Gonadal Steroids Maintain 24 h Acetylcholine Release in the Hippocampus: Organizational and Activational Effects in Behaving Rats
Extracellular acetylcholine (ACh) levels in the dorsal hippocampus increases during learning or exploration, exhibiting a sex-specific 24 h release profile. To examine the activational effect of gonadal steroid hormones on the sex-specific ACh levels and its correlation with spontaneous locomotor ac...
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| Veröffentlicht in: | The Journal of neuroscience 2009-03, Vol.29 (12), p.3808-3815 |
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| creator | Mitsushima, Dai Takase, Kenkichi Funabashi, Toshiya Kimura, Fukuko |
| description | Extracellular acetylcholine (ACh) levels in the dorsal hippocampus increases during learning or exploration, exhibiting a sex-specific 24 h release profile. To examine the activational effect of gonadal steroid hormones on the sex-specific ACh levels and its correlation with spontaneous locomotor activity, we observed these parameters simultaneously for 24 h. Gonadectomy severely attenuated the ACh levels, whereas the testosterone replacement in gonadectomized males or 17beta-estradiol replacement in gonadectomized females successfully restored the levels. 17beta-Estradiol-priming in gonadectomized males could not restore the ACh levels, and testosterone replacement in gonadectomized females failed to raise ACh levels to those seen in testosterone-primed gonadectomized males, revealing a sex-specific activational effect. Spontaneous locomotor activity was not changed in males by gonadectomy or the replacement of gonadal steroids, but 17beta-estradiol enhanced the activity in gonadectomized females. Gonadectomy severely reduced the correlation between ACh release and activity levels, but the testosterone replacement in gonadectomized males or 17beta-estradiol replacement in gonadectomized females successfully restored it. To further analyze the sex-specific effect of gonadal steroids, we examined the organizational effect of gonadal steroids on the ACh release in female rats. Neonatal testosterone or 17beta-estradiol treatment not only increased the ACh levels but also altered them to resemble male-specific ACh release properties without affecting levels of spontaneous locomotor activity. We conclude that the activational effects of gonadal steroids maintaining the ACh levels and the high correlation with spontaneous locomotor activity are sex-specific, and that the organizational effects of gonadal steroids suggest estrogen receptor-mediated masculinization of the septo-hippocampal cholinergic system. |
| doi_str_mv | 10.1523/JNEUROSCI.5301-08.2009 |
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To examine the activational effect of gonadal steroid hormones on the sex-specific ACh levels and its correlation with spontaneous locomotor activity, we observed these parameters simultaneously for 24 h. Gonadectomy severely attenuated the ACh levels, whereas the testosterone replacement in gonadectomized males or 17beta-estradiol replacement in gonadectomized females successfully restored the levels. 17beta-Estradiol-priming in gonadectomized males could not restore the ACh levels, and testosterone replacement in gonadectomized females failed to raise ACh levels to those seen in testosterone-primed gonadectomized males, revealing a sex-specific activational effect. Spontaneous locomotor activity was not changed in males by gonadectomy or the replacement of gonadal steroids, but 17beta-estradiol enhanced the activity in gonadectomized females. Gonadectomy severely reduced the correlation between ACh release and activity levels, but the testosterone replacement in gonadectomized males or 17beta-estradiol replacement in gonadectomized females successfully restored it. To further analyze the sex-specific effect of gonadal steroids, we examined the organizational effect of gonadal steroids on the ACh release in female rats. Neonatal testosterone or 17beta-estradiol treatment not only increased the ACh levels but also altered them to resemble male-specific ACh release properties without affecting levels of spontaneous locomotor activity. We conclude that the activational effects of gonadal steroids maintaining the ACh levels and the high correlation with spontaneous locomotor activity are sex-specific, and that the organizational effects of gonadal steroids suggest estrogen receptor-mediated masculinization of the septo-hippocampal cholinergic system.</description><identifier>ISSN: 0270-6474</identifier><identifier>ISSN: 1529-2401</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.5301-08.2009</identifier><identifier>PMID: 19321777</identifier><language>eng</language><publisher>United States: Soc Neuroscience</publisher><subject>Acetylcholine - metabolism ; Animals ; Animals, Newborn ; Estradiol - pharmacology ; Extracellular Space - metabolism ; Female ; Gonadal Hormones - pharmacology ; Hippocampus - drug effects ; Hippocampus - metabolism ; Male ; Motor Activity ; Orchiectomy ; Ovariectomy ; Rats ; Sex Differentiation ; Sex Factors ; Testosterone - pharmacology</subject><ispartof>The Journal of neuroscience, 2009-03, Vol.29 (12), p.3808-3815</ispartof><rights>Copyright © 2009 Society for Neuroscience 0270-6474/09/293808-08$15.00/0 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c563t-ca772af010306dcd0972b04745a0779d8fd06854e43c1d3a088974cd0d20cee93</citedby><cites>FETCH-LOGICAL-c563t-ca772af010306dcd0972b04745a0779d8fd06854e43c1d3a088974cd0d20cee93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6665029/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6665029/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19321777$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mitsushima, Dai</creatorcontrib><creatorcontrib>Takase, Kenkichi</creatorcontrib><creatorcontrib>Funabashi, Toshiya</creatorcontrib><creatorcontrib>Kimura, Fukuko</creatorcontrib><title>Gonadal Steroids Maintain 24 h Acetylcholine Release in the Hippocampus: Organizational and Activational Effects in Behaving Rats</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Extracellular acetylcholine (ACh) levels in the dorsal hippocampus increases during learning or exploration, exhibiting a sex-specific 24 h release profile. To examine the activational effect of gonadal steroid hormones on the sex-specific ACh levels and its correlation with spontaneous locomotor activity, we observed these parameters simultaneously for 24 h. Gonadectomy severely attenuated the ACh levels, whereas the testosterone replacement in gonadectomized males or 17beta-estradiol replacement in gonadectomized females successfully restored the levels. 17beta-Estradiol-priming in gonadectomized males could not restore the ACh levels, and testosterone replacement in gonadectomized females failed to raise ACh levels to those seen in testosterone-primed gonadectomized males, revealing a sex-specific activational effect. Spontaneous locomotor activity was not changed in males by gonadectomy or the replacement of gonadal steroids, but 17beta-estradiol enhanced the activity in gonadectomized females. Gonadectomy severely reduced the correlation between ACh release and activity levels, but the testosterone replacement in gonadectomized males or 17beta-estradiol replacement in gonadectomized females successfully restored it. To further analyze the sex-specific effect of gonadal steroids, we examined the organizational effect of gonadal steroids on the ACh release in female rats. Neonatal testosterone or 17beta-estradiol treatment not only increased the ACh levels but also altered them to resemble male-specific ACh release properties without affecting levels of spontaneous locomotor activity. We conclude that the activational effects of gonadal steroids maintaining the ACh levels and the high correlation with spontaneous locomotor activity are sex-specific, and that the organizational effects of gonadal steroids suggest estrogen receptor-mediated masculinization of the septo-hippocampal cholinergic system.</description><subject>Acetylcholine - metabolism</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Estradiol - pharmacology</subject><subject>Extracellular Space - metabolism</subject><subject>Female</subject><subject>Gonadal Hormones - pharmacology</subject><subject>Hippocampus - drug effects</subject><subject>Hippocampus - metabolism</subject><subject>Male</subject><subject>Motor Activity</subject><subject>Orchiectomy</subject><subject>Ovariectomy</subject><subject>Rats</subject><subject>Sex Differentiation</subject><subject>Sex Factors</subject><subject>Testosterone - pharmacology</subject><issn>0270-6474</issn><issn>1529-2401</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkV9v0zAUxS0EYmXwFSY_wVPKtZ3ECQ9Ioyrb0KBSx54tz7lpjJw_i91W423ffI5aBjxYlnx-51zbh5AzBnOWcfHx24_l7Xp1s7iaZwJYAsWcA5QvyCyqZcJTYC_JDLiEJE9lekLeeP8LACQw-ZqcsFJwJqWckceLvtOVdvQm4NjbytPv2nYhLspT2tBzg-HBmaZ3tkO6RofaI41qaJBe2mHojW6Hrf9EV-NGd_a3DjYmOqq7KpqD3f05WNY1muAn7xds9M52G7rWwb8lr2rtPL477qfk9uvy5-IyuV5dXC3OrxOT5SIkRkvJdQ0MBOSVqaCU_A7i2zINUpZVUVeQF1mKqTCsEhqKopRp5CoOBrEUp-TzIXfY3rVYGezCqJ0aRtvq8UH12qr_lc42atPvVJ7nGfAp4P0xYOzvt-iDaq036JzusN96lUso4veyCOYH0Iy99yPWz0MYqKk99dyemtpTUKipvWg8-_eKf23HuiLw4QA0dtPs7YjKt9q5iDO13-95qRhXooBCPAHRz6ah</recordid><startdate>20090325</startdate><enddate>20090325</enddate><creator>Mitsushima, Dai</creator><creator>Takase, Kenkichi</creator><creator>Funabashi, Toshiya</creator><creator>Kimura, Fukuko</creator><general>Soc Neuroscience</general><general>Society for Neuroscience</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20090325</creationdate><title>Gonadal Steroids Maintain 24 h Acetylcholine Release in the Hippocampus: Organizational and Activational Effects in Behaving Rats</title><author>Mitsushima, Dai ; Takase, Kenkichi ; Funabashi, Toshiya ; Kimura, Fukuko</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c563t-ca772af010306dcd0972b04745a0779d8fd06854e43c1d3a088974cd0d20cee93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Acetylcholine - metabolism</topic><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Estradiol - pharmacology</topic><topic>Extracellular Space - metabolism</topic><topic>Female</topic><topic>Gonadal Hormones - pharmacology</topic><topic>Hippocampus - drug effects</topic><topic>Hippocampus - metabolism</topic><topic>Male</topic><topic>Motor Activity</topic><topic>Orchiectomy</topic><topic>Ovariectomy</topic><topic>Rats</topic><topic>Sex Differentiation</topic><topic>Sex Factors</topic><topic>Testosterone - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mitsushima, Dai</creatorcontrib><creatorcontrib>Takase, Kenkichi</creatorcontrib><creatorcontrib>Funabashi, Toshiya</creatorcontrib><creatorcontrib>Kimura, Fukuko</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mitsushima, Dai</au><au>Takase, Kenkichi</au><au>Funabashi, Toshiya</au><au>Kimura, Fukuko</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Gonadal Steroids Maintain 24 h Acetylcholine Release in the Hippocampus: Organizational and Activational Effects in Behaving Rats</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2009-03-25</date><risdate>2009</risdate><volume>29</volume><issue>12</issue><spage>3808</spage><epage>3815</epage><pages>3808-3815</pages><issn>0270-6474</issn><issn>1529-2401</issn><eissn>1529-2401</eissn><abstract>Extracellular acetylcholine (ACh) levels in the dorsal hippocampus increases during learning or exploration, exhibiting a sex-specific 24 h release profile. To examine the activational effect of gonadal steroid hormones on the sex-specific ACh levels and its correlation with spontaneous locomotor activity, we observed these parameters simultaneously for 24 h. Gonadectomy severely attenuated the ACh levels, whereas the testosterone replacement in gonadectomized males or 17beta-estradiol replacement in gonadectomized females successfully restored the levels. 17beta-Estradiol-priming in gonadectomized males could not restore the ACh levels, and testosterone replacement in gonadectomized females failed to raise ACh levels to those seen in testosterone-primed gonadectomized males, revealing a sex-specific activational effect. Spontaneous locomotor activity was not changed in males by gonadectomy or the replacement of gonadal steroids, but 17beta-estradiol enhanced the activity in gonadectomized females. Gonadectomy severely reduced the correlation between ACh release and activity levels, but the testosterone replacement in gonadectomized males or 17beta-estradiol replacement in gonadectomized females successfully restored it. To further analyze the sex-specific effect of gonadal steroids, we examined the organizational effect of gonadal steroids on the ACh release in female rats. Neonatal testosterone or 17beta-estradiol treatment not only increased the ACh levels but also altered them to resemble male-specific ACh release properties without affecting levels of spontaneous locomotor activity. We conclude that the activational effects of gonadal steroids maintaining the ACh levels and the high correlation with spontaneous locomotor activity are sex-specific, and that the organizational effects of gonadal steroids suggest estrogen receptor-mediated masculinization of the septo-hippocampal cholinergic system.</abstract><cop>United States</cop><pub>Soc Neuroscience</pub><pmid>19321777</pmid><doi>10.1523/JNEUROSCI.5301-08.2009</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Acetylcholine - metabolism Animals Animals, Newborn Estradiol - pharmacology Extracellular Space - metabolism Female Gonadal Hormones - pharmacology Hippocampus - drug effects Hippocampus - metabolism Male Motor Activity Orchiectomy Ovariectomy Rats Sex Differentiation Sex Factors Testosterone - pharmacology |
| title | Gonadal Steroids Maintain 24 h Acetylcholine Release in the Hippocampus: Organizational and Activational Effects in Behaving Rats |
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