Serotonin drives striatal synaptic plasticity in a sex-related manner
Plasticity at corticostriatal synapses is a key substrate for a variety of brain functions – including motor control, learning and reward processing – and is often disrupted in disease conditions. Despite intense research pointing toward a dynamic interplay between glutamate, dopamine (DA), and sero...
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| Published in: | Neurobiology of disease Vol. 158; p. 105448 |
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| Main Authors: | , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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01.10.2021
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| ISSN: | 0969-9961, 1095-953X, 1095-953X |
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| Abstract | Plasticity at corticostriatal synapses is a key substrate for a variety of brain functions – including motor control, learning and reward processing – and is often disrupted in disease conditions. Despite intense research pointing toward a dynamic interplay between glutamate, dopamine (DA), and serotonin (5-HT) neurotransmission, their precise circuit and synaptic mechanisms regulating their role in striatal plasticity are still unclear. Here, we analyze the role of serotonergic raphe-striatal innervation in the regulation of DA-dependent corticostriatal plasticity.
Mice (males and females, 2–6 months of age) were housed in standard plexiglass cages at constant temperature (22 ± 1°C) and maintained on a 12/12h light/dark cycle with food and demineralized water ad libitum. In the present study, we used a knock-in mouse line in which the green fluorescent protein reporter gene (GFP) replaced the I Tph2 exon (Tph2GFP mice), allowing selective expression of GFP in the whole 5-HT system, highlighting both somata and neuritis of serotonergic neurons. Heterozygous, Tph2+/GFP, mice were intercrossed to obtain experimental cohorts, which included Wild-type (Tph2+/+), Heterozygous (Tph2+/GFP), and Mutant serotonin-depleted (Tph2GFP/GFP) animals.
Using male and female mice, carrying on different Tph2 gene dosages, we show that Tph2 gene modulation results in sex-specific corticostriatal abnormalities, encompassing the abnormal amplitude of spontaneous glutamatergic transmission and the loss of Long Term Potentiation (LTP) in Tph2GFP/GFP mice of both sexes, while this form of plasticity is normally expressed in control mice (Tph2+/+). Once LTP is induced, only the Tph2+/GFP female mice present a loss of synaptic depotentiation.
We showed a relevant role of the interaction between dopaminergic and serotonergic systems in controlling striatal synaptic plasticity. Overall, our data unveil that 5-HT plays a primary role in regulating DA-dependent corticostriatal plasticity in a sex-related manner and propose altered 5-HT levels as a critical determinant of disease-associated plasticity defects.
•Tph2 catalyzes the rate-limiting step in 5-HT biosynthesis via subsequent decarboxylation.•Neurotransmitter systems (DA and 5-HT) are differently regulated between sexes.•Serotonergic and dopaminergic interplay modulates synaptic activity within the striatal nucleus.•Tph2 gene dosage exerts a primary role in modulating bidirectional synaptic plasticity in a sex-related manner. |
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| AbstractList | Plasticity at corticostriatal synapses is a key substrate for a variety of brain functions - including motor control, learning and reward processing - and is often disrupted in disease conditions. Despite intense research pointing toward a dynamic interplay between glutamate, dopamine (DA), and serotonin (5-HT) neurotransmission, their precise circuit and synaptic mechanisms regulating their role in striatal plasticity are still unclear. Here, we analyze the role of serotonergic raphe-striatal innervation in the regulation of DA-dependent corticostriatal plasticity.
Mice (males and females, 2-6 months of age) were housed in standard plexiglass cages at constant temperature (22 ± 1°C) and maintained on a 12/12h light/dark cycle with food and demineralized water ad libitum. In the present study, we used a knock-in mouse line in which the green fluorescent protein reporter gene (GFP) replaced the I Tph2 exon (Tph2
mice), allowing selective expression of GFP in the whole 5-HT system, highlighting both somata and neuritis of serotonergic neurons. Heterozygous, Tph2
, mice were intercrossed to obtain experimental cohorts, which included Wild-type (Tph2
), Heterozygous (Tph2
), and Mutant serotonin-depleted (Tph2
) animals.
Using male and female mice, carrying on different Tph2 gene dosages, we show that Tph2 gene modulation results in sex-specific corticostriatal abnormalities, encompassing the abnormal amplitude of spontaneous glutamatergic transmission and the loss of Long Term Potentiation (LTP) in Tph2
mice of both sexes, while this form of plasticity is normally expressed in control mice (Tph2
). Once LTP is induced, only the Tph2
female mice present a loss of synaptic depotentiation.
We showed a relevant role of the interaction between dopaminergic and serotonergic systems in controlling striatal synaptic plasticity. Overall, our data unveil that 5-HT plays a primary role in regulating DA-dependent corticostriatal plasticity in a sex-related manner and propose altered 5-HT levels as a critical determinant of disease-associated plasticity defects. Introduction: Plasticity at corticostriatal synapses is a key substrate for a variety of brain functions – including motor control, learning and reward processing – and is often disrupted in disease conditions. Despite intense research pointing toward a dynamic interplay between glutamate, dopamine (DA), and serotonin (5-HT) neurotransmission, their precise circuit and synaptic mechanisms regulating their role in striatal plasticity are still unclear. Here, we analyze the role of serotonergic raphe-striatal innervation in the regulation of DA-dependent corticostriatal plasticity. Methods: Mice (males and females, 2–6 months of age) were housed in standard plexiglass cages at constant temperature (22 ± 1°C) and maintained on a 12/12h light/dark cycle with food and demineralized water ad libitum. In the present study, we used a knock-in mouse line in which the green fluorescent protein reporter gene (GFP) replaced the I Tph2 exon (Tph2GFP mice), allowing selective expression of GFP in the whole 5-HT system, highlighting both somata and neuritis of serotonergic neurons. Heterozygous, Tph2+/GFP, mice were intercrossed to obtain experimental cohorts, which included Wild-type (Tph2+/+), Heterozygous (Tph2+/GFP), and Mutant serotonin-depleted (Tph2GFP/GFP) animals. Results: Using male and female mice, carrying on different Tph2 gene dosages, we show that Tph2 gene modulation results in sex-specific corticostriatal abnormalities, encompassing the abnormal amplitude of spontaneous glutamatergic transmission and the loss of Long Term Potentiation (LTP) in Tph2GFP/GFP mice of both sexes, while this form of plasticity is normally expressed in control mice (Tph2+/+). Once LTP is induced, only the Tph2+/GFP female mice present a loss of synaptic depotentiation. Conclusion: We showed a relevant role of the interaction between dopaminergic and serotonergic systems in controlling striatal synaptic plasticity. Overall, our data unveil that 5-HT plays a primary role in regulating DA-dependent corticostriatal plasticity in a sex-related manner and propose altered 5-HT levels as a critical determinant of disease-associated plasticity defects. Plasticity at corticostriatal synapses is a key substrate for a variety of brain functions – including motor control, learning and reward processing – and is often disrupted in disease conditions. Despite intense research pointing toward a dynamic interplay between glutamate, dopamine (DA), and serotonin (5-HT) neurotransmission, their precise circuit and synaptic mechanisms regulating their role in striatal plasticity are still unclear. Here, we analyze the role of serotonergic raphe-striatal innervation in the regulation of DA-dependent corticostriatal plasticity. Mice (males and females, 2–6 months of age) were housed in standard plexiglass cages at constant temperature (22 ± 1°C) and maintained on a 12/12h light/dark cycle with food and demineralized water ad libitum. In the present study, we used a knock-in mouse line in which the green fluorescent protein reporter gene (GFP) replaced the I Tph2 exon (Tph2GFP mice), allowing selective expression of GFP in the whole 5-HT system, highlighting both somata and neuritis of serotonergic neurons. Heterozygous, Tph2+/GFP, mice were intercrossed to obtain experimental cohorts, which included Wild-type (Tph2+/+), Heterozygous (Tph2+/GFP), and Mutant serotonin-depleted (Tph2GFP/GFP) animals. Using male and female mice, carrying on different Tph2 gene dosages, we show that Tph2 gene modulation results in sex-specific corticostriatal abnormalities, encompassing the abnormal amplitude of spontaneous glutamatergic transmission and the loss of Long Term Potentiation (LTP) in Tph2GFP/GFP mice of both sexes, while this form of plasticity is normally expressed in control mice (Tph2+/+). Once LTP is induced, only the Tph2+/GFP female mice present a loss of synaptic depotentiation. We showed a relevant role of the interaction between dopaminergic and serotonergic systems in controlling striatal synaptic plasticity. Overall, our data unveil that 5-HT plays a primary role in regulating DA-dependent corticostriatal plasticity in a sex-related manner and propose altered 5-HT levels as a critical determinant of disease-associated plasticity defects. •Tph2 catalyzes the rate-limiting step in 5-HT biosynthesis via subsequent decarboxylation.•Neurotransmitter systems (DA and 5-HT) are differently regulated between sexes.•Serotonergic and dopaminergic interplay modulates synaptic activity within the striatal nucleus.•Tph2 gene dosage exerts a primary role in modulating bidirectional synaptic plasticity in a sex-related manner. Plasticity at corticostriatal synapses is a key substrate for a variety of brain functions - including motor control, learning and reward processing - and is often disrupted in disease conditions. Despite intense research pointing toward a dynamic interplay between glutamate, dopamine (DA), and serotonin (5-HT) neurotransmission, their precise circuit and synaptic mechanisms regulating their role in striatal plasticity are still unclear. Here, we analyze the role of serotonergic raphe-striatal innervation in the regulation of DA-dependent corticostriatal plasticity.INTRODUCTIONPlasticity at corticostriatal synapses is a key substrate for a variety of brain functions - including motor control, learning and reward processing - and is often disrupted in disease conditions. Despite intense research pointing toward a dynamic interplay between glutamate, dopamine (DA), and serotonin (5-HT) neurotransmission, their precise circuit and synaptic mechanisms regulating their role in striatal plasticity are still unclear. Here, we analyze the role of serotonergic raphe-striatal innervation in the regulation of DA-dependent corticostriatal plasticity.Mice (males and females, 2-6 months of age) were housed in standard plexiglass cages at constant temperature (22 ± 1°C) and maintained on a 12/12h light/dark cycle with food and demineralized water ad libitum. In the present study, we used a knock-in mouse line in which the green fluorescent protein reporter gene (GFP) replaced the I Tph2 exon (Tph2GFP mice), allowing selective expression of GFP in the whole 5-HT system, highlighting both somata and neuritis of serotonergic neurons. Heterozygous, Tph2+/GFP, mice were intercrossed to obtain experimental cohorts, which included Wild-type (Tph2+/+), Heterozygous (Tph2+/GFP), and Mutant serotonin-depleted (Tph2GFP/GFP) animals.METHODSMice (males and females, 2-6 months of age) were housed in standard plexiglass cages at constant temperature (22 ± 1°C) and maintained on a 12/12h light/dark cycle with food and demineralized water ad libitum. In the present study, we used a knock-in mouse line in which the green fluorescent protein reporter gene (GFP) replaced the I Tph2 exon (Tph2GFP mice), allowing selective expression of GFP in the whole 5-HT system, highlighting both somata and neuritis of serotonergic neurons. Heterozygous, Tph2+/GFP, mice were intercrossed to obtain experimental cohorts, which included Wild-type (Tph2+/+), Heterozygous (Tph2+/GFP), and Mutant serotonin-depleted (Tph2GFP/GFP) animals.Using male and female mice, carrying on different Tph2 gene dosages, we show that Tph2 gene modulation results in sex-specific corticostriatal abnormalities, encompassing the abnormal amplitude of spontaneous glutamatergic transmission and the loss of Long Term Potentiation (LTP) in Tph2GFP/GFP mice of both sexes, while this form of plasticity is normally expressed in control mice (Tph2+/+). Once LTP is induced, only the Tph2+/GFP female mice present a loss of synaptic depotentiation.RESULTSUsing male and female mice, carrying on different Tph2 gene dosages, we show that Tph2 gene modulation results in sex-specific corticostriatal abnormalities, encompassing the abnormal amplitude of spontaneous glutamatergic transmission and the loss of Long Term Potentiation (LTP) in Tph2GFP/GFP mice of both sexes, while this form of plasticity is normally expressed in control mice (Tph2+/+). Once LTP is induced, only the Tph2+/GFP female mice present a loss of synaptic depotentiation.We showed a relevant role of the interaction between dopaminergic and serotonergic systems in controlling striatal synaptic plasticity. Overall, our data unveil that 5-HT plays a primary role in regulating DA-dependent corticostriatal plasticity in a sex-related manner and propose altered 5-HT levels as a critical determinant of disease-associated plasticity defects.CONCLUSIONWe showed a relevant role of the interaction between dopaminergic and serotonergic systems in controlling striatal synaptic plasticity. Overall, our data unveil that 5-HT plays a primary role in regulating DA-dependent corticostriatal plasticity in a sex-related manner and propose altered 5-HT levels as a critical determinant of disease-associated plasticity defects. |
| ArticleNumber | 105448 |
| Author | Maddaloni, Giacomo Usiello, Alessandro Calabresi, Paolo Pasqualetti, Massimo Picconi, Barbara Campanelli, Federica Calabrese, Valeria Marino, Gioia Barsotti, Noemi Ghiglieri, Veronica Natale, Giuseppina Cardinale, Antonella |
| Author_xml | – sequence: 1 givenname: Federica surname: Campanelli fullname: Campanelli, Federica organization: Laboratory of Neurophysiology, Santa Lucia Foundation IRCCS, Rome 00143, Italy – sequence: 2 givenname: Gioia surname: Marino fullname: Marino, Gioia organization: Laboratory of Neurophysiology, Santa Lucia Foundation IRCCS, Rome 00143, Italy – sequence: 3 givenname: Noemi surname: Barsotti fullname: Barsotti, Noemi organization: Department of Biology Unit of Cell and Developmental Biology, University of Pisa, Pisa 56127, Italy – sequence: 4 givenname: Giuseppina surname: Natale fullname: Natale, Giuseppina organization: Laboratory of Neurophysiology, Santa Lucia Foundation IRCCS, Rome 00143, Italy – sequence: 5 givenname: Valeria surname: Calabrese fullname: Calabrese, Valeria organization: Department of Medicine, Università degli Studi di Perugia, Perugia 06123, Italy – sequence: 6 givenname: Antonella surname: Cardinale fullname: Cardinale, Antonella organization: Department of Neuroscience, Università Cattolica del Sacro Cuore, Rome 00168, Italy – sequence: 7 givenname: Veronica surname: Ghiglieri fullname: Ghiglieri, Veronica organization: Università Telematica San Raffaele, Rome 00166, Italy – sequence: 8 givenname: Giacomo surname: Maddaloni fullname: Maddaloni, Giacomo organization: Department of Biology Unit of Cell and Developmental Biology, University of Pisa, Pisa 56127, Italy – sequence: 9 givenname: Alessandro surname: Usiello fullname: Usiello, Alessandro organization: Department of Environmental, Biological and Pharmaceutical Sciences and Technologies, University of Campania, Luigi Vanvitelli, Caserta 81100, Italy – sequence: 10 givenname: Paolo surname: Calabresi fullname: Calabresi, Paolo organization: Department of Neuroscience, Università Cattolica del Sacro Cuore, Rome 00168, Italy – sequence: 11 givenname: Massimo surname: Pasqualetti fullname: Pasqualetti, Massimo organization: Department of Biology Unit of Cell and Developmental Biology, University of Pisa, Pisa 56127, Italy – sequence: 12 givenname: Barbara surname: Picconi fullname: Picconi, Barbara email: barbara.picconi@uniroma5.it organization: Laboratory Experimental Neurophysiology, IRCCS San Raffaele Pisana, Rome 00166, Italy |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34280523$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_2174_011570159X336597241217062042 crossref_primary_10_1016_j_neuro_2023_12_007 crossref_primary_10_3389_fnins_2022_994735 crossref_primary_10_1016_j_heliyon_2024_e38192 crossref_primary_10_3390_brainsci14050514 |
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| Keywords | Tph2 Striatum Dopamine Functional recovery Serotonin Synaptic plasticity |
| Language | English |
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| Snippet | Plasticity at corticostriatal synapses is a key substrate for a variety of brain functions – including motor control, learning and reward processing – and is... Plasticity at corticostriatal synapses is a key substrate for a variety of brain functions - including motor control, learning and reward processing - and is... Introduction: Plasticity at corticostriatal synapses is a key substrate for a variety of brain functions – including motor control, learning and reward... |
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| SubjectTerms | Animals Animals, Genetically Modified Dopamine Electrophysiological Phenomena Female Functional recovery Glutamic Acid - physiology Long-Term Potentiation Male Mice Neostriatum - physiology Nerve Fibers Neuronal Plasticity - physiology Parkinson Disease, Secondary - physiopathology Serotonin Serotonin - physiology Sex Characteristics Striatum Synapses - physiology Synaptic plasticity Synaptic Transmission - physiology Tph2 Tryptophan Hydroxylase - metabolism |
| Title | Serotonin drives striatal synaptic plasticity in a sex-related manner |
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