R. Studenik Jana Lubec Gert Lubec |
| author_facet | Claudia Sagheddu Tamara Stojanovic Shima Kouhnavardi Shima Kouhnavardi Artem Savchenko Artem Savchenko Ahmed M. Hussein Ahmed M. Hussein Ahmed M. Hussein Marco Pistis Marco Pistis Marco Pistis Francisco J. Monje Roberto Plasenzotti Mohammed Aufy Christian R. Studenik Jana Lubec Gert Lubec |
| author_sort | Claudia Sagheddu |
| collection | DOAJ |
| description | IntroductionDeterioration of cognitive functions is commonly associated with aging, although there is wide variation in the onset and manifestation. Albeit heterogeneity in age-related cognitive decline has been studied at the cellular and molecular level, there is poor evidence for electrophysiological correlates. The aim of the current study was to address the electrophysiological basis of heterogeneity of cognitive functions in cognitively Inferior and Superior old (19-20 months) rats in the ventral tegmental area (VTA) and the hippocampus, having Young (12 weeks) rats as a control. The midbrain VTA operates as a hub amidst affective and cognitive facets, processing sensory inputs related to motivated behaviours and hippocampal memory. Increasing evidence shows direct dopaminergic and non-dopaminergic input from the VTA to the hippocampus.MethodsAged Superior and Inferior male rats were selected from a cohort of 88 animals based on their performance in a spatial learning and memory task. Using in vivo single-cell recording in the VTA, we examined the electrical activity of different neuronal populations (putative dopaminergic, glutamatergic and GABAergic neurons). In the same animals, basal synaptic transmission and synaptic plasticity were examined in hippocampal slices.ResultsElectrophysiological recordings from the VTA and hippocampus showed alterations associated with aging per se, together with differences specifically linked to the cognitive status of aged animals. In particular, the bursting activity of dopamine neurons was lower, while the firing frequency of glutamatergic neurons was higher in VTA of Inferior old rats. The response to high-frequency stimulation in hippocampal slices also discriminated between Superior and Inferior aged animals.DiscussionThis study provides new insight into electrophysiological information underlying compromised cerebral ageing. Further understanding of brain senescence, possibly related to neurocognitive decline, will help develop new strategies towards the preservation of a high quality of life. |
| first_indexed | 2024-03-07T21:36:37Z |
| format | Article |
| id | doaj.art-71955093d7d1495cbc30f67de0923ba9 |
| institution | Directory Open Access Journal |
| issn | 1663-4365 |
| language | English |
| last_indexed | 2024-03-07T21:36:37Z |
| publishDate | 2024-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Aging Neuroscience |
| spelling | doaj.art-71955093d7d1495cbc30f67de0923ba92024-02-26T12:10:09ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652024-02-011610.3389/fnagi.2024.13573471357347Cognitive performance in aged rats is associated with differences in distinctive neuronal populations in the ventral tegmental area and altered synaptic plasticity in the hippocampusClaudia Sagheddu0Tamara Stojanovic1Shima Kouhnavardi2Shima Kouhnavardi3Artem Savchenko4Artem Savchenko5Ahmed M. Hussein6Ahmed M. Hussein7Ahmed M. Hussein8Marco Pistis9Marco Pistis10Marco Pistis11Francisco J. Monje12Roberto Plasenzotti13Mohammed Aufy14Christian R. Studenik15Jana Lubec16Gert Lubec17Division of Neuroscience and Clinical Pharmacology, Department of Biomedical Sciences, University of Cagliari, Monserrato, ItalyProgramme for Proteomics, Paracelsus Medical University, Salzburg, AustriaProgramme for Proteomics, Paracelsus Medical University, Salzburg, AustriaDivision of Pharmacology and Toxicology, Department of Pharmaceutical Sciences, University of Vienna, Vienna, AustriaProgramme for Proteomics, Paracelsus Medical University, Salzburg, AustriaInstitute of Pharmacology, Pavlov First Saint Petersburg State Medical University, St. Petersburg, RussiaProgramme for Proteomics, Paracelsus Medical University, Salzburg, AustriaDivision of Pharmacology and Toxicology, Department of Pharmaceutical Sciences, University of Vienna, Vienna, AustriaDepartment of Zoology, Faculty of Science, Al-Azhar University, Asyut, EgyptDivision of Neuroscience and Clinical Pharmacology, Department of Biomedical Sciences, University of Cagliari, Monserrato, ItalySection of Cagliari, Neuroscience Institute National Research Council of Italy (CNR), Cagliari, ItalyUnit of Clinical Pharmacology, University Hospital, Cagliari, ItalyCenter for Physiology and Pharmacology, Department of Neurophysiology and Neuropharmacology, Medical University of Vienna, Vienna, AustriaDivision of Biomedical Research, Medical University of Vienna, Vienna, AustriaDivision of Pharmacology and Toxicology, Department of Pharmaceutical Sciences, University of Vienna, Vienna, AustriaDivision of Pharmacology and Toxicology, Department of Pharmaceutical Sciences, University of Vienna, Vienna, AustriaProgramme for Proteomics, Paracelsus Medical University, Salzburg, AustriaProgramme for Proteomics, Paracelsus Medical University, Salzburg, AustriaIntroductionDeterioration of cognitive functions is commonly associated with aging, although there is wide variation in the onset and manifestation. Albeit heterogeneity in age-related cognitive decline has been studied at the cellular and molecular level, there is poor evidence for electrophysiological correlates. The aim of the current study was to address the electrophysiological basis of heterogeneity of cognitive functions in cognitively Inferior and Superior old (19-20 months) rats in the ventral tegmental area (VTA) and the hippocampus, having Young (12 weeks) rats as a control. The midbrain VTA operates as a hub amidst affective and cognitive facets, processing sensory inputs related to motivated behaviours and hippocampal memory. Increasing evidence shows direct dopaminergic and non-dopaminergic input from the VTA to the hippocampus.MethodsAged Superior and Inferior male rats were selected from a cohort of 88 animals based on their performance in a spatial learning and memory task. Using in vivo single-cell recording in the VTA, we examined the electrical activity of different neuronal populations (putative dopaminergic, glutamatergic and GABAergic neurons). In the same animals, basal synaptic transmission and synaptic plasticity were examined in hippocampal slices.ResultsElectrophysiological recordings from the VTA and hippocampus showed alterations associated with aging per se, together with differences specifically linked to the cognitive status of aged animals. In particular, the bursting activity of dopamine neurons was lower, while the firing frequency of glutamatergic neurons was higher in VTA of Inferior old rats. The response to high-frequency stimulation in hippocampal slices also discriminated between Superior and Inferior aged animals.DiscussionThis study provides new insight into electrophysiological information underlying compromised cerebral ageing. Further understanding of brain senescence, possibly related to neurocognitive decline, will help develop new strategies towards the preservation of a high quality of life.https://www.frontiersin.org/articles/10.3389/fnagi.2024.1357347/fulldopamineLTPlearning and memoryin vivo electrophysiologyVTA GABAergic and VTA glutamatergic neuronsdementia |
| spellingShingle | Claudia Sagheddu Tamara Stojanovic Shima Kouhnavardi Shima Kouhnavardi Artem Savchenko Artem Savchenko Ahmed M. Hussein Ahmed M. Hussein Ahmed M. Hussein Marco Pistis Marco Pistis Marco Pistis Francisco J. Monje Roberto Plasenzotti Mohammed Aufy Christian R. Studenik Jana Lubec Gert Lubec Cognitive performance in aged rats is associated with differences in distinctive neuronal populations in the ventral tegmental area and altered synaptic plasticity in the hippocampus Frontiers in Aging Neuroscience dopamine LTP learning and memory in vivo electrophysiology VTA GABAergic and VTA glutamatergic neurons dementia |
| title | Cognitive performance in aged rats is associated with differences in distinctive neuronal populations in the ventral tegmental area and altered synaptic plasticity in the hippocampus |
| title_full | Cognitive performance in aged rats is associated with differences in distinctive neuronal populations in the ventral tegmental area and altered synaptic plasticity in the hippocampus |
| title_fullStr | Cognitive performance in aged rats is associated with differences in distinctive neuronal populations in the ventral tegmental area and altered synaptic plasticity in the hippocampus |
| title_full_unstemmed | Cognitive performance in aged rats is associated with differences in distinctive neuronal populations in the ventral tegmental area and altered synaptic plasticity in the hippocampus |
| title_short | Cognitive performance in aged rats is associated with differences in distinctive neuronal populations in the ventral tegmental area and altered synaptic plasticity in the hippocampus |
| title_sort | cognitive performance in aged rats is associated with differences in distinctive neuronal populations in the ventral tegmental area and altered synaptic plasticity in the hippocampus |
| topic | dopamine LTP learning and memory in vivo electrophysiology VTA GABAergic and VTA glutamatergic neurons dementia |
| url | https://www.frontiersin.org/articles/10.3389/fnagi.2024.1357347/full |
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