Distribution of serotonin 5-HT1A-binding sites in the brainstem and the hypothalamus, and their roles in 5-HT-induced sleep and ingestive behaviors in rock pigeons (Columba livia)

•5-HT1AR was found in brainstem 5-HT areas and in the hypothalamus of pigeons.•ICV 5-HT or DPAT evokes drinking, sleep, and c-Fos expression in these areas.•5-HT1AR heteroreceptor antagonist blocks 5-HT- and DPAT-evoked drinking and sleep.•5-HT-specific neurotoxin 5,7-DHT does not alter 5-HT activit...

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Veröffentlicht in:Behavioural brain research 2015-12, Vol.295, p.45-63
Hauptverfasser: dos Santos, Tiago Souza, Krüger, Jéssica, Melleu, Fernando Falkenburger, Herold, Christina, Zilles, Karl, Poli, Anicleto, Güntürkün, Onur, Marino-Neto, José
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container_title Behavioural brain research
container_volume 295
creator dos Santos, Tiago Souza
Krüger, Jéssica
Melleu, Fernando Falkenburger
Herold, Christina
Zilles, Karl
Poli, Anicleto
Güntürkün, Onur
Marino-Neto, José
description •5-HT1AR was found in brainstem 5-HT areas and in the hypothalamus of pigeons.•ICV 5-HT or DPAT evokes drinking, sleep, and c-Fos expression in these areas.•5-HT1AR heteroreceptor antagonist blocks 5-HT- and DPAT-evoked drinking and sleep.•5-HT-specific neurotoxin 5,7-DHT does not alter 5-HT activity but does increase sleep.•5-HT1ARs play crucial but complex roles in ingestive and postprandial behavior. Serotonin 1A receptors (5-HT1ARs), which are widely distributed in the mammalian brain, participate in cognitive and emotional functions. In birds, 5-HT1ARs are expressed in prosencephalic areas involved in visual and cognitive functions. Diverse evidence supports 5-HT1AR-mediated 5-HT-induced ingestive and sleep behaviors in birds. Here, we describe the distribution of 5-HT1ARs in the hypothalamus and brainstem of birds, analyze their potential roles in sleep and ingestive behaviors, and attempt to determine the involvement of auto-/hetero-5-HT1ARs in these behaviors. In 6 pigeons, the anatomical distribution of [3H]8-OH-DPAT binding in the rostral brainstem and hypothalamus was examined. Ingestive/sleep behaviors were recorded (1h) in 16 pigeons pretreated with MM77 (a heterosynaptic 5-HT1AR antagonist; 23 or 69nmol) for 20min, followed by intracerebroventricular ICV injection of 5-HT (N:8; 150nmol), 8-OH-DPAT (DPAT, a 5-HT1A,7R agonist, 30nmol N:8) or vehicle. 5-HT- and DPAT-induced sleep and ingestive behaviors, brainstem 5-HT neuronal density and brain 5-HT content were examined in 12 pigeons, pretreated by ICV with the 5-HT neurotoxin 5,7-dihydroxytryptamine (5,7-DHT) or vehicle (N:6/group). The distribution of brainstem and diencephalic c-Fos immunoreactivity after ICV injection of 5-HT, DPAT or vehicle (N:5/group) into birds provided with or denied access to water is also described. 5-HT1ARs are concentrated in the brainstem 5-HTergic areas and throughout the periventricular hypothalamus, preoptic nuclei and circumventricular organs. 5-HT and DPAT produced a complex c-Fos expression pattern in the 5-HT1AR-enriched preoptic hypothalamus and the circumventricular organs, which are related to drinking and sleep regulation, but modestly affected c-Fos expression in 5-HTergic neurons. The 5-HT-induced ingestivebehaviors and the 5-HT- and DPAT-induced sleep behaviors were reduced by MM77 pretreatment. 5,7-DHT increased sleep per se, decreased tryptophan hydroxylase expression in the raphe nuclei and decreased prosencephalic 5-HT release but failed to affe
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Serotonin 1A receptors (5-HT1ARs), which are widely distributed in the mammalian brain, participate in cognitive and emotional functions. In birds, 5-HT1ARs are expressed in prosencephalic areas involved in visual and cognitive functions. Diverse evidence supports 5-HT1AR-mediated 5-HT-induced ingestive and sleep behaviors in birds. Here, we describe the distribution of 5-HT1ARs in the hypothalamus and brainstem of birds, analyze their potential roles in sleep and ingestive behaviors, and attempt to determine the involvement of auto-/hetero-5-HT1ARs in these behaviors. In 6 pigeons, the anatomical distribution of [3H]8-OH-DPAT binding in the rostral brainstem and hypothalamus was examined. Ingestive/sleep behaviors were recorded (1h) in 16 pigeons pretreated with MM77 (a heterosynaptic 5-HT1AR antagonist; 23 or 69nmol) for 20min, followed by intracerebroventricular ICV injection of 5-HT (N:8; 150nmol), 8-OH-DPAT (DPAT, a 5-HT1A,7R agonist, 30nmol N:8) or vehicle. 5-HT- and DPAT-induced sleep and ingestive behaviors, brainstem 5-HT neuronal density and brain 5-HT content were examined in 12 pigeons, pretreated by ICV with the 5-HT neurotoxin 5,7-dihydroxytryptamine (5,7-DHT) or vehicle (N:6/group). The distribution of brainstem and diencephalic c-Fos immunoreactivity after ICV injection of 5-HT, DPAT or vehicle (N:5/group) into birds provided with or denied access to water is also described. 5-HT1ARs are concentrated in the brainstem 5-HTergic areas and throughout the periventricular hypothalamus, preoptic nuclei and circumventricular organs. 5-HT and DPAT produced a complex c-Fos expression pattern in the 5-HT1AR-enriched preoptic hypothalamus and the circumventricular organs, which are related to drinking and sleep regulation, but modestly affected c-Fos expression in 5-HTergic neurons. The 5-HT-induced ingestivebehaviors and the 5-HT- and DPAT-induced sleep behaviors were reduced by MM77 pretreatment. 5,7-DHT increased sleep per se, decreased tryptophan hydroxylase expression in the raphe nuclei and decreased prosencephalic 5-HT release but failed to affect 5-HT- or DPAT-induced drinking or sleep behavior. 5-HT- and DPAT-induced ingestive and sleep behaviors in pigeons appear to be mediated by heterosynaptic and/or non-somatodendritic presynaptic 5-HT1ARs localized to periventricular diencephalic circuits.</description><identifier>ISSN: 0166-4328</identifier><identifier>EISSN: 1872-7549</identifier><identifier>DOI: 10.1016/j.bbr.2015.03.059</identifier><identifier>PMID: 25843559</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>5,7-Dihydroxytryptamine - pharmacology ; 5-HT-1A receptor ; 8-Hydroxy-2-(di-n-propylamino)tetralin - pharmacology ; Animals ; Binding Sites ; Brain Stem - drug effects ; Brain Stem - metabolism ; Cerebrospinal fluid ; Columba livia ; Columbidae - metabolism ; Drinking ; Feeding ; Feeding Behavior - drug effects ; Female ; Hypothalamus - metabolism ; Male ; Raphe Nuclei - metabolism ; Receptor, Serotonin, 5-HT1A - metabolism ; Receptors, Serotonin ; Serotonin ; Serotonin - metabolism ; Serotonin Receptor Agonists - pharmacology ; Sleep ; Sleep - drug effects ; Sleep - physiology ; Sleep Aids, Pharmaceutical</subject><ispartof>Behavioural brain research, 2015-12, Vol.295, p.45-63</ispartof><rights>2015 Elsevier B.V.</rights><rights>Copyright © 2015 Elsevier B.V. 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Serotonin 1A receptors (5-HT1ARs), which are widely distributed in the mammalian brain, participate in cognitive and emotional functions. In birds, 5-HT1ARs are expressed in prosencephalic areas involved in visual and cognitive functions. Diverse evidence supports 5-HT1AR-mediated 5-HT-induced ingestive and sleep behaviors in birds. Here, we describe the distribution of 5-HT1ARs in the hypothalamus and brainstem of birds, analyze their potential roles in sleep and ingestive behaviors, and attempt to determine the involvement of auto-/hetero-5-HT1ARs in these behaviors. In 6 pigeons, the anatomical distribution of [3H]8-OH-DPAT binding in the rostral brainstem and hypothalamus was examined. Ingestive/sleep behaviors were recorded (1h) in 16 pigeons pretreated with MM77 (a heterosynaptic 5-HT1AR antagonist; 23 or 69nmol) for 20min, followed by intracerebroventricular ICV injection of 5-HT (N:8; 150nmol), 8-OH-DPAT (DPAT, a 5-HT1A,7R agonist, 30nmol N:8) or vehicle. 5-HT- and DPAT-induced sleep and ingestive behaviors, brainstem 5-HT neuronal density and brain 5-HT content were examined in 12 pigeons, pretreated by ICV with the 5-HT neurotoxin 5,7-dihydroxytryptamine (5,7-DHT) or vehicle (N:6/group). The distribution of brainstem and diencephalic c-Fos immunoreactivity after ICV injection of 5-HT, DPAT or vehicle (N:5/group) into birds provided with or denied access to water is also described. 5-HT1ARs are concentrated in the brainstem 5-HTergic areas and throughout the periventricular hypothalamus, preoptic nuclei and circumventricular organs. 5-HT and DPAT produced a complex c-Fos expression pattern in the 5-HT1AR-enriched preoptic hypothalamus and the circumventricular organs, which are related to drinking and sleep regulation, but modestly affected c-Fos expression in 5-HTergic neurons. The 5-HT-induced ingestivebehaviors and the 5-HT- and DPAT-induced sleep behaviors were reduced by MM77 pretreatment. 5,7-DHT increased sleep per se, decreased tryptophan hydroxylase expression in the raphe nuclei and decreased prosencephalic 5-HT release but failed to affect 5-HT- or DPAT-induced drinking or sleep behavior. 5-HT- and DPAT-induced ingestive and sleep behaviors in pigeons appear to be mediated by heterosynaptic and/or non-somatodendritic presynaptic 5-HT1ARs localized to periventricular diencephalic circuits.</description><subject>5,7-Dihydroxytryptamine - pharmacology</subject><subject>5-HT-1A receptor</subject><subject>8-Hydroxy-2-(di-n-propylamino)tetralin - pharmacology</subject><subject>Animals</subject><subject>Binding Sites</subject><subject>Brain Stem - drug effects</subject><subject>Brain Stem - metabolism</subject><subject>Cerebrospinal fluid</subject><subject>Columba livia</subject><subject>Columbidae - metabolism</subject><subject>Drinking</subject><subject>Feeding</subject><subject>Feeding Behavior - drug effects</subject><subject>Female</subject><subject>Hypothalamus - metabolism</subject><subject>Male</subject><subject>Raphe Nuclei - metabolism</subject><subject>Receptor, Serotonin, 5-HT1A - metabolism</subject><subject>Receptors, Serotonin</subject><subject>Serotonin</subject><subject>Serotonin - metabolism</subject><subject>Serotonin Receptor Agonists - pharmacology</subject><subject>Sleep</subject><subject>Sleep - drug effects</subject><subject>Sleep - physiology</subject><subject>Sleep Aids, Pharmaceutical</subject><issn>0166-4328</issn><issn>1872-7549</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo1kc1u1DAURiMEotPCA7BBXhaJBP_EcSxW1UApUiU2ZW059k3HQ2IH2xmpz8UL4plpV1f6dO7R1f2q6gPBDcGk-7JvhiE2FBPeYNZgLl9VG9ILWgveytfVpjBd3TLaX1SXKe0xxi3m5G11QXnfMs7lpvr3zaUc3bBmFzwKI0oQQw7eecTruwdyUw_OW-cfUXIZEip53gEaonY-ZZiR9vaU7J6WkHd60vOaPr-kLqIYpvPaUVcX12rAojQBLCeqqCFldyhO2OmDC_FEx2D-oMU9QvAJXW_DtM6DRpM7OP3pXfVm1FOC98_zqvp9-_1he1ff__rxc3tzXwPrulyb3lgNve1ba3RPKVgrxChGjC2TdKCcadF2bBwNl8ZiKY3sRT8SrpkkAo_sqro-e5cY_q7lSjW7ZGCatIewJkUE45JSyUVBPz6j6zCDVUt0s45P6uXRBfh6BqAcfHAQVTIOfPmFi2CyssEpgtWxVrVXpVZ1rFVhpkqt7D9P5pcu</recordid><startdate>20151215</startdate><enddate>20151215</enddate><creator>dos Santos, Tiago Souza</creator><creator>Krüger, Jéssica</creator><creator>Melleu, Fernando Falkenburger</creator><creator>Herold, Christina</creator><creator>Zilles, Karl</creator><creator>Poli, Anicleto</creator><creator>Güntürkün, Onur</creator><creator>Marino-Neto, José</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QG</scope><scope>7TK</scope></search><sort><creationdate>20151215</creationdate><title>Distribution of serotonin 5-HT1A-binding sites in the brainstem and the hypothalamus, and their roles in 5-HT-induced sleep and ingestive behaviors in rock pigeons (Columba livia)</title><author>dos Santos, Tiago Souza ; 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Serotonin 1A receptors (5-HT1ARs), which are widely distributed in the mammalian brain, participate in cognitive and emotional functions. In birds, 5-HT1ARs are expressed in prosencephalic areas involved in visual and cognitive functions. Diverse evidence supports 5-HT1AR-mediated 5-HT-induced ingestive and sleep behaviors in birds. Here, we describe the distribution of 5-HT1ARs in the hypothalamus and brainstem of birds, analyze their potential roles in sleep and ingestive behaviors, and attempt to determine the involvement of auto-/hetero-5-HT1ARs in these behaviors. In 6 pigeons, the anatomical distribution of [3H]8-OH-DPAT binding in the rostral brainstem and hypothalamus was examined. Ingestive/sleep behaviors were recorded (1h) in 16 pigeons pretreated with MM77 (a heterosynaptic 5-HT1AR antagonist; 23 or 69nmol) for 20min, followed by intracerebroventricular ICV injection of 5-HT (N:8; 150nmol), 8-OH-DPAT (DPAT, a 5-HT1A,7R agonist, 30nmol N:8) or vehicle. 5-HT- and DPAT-induced sleep and ingestive behaviors, brainstem 5-HT neuronal density and brain 5-HT content were examined in 12 pigeons, pretreated by ICV with the 5-HT neurotoxin 5,7-dihydroxytryptamine (5,7-DHT) or vehicle (N:6/group). The distribution of brainstem and diencephalic c-Fos immunoreactivity after ICV injection of 5-HT, DPAT or vehicle (N:5/group) into birds provided with or denied access to water is also described. 5-HT1ARs are concentrated in the brainstem 5-HTergic areas and throughout the periventricular hypothalamus, preoptic nuclei and circumventricular organs. 5-HT and DPAT produced a complex c-Fos expression pattern in the 5-HT1AR-enriched preoptic hypothalamus and the circumventricular organs, which are related to drinking and sleep regulation, but modestly affected c-Fos expression in 5-HTergic neurons. The 5-HT-induced ingestivebehaviors and the 5-HT- and DPAT-induced sleep behaviors were reduced by MM77 pretreatment. 5,7-DHT increased sleep per se, decreased tryptophan hydroxylase expression in the raphe nuclei and decreased prosencephalic 5-HT release but failed to affect 5-HT- or DPAT-induced drinking or sleep behavior. 5-HT- and DPAT-induced ingestive and sleep behaviors in pigeons appear to be mediated by heterosynaptic and/or non-somatodendritic presynaptic 5-HT1ARs localized to periventricular diencephalic circuits.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>25843559</pmid><doi>10.1016/j.bbr.2015.03.059</doi><tpages>19</tpages></addata></record>
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subjects 5,7-Dihydroxytryptamine - pharmacology
5-HT-1A receptor
8-Hydroxy-2-(di-n-propylamino)tetralin - pharmacology
Animals
Binding Sites
Brain Stem - drug effects
Brain Stem - metabolism
Cerebrospinal fluid
Columba livia
Columbidae - metabolism
Drinking
Feeding
Feeding Behavior - drug effects
Female
Hypothalamus - metabolism
Male
Raphe Nuclei - metabolism
Receptor, Serotonin, 5-HT1A - metabolism
Receptors, Serotonin
Serotonin
Serotonin - metabolism
Serotonin Receptor Agonists - pharmacology
Sleep
Sleep - drug effects
Sleep - physiology
Sleep Aids, Pharmaceutical
title Distribution of serotonin 5-HT1A-binding sites in the brainstem and the hypothalamus, and their roles in 5-HT-induced sleep and ingestive behaviors in rock pigeons (Columba livia)
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