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Thirst Is Associated with Suppression of Habenula Output and Active Stress Coping: Is there a Role for a Non-canonical Vasopressin-Glutamate Pathway?

Zhang L, Hernández VS, Vázquez-Juárez E, Chay FK, Barrio RA - Front Neural Circuits (2016)

Bottom Line: We demonstrate a direct pathway from hypothalamic paraventricular VP-expressing, glutamatergic magnocellular neurons to the medial division of lateral habenula (LHbM), a region containing GABAergic neurons.In vivo recording and juxtacellular labeling revealed that GABAergic neurons in the LHbM had locally branching axons, and received VP-positive axon terminal contacts on their dendrites.Our results reveal a novel VP-expressing hypothalamus to the LHbM circuit that is likely to evoke GABA-mediated inhibition in the LHbM, which promotes escape behavior during stress coping.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Fisiología, Facultad de Medicina, Universidad Nacional Autónoma de México Ciudad de México, Mexico.

ABSTRACT
Water-homeostasis is a fundamental physiological process for terrestrial life. In vertebrates, thirst drives water intake, but the neuronal circuits that connect the physiology of water regulation with emotional context are poorly understood. Vasopressin (VP) is a prominent messenger in this circuit, as well as L-glutamate. We have investigated the role of a VP circuit and interaction between thirst and motivational behaviors evoked by life-threatening stimuli in rats. We demonstrate a direct pathway from hypothalamic paraventricular VP-expressing, glutamatergic magnocellular neurons to the medial division of lateral habenula (LHbM), a region containing GABAergic neurons. In vivo recording and juxtacellular labeling revealed that GABAergic neurons in the LHbM had locally branching axons, and received VP-positive axon terminal contacts on their dendrites. Water deprivation significantly reduced freezing and immobility behaviors evoked by innate fear and behavioral despair, respectively, accompanied by decreased Fos expression in the lateral habenula. Our results reveal a novel VP-expressing hypothalamus to the LHbM circuit that is likely to evoke GABA-mediated inhibition in the LHbM, which promotes escape behavior during stress coping.

No MeSH data available.


Related in: MedlinePlus

Vasopressin immunopositive fiber distribution through the rostro-caudal extent of rat habenular complex. Panels (A–I) dark-field photomicrographs of AVP immunoreaction on coronal sections at the rostro-caudal Bregma levels indicated in each panel. Vasopressin immunopositive fibers densely innervate the medial division of lateral habenular complex (LHbM), i.e., the superior subnucleus (LHbMS), the central subnucleus (LHbMC), remarkably its parvocellular subnucleus (LHbMPc), and the marginal subnucleus (LHbMMg). Inset of the panel (G) shows a drawing with the subnuclei mentioned. Note that highest density of AVP+ fibers is observed inside the LHbMC (panels F–H arrows). Scale bars: 250 μm. D3V, dorsal 3rd ventricle; MHb, medial habenular complex; LHb, lateral habenular complex; SM, stria medularis; FR, fasciculus retroflexus.
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Figure 1: Vasopressin immunopositive fiber distribution through the rostro-caudal extent of rat habenular complex. Panels (A–I) dark-field photomicrographs of AVP immunoreaction on coronal sections at the rostro-caudal Bregma levels indicated in each panel. Vasopressin immunopositive fibers densely innervate the medial division of lateral habenular complex (LHbM), i.e., the superior subnucleus (LHbMS), the central subnucleus (LHbMC), remarkably its parvocellular subnucleus (LHbMPc), and the marginal subnucleus (LHbMMg). Inset of the panel (G) shows a drawing with the subnuclei mentioned. Note that highest density of AVP+ fibers is observed inside the LHbMC (panels F–H arrows). Scale bars: 250 μm. D3V, dorsal 3rd ventricle; MHb, medial habenular complex; LHb, lateral habenular complex; SM, stria medularis; FR, fasciculus retroflexus.

Mentions: We used anti-VP antibodies to characterize the VP immunopositive fiber distribution and found a highly selective distribution pattern in the medial subdivision of the LHb (LHbM) (Figure 1). The fibers were grouped mainly in three subnuclei: the superior subnucleus (LHbMS), the central subnucleus (LHbMC), and the marginal subnucleus (LHbMMg) (see inset of panel G). Notice that the highest density of VP+ fibers was observed inside the LHbMC (Figures 1F–I, arrows). For the sake of completeness, we also examined the expression of other relevant neurochemical markers: tyrosine hydroxylase (TH), dopamine beta hydroxylase (DBH), serotonin transporter (SerT), somatostatin (SOM), enkephalin (ENK), substance P (SP), calretinin (CR), calbindin (CB), G protein-coupled inwardly-rectifying potassium channel 1 and 2 (GIRK1 and GIRK2) (see supplementary information Figure S1). Interestingly, a strong regional innervation overlapping pattern was observed within the LHbMC between VP and midbrain aminergic projections (immnoreactivity to TH and SerT, but not DBH which was sparse and not regional–specific) (supplementary information SI, Figures S1A–C). This phenomenon may indicate that: (1) the LHbMC is a key region modulated by subcortical aminergic pathway; (2) the VP innervation may contribute to the robustness of the modulatory mechanism for LHb function, which is also regulated by midbrain aminergic pathways. The region of strong immunostaining for SOM, CR, and CB was also similar to VP. The expressions of ENK, SP, and GIRK1 and GIRK2 were not similar to that of VP, particularly low in LHbMC. CB immunopositive somata were predominantly located in the LHbMC and CB+ axons seemed to project to fasciculus retroflexus.


Thirst Is Associated with Suppression of Habenula Output and Active Stress Coping: Is there a Role for a Non-canonical Vasopressin-Glutamate Pathway?

Zhang L, Hernández VS, Vázquez-Juárez E, Chay FK, Barrio RA - Front Neural Circuits (2016)

Vasopressin immunopositive fiber distribution through the rostro-caudal extent of rat habenular complex. Panels (A–I) dark-field photomicrographs of AVP immunoreaction on coronal sections at the rostro-caudal Bregma levels indicated in each panel. Vasopressin immunopositive fibers densely innervate the medial division of lateral habenular complex (LHbM), i.e., the superior subnucleus (LHbMS), the central subnucleus (LHbMC), remarkably its parvocellular subnucleus (LHbMPc), and the marginal subnucleus (LHbMMg). Inset of the panel (G) shows a drawing with the subnuclei mentioned. Note that highest density of AVP+ fibers is observed inside the LHbMC (panels F–H arrows). Scale bars: 250 μm. D3V, dorsal 3rd ventricle; MHb, medial habenular complex; LHb, lateral habenular complex; SM, stria medularis; FR, fasciculus retroflexus.
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Related In: Results  -  Collection

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Figure 1: Vasopressin immunopositive fiber distribution through the rostro-caudal extent of rat habenular complex. Panels (A–I) dark-field photomicrographs of AVP immunoreaction on coronal sections at the rostro-caudal Bregma levels indicated in each panel. Vasopressin immunopositive fibers densely innervate the medial division of lateral habenular complex (LHbM), i.e., the superior subnucleus (LHbMS), the central subnucleus (LHbMC), remarkably its parvocellular subnucleus (LHbMPc), and the marginal subnucleus (LHbMMg). Inset of the panel (G) shows a drawing with the subnuclei mentioned. Note that highest density of AVP+ fibers is observed inside the LHbMC (panels F–H arrows). Scale bars: 250 μm. D3V, dorsal 3rd ventricle; MHb, medial habenular complex; LHb, lateral habenular complex; SM, stria medularis; FR, fasciculus retroflexus.
Mentions: We used anti-VP antibodies to characterize the VP immunopositive fiber distribution and found a highly selective distribution pattern in the medial subdivision of the LHb (LHbM) (Figure 1). The fibers were grouped mainly in three subnuclei: the superior subnucleus (LHbMS), the central subnucleus (LHbMC), and the marginal subnucleus (LHbMMg) (see inset of panel G). Notice that the highest density of VP+ fibers was observed inside the LHbMC (Figures 1F–I, arrows). For the sake of completeness, we also examined the expression of other relevant neurochemical markers: tyrosine hydroxylase (TH), dopamine beta hydroxylase (DBH), serotonin transporter (SerT), somatostatin (SOM), enkephalin (ENK), substance P (SP), calretinin (CR), calbindin (CB), G protein-coupled inwardly-rectifying potassium channel 1 and 2 (GIRK1 and GIRK2) (see supplementary information Figure S1). Interestingly, a strong regional innervation overlapping pattern was observed within the LHbMC between VP and midbrain aminergic projections (immnoreactivity to TH and SerT, but not DBH which was sparse and not regional–specific) (supplementary information SI, Figures S1A–C). This phenomenon may indicate that: (1) the LHbMC is a key region modulated by subcortical aminergic pathway; (2) the VP innervation may contribute to the robustness of the modulatory mechanism for LHb function, which is also regulated by midbrain aminergic pathways. The region of strong immunostaining for SOM, CR, and CB was also similar to VP. The expressions of ENK, SP, and GIRK1 and GIRK2 were not similar to that of VP, particularly low in LHbMC. CB immunopositive somata were predominantly located in the LHbMC and CB+ axons seemed to project to fasciculus retroflexus.

Bottom Line: We demonstrate a direct pathway from hypothalamic paraventricular VP-expressing, glutamatergic magnocellular neurons to the medial division of lateral habenula (LHbM), a region containing GABAergic neurons.In vivo recording and juxtacellular labeling revealed that GABAergic neurons in the LHbM had locally branching axons, and received VP-positive axon terminal contacts on their dendrites.Our results reveal a novel VP-expressing hypothalamus to the LHbM circuit that is likely to evoke GABA-mediated inhibition in the LHbM, which promotes escape behavior during stress coping.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Fisiología, Facultad de Medicina, Universidad Nacional Autónoma de México Ciudad de México, Mexico.

ABSTRACT
Water-homeostasis is a fundamental physiological process for terrestrial life. In vertebrates, thirst drives water intake, but the neuronal circuits that connect the physiology of water regulation with emotional context are poorly understood. Vasopressin (VP) is a prominent messenger in this circuit, as well as L-glutamate. We have investigated the role of a VP circuit and interaction between thirst and motivational behaviors evoked by life-threatening stimuli in rats. We demonstrate a direct pathway from hypothalamic paraventricular VP-expressing, glutamatergic magnocellular neurons to the medial division of lateral habenula (LHbM), a region containing GABAergic neurons. In vivo recording and juxtacellular labeling revealed that GABAergic neurons in the LHbM had locally branching axons, and received VP-positive axon terminal contacts on their dendrites. Water deprivation significantly reduced freezing and immobility behaviors evoked by innate fear and behavioral despair, respectively, accompanied by decreased Fos expression in the lateral habenula. Our results reveal a novel VP-expressing hypothalamus to the LHbM circuit that is likely to evoke GABA-mediated inhibition in the LHbM, which promotes escape behavior during stress coping.

No MeSH data available.


Related in: MedlinePlus