A Synaptically Connected Hypothalamic Magnocellular Vasopressin-Locus Coeruleus Neuronal Circuit and Its Plasticity in Response to Emotional and Physiological Stress

Oscar R. Hernández-Pérez, Vito S. Hernández, Alicia T. Nava-Kopp, Rafael A. Barrio, Mohsen Seifi, Jerome D. Swinny, Lee E. Eiden, Limei Zhang

Research output: Contribution to journalArticle

Abstract

The locus coeruleus (LC)-norepinephrine (NE) system modulates a range of salient brain functions, including memory and response to stress. The LC-NE system is regulated by neurochemically diverse inputs, including a range of neuropeptides such as arginine-vasopressin (AVP). Whilst the origins of many of these LC inputs, their synaptic connectivity with LC neurons, and their contribution to LC-mediated brain functions, have been well characterized, this is not the case for the AVP-LC system. Therefore, our aims were to define the types of synapses formed by AVP+ fibers with LC neurons using immunohistochemistry together with confocal and transmission electron microscopy (TEM), the origins of such inputs, using retrograde tracers, and the plasticity of the LC AVP system in response to stress and spatial learning, using the maternal separation (MS) and Morris water maze (MWM) paradigms, respectively, in rat. Confocal microscopy revealed that AVP+ fibers contacting tyrosine hydroxylase (TH)+ LC neurons were also immunopositive for vesicular glutamate transporter 2, a marker of presynaptic glutamatergic axons. TEM confirmed that AVP+ axons formed Gray type I (asymmetric) synapses with TH+ dendrites thus confirming excitatory synaptic connections between these systems. Retrograde tracing revealed that these LC AVP+ fibers originate from hypothalamic vasopressinergic magnocellular neurosecretory neurons (AVPMNNs). MS induced a significant increase in the density of LC AVP+ fibers. Finally, AVPMNN circuit upregulation by water-deprivation improved MWM performance while increased Fos expression was found in LC and efferent regions such as hippocampus and prefrontal cortex, suggesting that AVPMMN projections to LC could integrate homeostatic responses modifying neuroplasticity.
Original languageEnglish
JournalFrontiers in Neuroscience
Volume13
DOIs
Publication statusPublished - 20 Mar 2019

Fingerprint

Physiological Stress
Locus Coeruleus
Vasopressins
Psychological Stress
Arginine Vasopressin
Neurons
Tyrosine 3-Monooxygenase
Transmission Electron Microscopy
Synapses
Axons
Norepinephrine
Vesicular Glutamate Transport Protein 2
Mothers
Water Deprivation
Neuronal Plasticity
Water
Brain
Dendrites
Prefrontal Cortex
Neuropeptides

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Hernández-Pérez, Oscar R. ; Hernández, Vito S. ; Nava-Kopp, Alicia T. ; Barrio, Rafael A. ; Seifi, Mohsen ; Swinny, Jerome D. ; Eiden, Lee E. ; Zhang, Limei. / A Synaptically Connected Hypothalamic Magnocellular Vasopressin-Locus Coeruleus Neuronal Circuit and Its Plasticity in Response to Emotional and Physiological Stress. In: Frontiers in Neuroscience. 2019 ; Vol. 13.
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abstract = "The locus coeruleus (LC)-norepinephrine (NE) system modulates a range of salient brain functions, including memory and response to stress. The LC-NE system is regulated by neurochemically diverse inputs, including a range of neuropeptides such as arginine-vasopressin (AVP). Whilst the origins of many of these LC inputs, their synaptic connectivity with LC neurons, and their contribution to LC-mediated brain functions, have been well characterized, this is not the case for the AVP-LC system. Therefore, our aims were to define the types of synapses formed by AVP+ fibers with LC neurons using immunohistochemistry together with confocal and transmission electron microscopy (TEM), the origins of such inputs, using retrograde tracers, and the plasticity of the LC AVP system in response to stress and spatial learning, using the maternal separation (MS) and Morris water maze (MWM) paradigms, respectively, in rat. Confocal microscopy revealed that AVP+ fibers contacting tyrosine hydroxylase (TH)+ LC neurons were also immunopositive for vesicular glutamate transporter 2, a marker of presynaptic glutamatergic axons. TEM confirmed that AVP+ axons formed Gray type I (asymmetric) synapses with TH+ dendrites thus confirming excitatory synaptic connections between these systems. Retrograde tracing revealed that these LC AVP+ fibers originate from hypothalamic vasopressinergic magnocellular neurosecretory neurons (AVPMNNs). MS induced a significant increase in the density of LC AVP+ fibers. Finally, AVPMNN circuit upregulation by water-deprivation improved MWM performance while increased Fos expression was found in LC and efferent regions such as hippocampus and prefrontal cortex, suggesting that AVPMMN projections to LC could integrate homeostatic responses modifying neuroplasticity.",
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A Synaptically Connected Hypothalamic Magnocellular Vasopressin-Locus Coeruleus Neuronal Circuit and Its Plasticity in Response to Emotional and Physiological Stress. / Hernández-Pérez, Oscar R.; Hernández, Vito S.; Nava-Kopp, Alicia T.; Barrio, Rafael A.; Seifi, Mohsen; Swinny, Jerome D.; Eiden, Lee E.; Zhang, Limei.

In: Frontiers in Neuroscience, Vol. 13, 20.03.2019.

Research output: Contribution to journalArticle

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AU - Hernández-Pérez, Oscar R.

AU - Hernández, Vito S.

AU - Nava-Kopp, Alicia T.

AU - Barrio, Rafael A.

AU - Seifi, Mohsen

AU - Swinny, Jerome D.

AU - Eiden, Lee E.

AU - Zhang, Limei

PY - 2019/3/20

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