The effects of brain serotonin deficiency on behavioural disinhibition and anxiety-like behaviour following mild early life stress
Aberrant serotonin (5-HT) signalling and exposure to early life stress have both been suggested to play a role in anxiety- and impulsivity-related behaviours. However, whether congenital 5-HT deficiency × early life stress interactions influence the development of anxiety- or impulsivity-like behavi...
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| Veröffentlicht in: | The international journal of neuropsychopharmacology 2013-10, Vol.16 (9), p.2081-2094 |
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| container_title | The international journal of neuropsychopharmacology |
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| creator | Sachs, Benjamin D. Rodriguiz, Ramona M. Siesser, William B. Kenan, Alexander Royer, Elizabeth L. Jacobsen, Jacob P. R. Wetsel, William C. Caron, Marc G. |
| description | Aberrant serotonin (5-HT) signalling and exposure to early life stress have both been suggested to play a role in anxiety- and impulsivity-related behaviours. However, whether congenital 5-HT deficiency × early life stress interactions influence the development of anxiety- or impulsivity-like behaviour has not been established. Here, we examined the effects of early life maternal separation (MS) stress on anxiety-like behaviour and behavioural disinhibition, a type of impulsivity-like behaviour, in wild-type (WT) and tryptophan hydroxylase 2 (Tph2) knock-in (Tph2KI) mice, which exhibit ∼60–80% reductions in the levels of brain 5-HT due to a R439H mutation in Tph2. We also investigated the effects of 5-HT deficiency and early life stress on adult hippocampal neurogenesis, plasma corticosterone levels and several signal transduction pathways in the amygdala. We demonstrate that MS slightly increases anxiety-like behaviour in WT mice and induces behavioural disinhibition in Tph2KI animals. We also demonstrate that MS leads to a slight decrease in cell proliferation within the hippocampus and potentiates corticosterone responses to acute stress, but these effects are not affected by brain 5-HT deficiency. However, we show that 5-HT deficiency leads to significant alterations in SGK-1 and GSK3β signalling and NMDA receptor expression in the amygdala in response to MS. Together, these findings support a potential role for 5-HT-dependent signalling in the amygdala in regulating the long-term effects of early life stress on anxiety-like behaviour and behavioural disinhibition. |
| doi_str_mv | 10.1017/S1461145713000321 |
| format | Article |
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R. ; Wetsel, William C. ; Caron, Marc G.</creator><creatorcontrib>Sachs, Benjamin D. ; Rodriguiz, Ramona M. ; Siesser, William B. ; Kenan, Alexander ; Royer, Elizabeth L. ; Jacobsen, Jacob P. R. ; Wetsel, William C. ; Caron, Marc G.</creatorcontrib><description>Aberrant serotonin (5-HT) signalling and exposure to early life stress have both been suggested to play a role in anxiety- and impulsivity-related behaviours. However, whether congenital 5-HT deficiency × early life stress interactions influence the development of anxiety- or impulsivity-like behaviour has not been established. Here, we examined the effects of early life maternal separation (MS) stress on anxiety-like behaviour and behavioural disinhibition, a type of impulsivity-like behaviour, in wild-type (WT) and tryptophan hydroxylase 2 (Tph2) knock-in (Tph2KI) mice, which exhibit ∼60–80% reductions in the levels of brain 5-HT due to a R439H mutation in Tph2. We also investigated the effects of 5-HT deficiency and early life stress on adult hippocampal neurogenesis, plasma corticosterone levels and several signal transduction pathways in the amygdala. We demonstrate that MS slightly increases anxiety-like behaviour in WT mice and induces behavioural disinhibition in Tph2KI animals. We also demonstrate that MS leads to a slight decrease in cell proliferation within the hippocampus and potentiates corticosterone responses to acute stress, but these effects are not affected by brain 5-HT deficiency. However, we show that 5-HT deficiency leads to significant alterations in SGK-1 and GSK3β signalling and NMDA receptor expression in the amygdala in response to MS. Together, these findings support a potential role for 5-HT-dependent signalling in the amygdala in regulating the long-term effects of early life stress on anxiety-like behaviour and behavioural disinhibition.</description><identifier>ISSN: 1461-1457</identifier><identifier>EISSN: 1469-5111</identifier><identifier>DOI: 10.1017/S1461145713000321</identifier><identifier>PMID: 23672796</identifier><language>eng</language><publisher>Cambridge, UK: Cambridge University Press</publisher><subject>Amygdala - metabolism ; Animals ; Anxiety ; Anxiety - etiology ; Anxiety - genetics ; Anxiety - metabolism ; Anxiety - physiopathology ; Anxiety - psychology ; Anxiety, Separation - complications ; Anxiety, Separation - psychology ; Behavior, Animal ; Brain - growth & development ; Brain - metabolism ; Brain - physiopathology ; Corticosterone - blood ; Disease Models, Animal ; Glycogen Synthase Kinase 3 - metabolism ; Glycogen Synthase Kinase 3 beta ; Hippocampus - growth & development ; Hippocampus - metabolism ; Immediate-Early Proteins - metabolism ; Impulsive Behavior - etiology ; Impulsive Behavior - genetics ; Impulsive Behavior - metabolism ; Impulsive Behavior - physiopathology ; Impulsive Behavior - psychology ; Mice ; Mice, 129 Strain ; Mice, Inbred C57BL ; Mice, Transgenic ; Motor Activity ; Neurogenesis ; Protein-Serine-Threonine Kinases - metabolism ; Receptors, N-Methyl-D-Aspartate - metabolism ; Serotonin - deficiency ; Signal Transduction ; Stress, Psychological - etiology ; Stress, Psychological - genetics ; Stress, Psychological - metabolism ; Stress, Psychological - physiopathology ; Stress, Psychological - psychology ; Tryptophan Hydroxylase - genetics ; Tryptophan Hydroxylase - metabolism</subject><ispartof>The international journal of neuropsychopharmacology, 2013-10, Vol.16 (9), p.2081-2094</ispartof><rights>CINP 2013</rights><rights>CINP 2013 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c504t-1c6223338a43f89a251e92ac6f78a74172a7fe29d403fb34a9895723ab265c8a3</citedby><cites>FETCH-LOGICAL-c504t-1c6223338a43f89a251e92ac6f78a74172a7fe29d403fb34a9895723ab265c8a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23672796$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sachs, Benjamin D.</creatorcontrib><creatorcontrib>Rodriguiz, Ramona M.</creatorcontrib><creatorcontrib>Siesser, William B.</creatorcontrib><creatorcontrib>Kenan, Alexander</creatorcontrib><creatorcontrib>Royer, Elizabeth L.</creatorcontrib><creatorcontrib>Jacobsen, Jacob P. R.</creatorcontrib><creatorcontrib>Wetsel, William C.</creatorcontrib><creatorcontrib>Caron, Marc G.</creatorcontrib><title>The effects of brain serotonin deficiency on behavioural disinhibition and anxiety-like behaviour following mild early life stress</title><title>The international journal of neuropsychopharmacology</title><addtitle>Int. J. Neuropsychopharm</addtitle><description>Aberrant serotonin (5-HT) signalling and exposure to early life stress have both been suggested to play a role in anxiety- and impulsivity-related behaviours. However, whether congenital 5-HT deficiency × early life stress interactions influence the development of anxiety- or impulsivity-like behaviour has not been established. Here, we examined the effects of early life maternal separation (MS) stress on anxiety-like behaviour and behavioural disinhibition, a type of impulsivity-like behaviour, in wild-type (WT) and tryptophan hydroxylase 2 (Tph2) knock-in (Tph2KI) mice, which exhibit ∼60–80% reductions in the levels of brain 5-HT due to a R439H mutation in Tph2. We also investigated the effects of 5-HT deficiency and early life stress on adult hippocampal neurogenesis, plasma corticosterone levels and several signal transduction pathways in the amygdala. We demonstrate that MS slightly increases anxiety-like behaviour in WT mice and induces behavioural disinhibition in Tph2KI animals. We also demonstrate that MS leads to a slight decrease in cell proliferation within the hippocampus and potentiates corticosterone responses to acute stress, but these effects are not affected by brain 5-HT deficiency. However, we show that 5-HT deficiency leads to significant alterations in SGK-1 and GSK3β signalling and NMDA receptor expression in the amygdala in response to MS. Together, these findings support a potential role for 5-HT-dependent signalling in the amygdala in regulating the long-term effects of early life stress on anxiety-like behaviour and behavioural disinhibition.</description><subject>Amygdala - metabolism</subject><subject>Animals</subject><subject>Anxiety</subject><subject>Anxiety - etiology</subject><subject>Anxiety - genetics</subject><subject>Anxiety - metabolism</subject><subject>Anxiety - physiopathology</subject><subject>Anxiety - psychology</subject><subject>Anxiety, Separation - complications</subject><subject>Anxiety, Separation - psychology</subject><subject>Behavior, Animal</subject><subject>Brain - growth & development</subject><subject>Brain - metabolism</subject><subject>Brain - physiopathology</subject><subject>Corticosterone - blood</subject><subject>Disease Models, Animal</subject><subject>Glycogen Synthase Kinase 3 - metabolism</subject><subject>Glycogen Synthase Kinase 3 beta</subject><subject>Hippocampus - growth & development</subject><subject>Hippocampus - metabolism</subject><subject>Immediate-Early Proteins - metabolism</subject><subject>Impulsive Behavior - etiology</subject><subject>Impulsive Behavior - genetics</subject><subject>Impulsive Behavior - metabolism</subject><subject>Impulsive Behavior - physiopathology</subject><subject>Impulsive Behavior - psychology</subject><subject>Mice</subject><subject>Mice, 129 Strain</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Motor Activity</subject><subject>Neurogenesis</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Receptors, N-Methyl-D-Aspartate - metabolism</subject><subject>Serotonin - deficiency</subject><subject>Signal Transduction</subject><subject>Stress, Psychological - etiology</subject><subject>Stress, Psychological - genetics</subject><subject>Stress, Psychological - metabolism</subject><subject>Stress, Psychological - physiopathology</subject><subject>Stress, Psychological - psychology</subject><subject>Tryptophan Hydroxylase - genetics</subject><subject>Tryptophan Hydroxylase - metabolism</subject><issn>1461-1457</issn><issn>1469-5111</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNqNkk1v1DAQhiMEoqXwA7ggS1x6CXhsJ04uSKjiS6rEgXKOHGe8O8Wxi51t2Wt_OV66lAJC4mB55Hnmtef1VNVT4C-Ag375CVQLoBoNknMuBdyrDstRXzcAcP9HDPUuf1A9yvmcc6Ea2T6sDoRstdB9e1hdn62RoXNol8yiY2MyFFjGFJcYSjShI0sY7JbFwEZcm0uKm2Q8myhTWNNIC5WMCVNZ3wiXbe3pC_5CmYvexysKKzaTnxia5LfMk0OWl4Q5P64eOOMzPtnvR9Xnt2_OTt7Xpx_ffTh5fVrbhqulBtsKIaXsjJKu641oAHthbOt0Z7QCLYx2KPpJcelGqUzf9Y0W0oyibWxn5FH16kb3YjPOOFkMS-ljuEg0m7QdoqHh90yg9bCKl4PsZbEbisDxXiDFrxvMyzBTtui9CRg3eQAlFRcdtPw_UNGLAmpZ0Od_oOfFtVCc2FGd1qX7plBwQ9kUc07obt8NfNgNw_DXMJSaZ3cbvq34-fsFkHtRM4-JphXeufufst8BDF3AFA</recordid><startdate>20131001</startdate><enddate>20131001</enddate><creator>Sachs, Benjamin D.</creator><creator>Rodriguiz, Ramona M.</creator><creator>Siesser, William B.</creator><creator>Kenan, Alexander</creator><creator>Royer, Elizabeth L.</creator><creator>Jacobsen, Jacob P. 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R.</au><au>Wetsel, William C.</au><au>Caron, Marc G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The effects of brain serotonin deficiency on behavioural disinhibition and anxiety-like behaviour following mild early life stress</atitle><jtitle>The international journal of neuropsychopharmacology</jtitle><addtitle>Int. J. Neuropsychopharm</addtitle><date>2013-10-01</date><risdate>2013</risdate><volume>16</volume><issue>9</issue><spage>2081</spage><epage>2094</epage><pages>2081-2094</pages><issn>1461-1457</issn><eissn>1469-5111</eissn><abstract>Aberrant serotonin (5-HT) signalling and exposure to early life stress have both been suggested to play a role in anxiety- and impulsivity-related behaviours. However, whether congenital 5-HT deficiency × early life stress interactions influence the development of anxiety- or impulsivity-like behaviour has not been established. Here, we examined the effects of early life maternal separation (MS) stress on anxiety-like behaviour and behavioural disinhibition, a type of impulsivity-like behaviour, in wild-type (WT) and tryptophan hydroxylase 2 (Tph2) knock-in (Tph2KI) mice, which exhibit ∼60–80% reductions in the levels of brain 5-HT due to a R439H mutation in Tph2. We also investigated the effects of 5-HT deficiency and early life stress on adult hippocampal neurogenesis, plasma corticosterone levels and several signal transduction pathways in the amygdala. We demonstrate that MS slightly increases anxiety-like behaviour in WT mice and induces behavioural disinhibition in Tph2KI animals. We also demonstrate that MS leads to a slight decrease in cell proliferation within the hippocampus and potentiates corticosterone responses to acute stress, but these effects are not affected by brain 5-HT deficiency. However, we show that 5-HT deficiency leads to significant alterations in SGK-1 and GSK3β signalling and NMDA receptor expression in the amygdala in response to MS. Together, these findings support a potential role for 5-HT-dependent signalling in the amygdala in regulating the long-term effects of early life stress on anxiety-like behaviour and behavioural disinhibition.</abstract><cop>Cambridge, UK</cop><pub>Cambridge University Press</pub><pmid>23672796</pmid><doi>10.1017/S1461145713000321</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Amygdala - metabolism Animals Anxiety Anxiety - etiology Anxiety - genetics Anxiety - metabolism Anxiety - physiopathology Anxiety - psychology Anxiety, Separation - complications Anxiety, Separation - psychology Behavior, Animal Brain - growth & development Brain - metabolism Brain - physiopathology Corticosterone - blood Disease Models, Animal Glycogen Synthase Kinase 3 - metabolism Glycogen Synthase Kinase 3 beta Hippocampus - growth & development Hippocampus - metabolism Immediate-Early Proteins - metabolism Impulsive Behavior - etiology Impulsive Behavior - genetics Impulsive Behavior - metabolism Impulsive Behavior - physiopathology Impulsive Behavior - psychology Mice Mice, 129 Strain Mice, Inbred C57BL Mice, Transgenic Motor Activity Neurogenesis Protein-Serine-Threonine Kinases - metabolism Receptors, N-Methyl-D-Aspartate - metabolism Serotonin - deficiency Signal Transduction Stress, Psychological - etiology Stress, Psychological - genetics Stress, Psychological - metabolism Stress, Psychological - physiopathology Stress, Psychological - psychology Tryptophan Hydroxylase - genetics Tryptophan Hydroxylase - metabolism |
| title | The effects of brain serotonin deficiency on behavioural disinhibition and anxiety-like behaviour following mild early life stress |
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