Vesicular glutamate transporter 3-immunoreactive pericellular baskets ensheath a distinct population of neurons in the lateral septum

Riedel, Anett; Westerholz, Sören; Braun, Katharina; Edwards, Robert H.; Arendt, Thomas; Härtig, Wolfgang

doi:10.1016/j.jchemneu.2008.06.003

Cited by 10 publications

(19 citation statements)

References 65 publications

(87 reference statements)

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“…The general pattern of calbindin (CB) staining observed in the LS was very similar to the findings of previous studies [48–51]. CB-immunoreactive neurons were heterogeneously distributed throughout the LS.…”

Section: Resultssupporting

confidence: 87%

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Characterization of GABAergic Neurons in the Mouse Lateral Septum: A Double Fluorescence In Situ Hybridization and Immunohistochemical Study Using Tyramide Signal Amplification

2013

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Gamma-aminobutyric acid (GABA) neurotransmission in the lateral septum (LS) is implicated in modulating various behavioral processes, including emotional reactivity and maternal behavior. However, identifying the phenotype of GABAergic neurons in the CNS has been hampered by the longstanding inability to reliably detect somal immunoreactivity for GABA or glutamic acid decarboxylase (GAD), the enzyme that produces GABA. In this study, we designed unique probes for both GAD65 (GAD2) and GAD67 (GAD1), and used fluorescence in Situ hybridization (FISH) with tyramide signal amplification (TSA) to achieve unequivocal detection of cell bodies of GABAergic neurons by GAD mRNAs. We quantitatively characterized the expression and chemical phenotype of GABAergic neurons across each subdivision of LS and in cingulate cortex (Cg) and medial preoptic area (MPOA) in female mice. Across LS, almost all GAD65 mRNA-expressing neurons were found to contain GAD67 mRNA (approximately 95-98%), while a small proportion of GAD67 mRNA-containing neurons did not express GAD65 mRNA (5-14%). Using the neuronal marker NeuN, almost every neuron in LS (> 90%) was also found to be GABA-positive. Interneuron markers using calcium-binding proteins showed that LS GABAergic neurons displayed immunoreactivity for calbindin (CB) or calretinin (CR), but not parvalbumin (PV); almost all CB- or CR-immunoreactive neurons (98-100%) were GABAergic. The proportion of GABAergic neurons immunoreactive for CB or CR varied depending on the subdivisions examined, with the highest percentage of colocalization in the caudal intermediate LS (LSI) (approximately 58% for CB and 35% for CR). These findings suggest that the vast majority of GABAergic neurons within the LS have the potential for synthesizing GABA via the dual enzyme systems GAD65 and GAD67, and each subtype of GABAergic neurons identified by distinct calcium-binding proteins may exert unique roles in the physiological function and neuronal circuitry of the LS.

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Section: Resultssupporting

confidence: 87%

“…The presence of CR-immunoreactive neurons in the LS has been reported [51,81]. However, very few quantitative and comparative studies have been made with regard to the distribution of CR and its colocalization with GABA within the LS.…”

Section: Discussionmentioning

confidence: 99%

Characterization of GABAergic Neurons in the Mouse Lateral Septum: A Double Fluorescence In Situ Hybridization and Immunohistochemical Study Using Tyramide Signal Amplification

2013

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“…1B′ and C′) in situ hybridization techniques, we detect prominent labeled neurons for the glutamate transporter 3 (VGLUT3) mRNA in BST (Fig. 1; (Gras et al , 2002; Schafer et al , 2002; Herzog et al , 2004; Riedel et al , 2008); and 2) Using [H 3 ] D-aspartate retrograde tracing technique, numerous radiolabelled cell bodies were detected in the anterolateral and antero ventral BST (Csaki et al , 2000; Kocsis et al , 2003). This data taken together with our retrograde and anterograde labelings, and antidromic activation of BST neurons by VTA stimulation (Georges and Aston-Jones, 2002), give anatomical and physiological support for a glutamatergic projection from the BST to the VTA.…”

Section: Bst As a Hub Connecting Hippocampus Prefrontal Cortex Anmentioning

confidence: 93%

Role of the bed nucleus of the stria terminalis in the control of ventral tegmental area dopamine neurons

Jalabert

Aston‐Jones

Herzog

et al. 2009

Progress in Neuro-Psychopharmacology and Biological Psychiatry

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Projections from neurons of the bed nucleus of the stria terminalis (BST) to the ventral tegmental area (VTA) are crucial to behaviors related to reward and motivation. Over the past few years, we have undertaken a series of studies to understand: 1) how excitatory inputs regulate in vivo excitable properties of BST neurons, and 2) how BST inputs in turn modulate neuronal activity of dopamine neurons in VTA. Using in vivo extracellular recording techniques in anesthetized rats and tract-tracing approaches, we have demonstrated that inputs from the infralimbic cortex and the ventral subiculum exert a strong excitatory influence on BST neurons projecting to the VTA. Thus, the BST is uniquely positioned to receive emotional and learning-associated informations and to integrate these into the reward/motivation circuitry. We will discuss how changes in the activity of BST neurons projecting to the VTA could participate in the development or exacerbation of psychiatric conditions such as drug addiction.

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“…These observations suggested that VGLUT3 distribution in 5-HT terminals from the hippocampus was highly regionalized. In Figure 4h, two neurons from the lateral septum are covered by dense VGLUT3-positive pericellular baskets (Riedel et al, 2008;Shutoh et al, 2008). Only one of these neurons is surrounded by VMAT2 ϩ 5-HTϩVGLUT3 fibers.…”

Section: Vglut3 Colocalizes With Vmat2 and 5-ht But Rarely With Sertmentioning

confidence: 96%

VGLUT3 (Vesicular Glutamate Transporter Type 3) Contribution to the Regulation of Serotonergic Transmission and Anxiety

Amilhon¹,

Lepicard²,

Renoir³

et al. 2010

J. Neurosci.

159

192

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Three different subtypes of Hϩ -dependent carriers (named VGLUT1-3) concentrate glutamate into synaptic vesicles before its exocytotic release. Neurons using other neurotransmitter than glutamate (such as cholinergic striatal interneurons and 5-HT neurons) express VGLUT3. It was recently reported that VGLUT3 increases acetylcholine vesicular filling, thereby, stimulating cholinergic transmission. This new regulatory mechanism is herein designated as vesicular-filling synergy (or vesicular synergy). In the present report, we found that deletion of VGLUT3 increased several anxiety-related behaviors in adult and in newborn mice as early as 8 d after birth. This precocious involvement of a vesicular glutamate transporter in anxiety led us to examine the underlying functional implications of VGLUT3 in 5-HT neurons. On one hand, VGLUT3 deletion caused a significant decrease of 5-HT 1A -mediated neurotransmission in raphe nuclei. On the other hand, VGLUT3 positively modulated 5-HT transmission of a specific subset of 5-HT terminals from the hippocampus and the cerebral cortex. VGLUT3-and VMAT2-positive serotonergic fibers show little or no 5-HT reuptake transporter. These results unravel the existence of a novel subset of 5-HT terminals in limbic areas that might play a crucial role in anxiety-like behaviors. In summary, VGLUT3 accelerates 5-HT transmission at the level of specific 5-HT terminals and can exert an inhibitory control at the raphe level. Furthermore, our results suggest that the loss of VGLUT3 expression leads to anxiety-associated behaviors and should be considered as a potential new target for the treatment of this disorder.

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Vesicular glutamate transporter 3-immunoreactive pericellular baskets ensheath a distinct population of neurons in the lateral septum

Cited by 10 publications

References 65 publications

Characterization of GABAergic Neurons in the Mouse Lateral Septum: A Double Fluorescence In Situ Hybridization and Immunohistochemical Study Using Tyramide Signal Amplification

Characterization of GABAergic Neurons in the Mouse Lateral Septum: A Double Fluorescence In Situ Hybridization and Immunohistochemical Study Using Tyramide Signal Amplification

Role of the bed nucleus of the stria terminalis in the control of ventral tegmental area dopamine neurons

VGLUT3 (Vesicular Glutamate Transporter Type 3) Contribution to the Regulation of Serotonergic Transmission and Anxiety

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