Long-Term Shaping of Corticostriatal Synaptic Activity by Acute Fasting

Food restriction is a robust nongenic, nonsurgical and nonpharmacologic intervention known to improve health and extend lifespan in various species. Food is considered the most essential and frequently consumed natural reward, and current observations have demonstrated homeostatic responses and neur...

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Vydané v:	International journal of molecular sciences Ročník 22; číslo 4; s. 1916
Hlavní autori:	Campanelli, Federica, Laricchiuta, Daniela, Natale, Giuseppina, Marino, Gioia, Calabrese, Valeria, Picconi, Barbara, Petrosini, Laura, Calabresi, Paolo, Ghiglieri, Veronica
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	Switzerland MDPI AG 15.02.2021 MDPI
Predmet:	Animal cognition Animals Corpus Striatum - metabolism Diet Therapy Dopamine - metabolism Fasting Fasting - physiology Food Food Deprivation - physiology Glutamic Acid - metabolism Male Mice Mice, Inbred C57BL Neuronal Plasticity - physiology Neurons - metabolism Protocol Receptors, AMPA - metabolism Synapses Synapses - metabolism Synaptic Transmission - physiology dorsolateral striatum GluA1 dietary restriction calcium-permeable AMPA naphthyl-acetyl spermine food deprivation
ISSN:	1422-0067, 1661-6596, 1422-0067
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Abstract	Food restriction is a robust nongenic, nonsurgical and nonpharmacologic intervention known to improve health and extend lifespan in various species. Food is considered the most essential and frequently consumed natural reward, and current observations have demonstrated homeostatic responses and neuroadaptations to sustained intermittent or chronic deprivation. Results obtained to date indicate that food deprivation affects glutamatergic synapses, favoring the insertion of GluA2-lacking α-Ammino-3-idrossi-5-Metil-4-idrossazol-Propionic Acid receptors (AMPARs) in postsynaptic membranes. Despite an increasing number of studies pointing towards specific changes in response to dietary restrictions in brain regions, such as the nucleus accumbens and hippocampus, none have investigated the long-term effects of such practice in the dorsal striatum. This basal ganglia nucleus is involved in habit formation and in eating behavior, especially that based on dopaminergic control of motivation for food in both humans and animals. Here, we explored whether we could retrieve long-term signs of changes in AMPARs subunit composition in dorsal striatal neurons of mice acutely deprived for 12 hours/day for two consecutive days by analyzing glutamatergic neurotransmission and the principal forms of dopamine and glutamate-dependent synaptic plasticity. Overall, our data show that a moderate food deprivation in experimental animals is a salient event mirrored by a series of neuroadaptations and suggest that dietary restriction may be determinant in shaping striatal synaptic plasticity in the physiological state.
AbstractList	Food restriction is a robust nongenic, nonsurgical and nonpharmacologic intervention known to improve health and extend lifespan in various species. Food is considered the most essential and frequently consumed natural reward, and current observations have demonstrated homeostatic responses and neuroadaptations to sustained intermittent or chronic deprivation. Results obtained to date indicate that food deprivation affects glutamatergic synapses, favoring the insertion of GluA2-lacking α-Ammino-3-idrossi-5-Metil-4-idrossazol-Propionic Acid receptors (AMPARs) in postsynaptic membranes. Despite an increasing number of studies pointing towards specific changes in response to dietary restrictions in brain regions, such as the nucleus accumbens and hippocampus, none have investigated the long-term effects of such practice in the dorsal striatum. This basal ganglia nucleus is involved in habit formation and in eating behavior, especially that based on dopaminergic control of motivation for food in both humans and animals. Here, we explored whether we could retrieve long-term signs of changes in AMPARs subunit composition in dorsal striatal neurons of mice acutely deprived for 12 hours/day for two consecutive days by analyzing glutamatergic neurotransmission and the principal forms of dopamine and glutamate-dependent synaptic plasticity. Overall, our data show that a moderate food deprivation in experimental animals is a salient event mirrored by a series of neuroadaptations and suggest that dietary restriction may be determinant in shaping striatal synaptic plasticity in the physiological state. Food restriction is a robust nongenic, nonsurgical and nonpharmacologic intervention known to improve health and extend lifespan in various species. Food is considered the most essential and frequently consumed natural reward, and current observations have demonstrated homeostatic responses and neuroadaptations to sustained intermittent or chronic deprivation. Results obtained to date indicate that food deprivation affects glutamatergic synapses, favoring the insertion of GluA2-lacking α-Ammino-3-idrossi-5-Metil-4-idrossazol-Propionic Acid receptors (AMPARs) in postsynaptic membranes. Despite an increasing number of studies pointing towards specific changes in response to dietary restrictions in brain regions, such as the nucleus accumbens and hippocampus, none have investigated the long-term effects of such practice in the dorsal striatum. This basal ganglia nucleus is involved in habit formation and in eating behavior, especially that based on dopaminergic control of motivation for food in both humans and animals. Here, we explored whether we could retrieve long-term signs of changes in AMPARs subunit composition in dorsal striatal neurons of mice acutely deprived for 12 hours/day for two consecutive days by analyzing glutamatergic neurotransmission and the principal forms of dopamine and glutamate-dependent synaptic plasticity. Overall, our data show that a moderate food deprivation in experimental animals is a salient event mirrored by a series of neuroadaptations and suggest that dietary restriction may be determinant in shaping striatal synaptic plasticity in the physiological state.Food restriction is a robust nongenic, nonsurgical and nonpharmacologic intervention known to improve health and extend lifespan in various species. Food is considered the most essential and frequently consumed natural reward, and current observations have demonstrated homeostatic responses and neuroadaptations to sustained intermittent or chronic deprivation. Results obtained to date indicate that food deprivation affects glutamatergic synapses, favoring the insertion of GluA2-lacking α-Ammino-3-idrossi-5-Metil-4-idrossazol-Propionic Acid receptors (AMPARs) in postsynaptic membranes. Despite an increasing number of studies pointing towards specific changes in response to dietary restrictions in brain regions, such as the nucleus accumbens and hippocampus, none have investigated the long-term effects of such practice in the dorsal striatum. This basal ganglia nucleus is involved in habit formation and in eating behavior, especially that based on dopaminergic control of motivation for food in both humans and animals. Here, we explored whether we could retrieve long-term signs of changes in AMPARs subunit composition in dorsal striatal neurons of mice acutely deprived for 12 hours/day for two consecutive days by analyzing glutamatergic neurotransmission and the principal forms of dopamine and glutamate-dependent synaptic plasticity. Overall, our data show that a moderate food deprivation in experimental animals is a salient event mirrored by a series of neuroadaptations and suggest that dietary restriction may be determinant in shaping striatal synaptic plasticity in the physiological state.
Author	Petrosini, Laura Calabresi, Paolo Picconi, Barbara Campanelli, Federica Calabrese, Valeria Marino, Gioia Laricchiuta, Daniela Ghiglieri, Veronica Natale, Giuseppina
AuthorAffiliation	4 IRCCS San Raffaele Pisana, Rome 00176, Italy; barbara.picconi@uniroma5.it 2 Dipartimento di Neuroscienze, Facoltà di Medicina e Chirurgia, Università Cattolica del Sacro Cuore, 00168 Rome, Italy; paolo.calabresi@policlinicogemelli.it 5 Università Telematica San Raffaele, 00166 Rome, Italy 6 Clinica Neurologica, Fondazione Policlinico Universitario Agostino Gemelli IRCCS, 00168 Rome, Italy 1 Dipartmento di Medicina, Università di Perugia, 06129 Perugia, Italy; federica.campanelli@unicatt.it (F.C.); giuseppina.natale@studenti.unipg.it (G.N.); gioia.marino@gmail.com (G.M.); valeria.calabrese@sanraffaele.it (V.C.) 3 Laboratorio di Neurofisiologia Sperimentale e del Comportamento, IRCCS Fondazione Santa Lucia c/o CERC, 00143 Rome, Italy; daniela.laricchiuta@gmail.com (D.L.); laura.petrosini@uniroma1.it (L.P.)
AuthorAffiliation_xml	– name: 6 Clinica Neurologica, Fondazione Policlinico Universitario Agostino Gemelli IRCCS, 00168 Rome, Italy – name: 5 Università Telematica San Raffaele, 00166 Rome, Italy – name: 3 Laboratorio di Neurofisiologia Sperimentale e del Comportamento, IRCCS Fondazione Santa Lucia c/o CERC, 00143 Rome, Italy; daniela.laricchiuta@gmail.com (D.L.); laura.petrosini@uniroma1.it (L.P.) – name: 4 IRCCS San Raffaele Pisana, Rome 00176, Italy; barbara.picconi@uniroma5.it – name: 1 Dipartmento di Medicina, Università di Perugia, 06129 Perugia, Italy; federica.campanelli@unicatt.it (F.C.); giuseppina.natale@studenti.unipg.it (G.N.); gioia.marino@gmail.com (G.M.); valeria.calabrese@sanraffaele.it (V.C.) – name: 2 Dipartimento di Neuroscienze, Facoltà di Medicina e Chirurgia, Università Cattolica del Sacro Cuore, 00168 Rome, Italy; paolo.calabresi@policlinicogemelli.it
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Keywords	dorsolateral striatum GluA1 dietary restriction calcium-permeable AMPA naphthyl-acetyl spermine food deprivation
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Snippet	Food restriction is a robust nongenic, nonsurgical and nonpharmacologic intervention known to improve health and extend lifespan in various species. Food is...
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SubjectTerms	Animal cognition Animals Corpus Striatum - metabolism Diet Therapy Dopamine - metabolism Fasting Fasting - physiology Food Food Deprivation - physiology Glutamic Acid - metabolism Male Mice Mice, Inbred C57BL Neuronal Plasticity - physiology Neurons - metabolism Protocol Receptors, AMPA - metabolism Synapses Synapses - metabolism Synaptic Transmission - physiology
Title	Long-Term Shaping of Corticostriatal Synaptic Activity by Acute Fasting
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