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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

Twenty-four hours of water deprivation (WD24) promoted active stress coping during innate fear processing (cat exposure) and behavioral despair (forced swimming test, FST). WD24 is a potent physiological stimulus to increase metabolic activities of AVP containing magnocellular neurosecretory neurons in SON and PVN. Upon cat exposure, rats expressed innate fear-related passive (freezing), and active (rearing, climbing, and displacement) behaviors (A,B). Rats from WD24 group showed significant reduction of freezing counts (A) and increase of climbing and rearing behaviors (B). Similar observations were obtained during FST for behavioral despair (C,D). For locomotor control, we performed the elevated plus maze (EPM) test to both groups (E). The WD24 rats showed normal locomotion patterns but reduced percentage of time spent in open-arms. (Mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001).
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Figure 4: Twenty-four hours of water deprivation (WD24) promoted active stress coping during innate fear processing (cat exposure) and behavioral despair (forced swimming test, FST). WD24 is a potent physiological stimulus to increase metabolic activities of AVP containing magnocellular neurosecretory neurons in SON and PVN. Upon cat exposure, rats expressed innate fear-related passive (freezing), and active (rearing, climbing, and displacement) behaviors (A,B). Rats from WD24 group showed significant reduction of freezing counts (A) and increase of climbing and rearing behaviors (B). Similar observations were obtained during FST for behavioral despair (C,D). For locomotor control, we performed the elevated plus maze (EPM) test to both groups (E). The WD24 rats showed normal locomotion patterns but reduced percentage of time spent in open-arms. (Mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001).

Mentions: The effects of WD24 on the passive stress coping strategies (freezing) or active stress coping strategies (rearing/climbing/displacement), displayed when exposed to a live predator, are shown in (Figures 4A,B). The WD24 group showed a significant reduction in freezing counts (Ctrl: 50.1 ± 9.99 vs. WD24: 26.2 ± 3.5, n = 12, p < 0.05) and a significant increase in the number of active escaping (rearing/climbing/displacement) counts (Ctrl: 58.6 ± 6.3 vs. WD24: 87.8 ± 4.3, n = 12, p < 0.001). The water deprivation effects on swimming behavior during the FST are illustrated in Figures 4C,D. In the WD24 group there was a significant decrease in the immobility episodes (Ctrl: 32.3 ± 3.0 vs. WD24: 22.3 ± 2.5, Ctrl n = 11, WD24: n = 12, p < 0.05) and a significant increase in the climbing episodes (Ctrl: 9.7 ± 2.4 vs. WD24: 33.1 ± 2.5, Ctrl n = 11, WD24: n = 12, p < 0.001).


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)

Twenty-four hours of water deprivation (WD24) promoted active stress coping during innate fear processing (cat exposure) and behavioral despair (forced swimming test, FST). WD24 is a potent physiological stimulus to increase metabolic activities of AVP containing magnocellular neurosecretory neurons in SON and PVN. Upon cat exposure, rats expressed innate fear-related passive (freezing), and active (rearing, climbing, and displacement) behaviors (A,B). Rats from WD24 group showed significant reduction of freezing counts (A) and increase of climbing and rearing behaviors (B). Similar observations were obtained during FST for behavioral despair (C,D). For locomotor control, we performed the elevated plus maze (EPM) test to both groups (E). The WD24 rats showed normal locomotion patterns but reduced percentage of time spent in open-arms. (Mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4814529&req=5

Figure 4: Twenty-four hours of water deprivation (WD24) promoted active stress coping during innate fear processing (cat exposure) and behavioral despair (forced swimming test, FST). WD24 is a potent physiological stimulus to increase metabolic activities of AVP containing magnocellular neurosecretory neurons in SON and PVN. Upon cat exposure, rats expressed innate fear-related passive (freezing), and active (rearing, climbing, and displacement) behaviors (A,B). Rats from WD24 group showed significant reduction of freezing counts (A) and increase of climbing and rearing behaviors (B). Similar observations were obtained during FST for behavioral despair (C,D). For locomotor control, we performed the elevated plus maze (EPM) test to both groups (E). The WD24 rats showed normal locomotion patterns but reduced percentage of time spent in open-arms. (Mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001).
Mentions: The effects of WD24 on the passive stress coping strategies (freezing) or active stress coping strategies (rearing/climbing/displacement), displayed when exposed to a live predator, are shown in (Figures 4A,B). The WD24 group showed a significant reduction in freezing counts (Ctrl: 50.1 ± 9.99 vs. WD24: 26.2 ± 3.5, n = 12, p < 0.05) and a significant increase in the number of active escaping (rearing/climbing/displacement) counts (Ctrl: 58.6 ± 6.3 vs. WD24: 87.8 ± 4.3, n = 12, p < 0.001). The water deprivation effects on swimming behavior during the FST are illustrated in Figures 4C,D. In the WD24 group there was a significant decrease in the immobility episodes (Ctrl: 32.3 ± 3.0 vs. WD24: 22.3 ± 2.5, Ctrl n = 11, WD24: n = 12, p < 0.05) and a significant increase in the climbing episodes (Ctrl: 9.7 ± 2.4 vs. WD24: 33.1 ± 2.5, Ctrl n = 11, WD24: n = 12, p < 0.001).

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