Changes in autonomic nervous function and influencing factors in a rat insular cortex electrical kindling model

Ming, Qianwen; Ma, Hongtao; Li, Jia; Yang, Fan; Li, Jing; Liang, Jing; Li, Dan; Lin, Weihong

doi:10.1016/j.neulet.2020.134782

Cited by 4 publications

(3 citation statements)

References 34 publications

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“…We found the principal hubs of the stress response network to be the Ins_C, the BA and the PVH, which are main components of the stress response network. The Ins is associated with the modulation of the autonomic response, including somatosensory, nociceptive and visceral processing (Aguilar‐Rivera et al, 2020; Kimura et al, 2010; Menon & Uddin, 2010; Ming et al, 2020; Rogers‐Carter et al, 2018); in addition, the more caudal part of the Ins (Ins_C), which is the one coming out in our analysis, is involved in respiratory and cardiovascular controls (Bagaev & Aleksandrov, 2006). The engagement of the Ins_C makes perfect sense as the autonomic response facing stress is crucial to allow efficient coping (de Kloet et al, 1998; Selye, 1950).…”

Section: Discussionmentioning

confidence: 99%

Functional brain‐wide network mapping during acute stress exposure in rats: Interaction between the lateral habenula and cortical, amygdalar, hypothalamic and monoaminergic regions

Durieux

Herbeaux

Borcuk

et al. 2022

Eur J of Neuroscience

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Upon stress exposure, a broad network of structures comes into play in order to provide adequate responses and restore homeostasis. It has been known for decades that the main structures engaged during the stress response are the medial prefrontal cortex, the amygdala, the hippocampus, the hypothalamus, the monoaminergic systems (noradrenaline, dopamine and serotonin) and the periaqueductal gray. The lateral habenula (LHb) is an epithalamic structure directly connected to prefrontal cortical areas and to the amygdala, whereas it functionally interacts with the hippocampus. Also, it is a main modulator of monoaminergic systems. The LHb is activated upon exposure to basically all types of stressors, suggesting it is also involved in the stress response. However, it remains unknown if and how the LHb functionally interacts with the broad stress response network. In the current study we performed in rats a restraint stress procedure followed by immunohistochemical staining of the c‐Fos protein throughout the brain. Using graph theory‐based functional connectivity analyses, we confirm the principal hubs of the stress network (e.g., prefrontal cortex, amygdala and periventricular hypothalamus) and show that the LHb is engaged during stress exposure in close interaction with the medial prefrontal cortex, the lateral septum and the medial habenula. In addition, we performed DREADD‐induced LHb inactivation during the same restraint paradigm in order to explore its consequences on the stress response network. This last experiment gave contrasting results as the DREADD ligand alone, clozapine‐N‐oxide, was able to modify the network.

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Section: Discussionmentioning

confidence: 99%

Functional brain‐wide network mapping during acute stress exposure in rats: Interaction between the lateral habenula and cortical, amygdalar, hypothalamic and monoaminergic regions

Durieux

Herbeaux

Borcuk

et al. 2022

Eur J of Neuroscience

View full text Add to dashboard Cite

show abstract

“…We found the principal hubs of the stress response network to be the Ins_C, the BA and the PVH, which are main components of the stress response network. The Ins is associated with the modulation of the autonomic response, including somatosensory, nociceptive and visceral processing (Kimura et al, 2010; Menon and Uddin, 2010; Rogers-Carter et al, 2018; Aguilar-Rivera et al, 2020; Ming et al, 2020); in addition, the more caudal part of the Ins (Ins_C), which is the one coming out in our analysis, is involved in respiratory and cardiovascular controls (Bagaev and Aleksandrov, 2006). The engagement of the Ins_C makes perfect sense as the autonomic response facing stress is crucial to allow efficient coping (Selye, 1950; de Kloet et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

Functional brain-wide network mapping during acute stress exposure in rats: Interaction between the lateral habenula and cortical, amygdalar, hypothalamic and monoaminergic regions

Durieux

Herbeaux

Borcuk

et al. 2022

Preprint

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Upon stress exposure a broad network of structures comes into play in order to provide adequate responses and restore homeostasis. It has been known for decades that the main structures engaged during the stress response are the medial prefrontal cortex, the amygdala, the hippocampus, the hypothalamus, the monoaminergic systems (noradrenaline, dopamine, serotonin), and the periaqueductal gray. The lateral habenula (LHb) is an epithalamic structure directly connected to prefrontal cortical areas and to the amygdala, whereas it functionally interacts with the hippocampus. Also, it is a main modulator of monoaminergic systems. The LHb is activated upon exposure to basically all types of stressors, suggesting it is also involved in the stress response. However, it remains unknown if and how the LHb functionally interacts with the broad stress response network. In the current study we performed in rats a restraint stress procedure followed by immunohistochemical staining of the c-Fos protein throughout the brain. Using Graph Theory-based functional connectivity analyses, we confirm the principal hubs of the stress network (e.g. prefrontal cortex, amygdala, periventricular hypothalamus), and show that the LHb is engaged during stress exposure in close interaction with the medial prefrontal cortex, the lateral septum, and the medial habenula. In addition, we performed DREADD-induced LHb inactivation during the same restraint paradigm in order to explore its consequences on the stress response network. This last experiment gave contrasting results as the DREADD ligand alone, clozapine-N-oxide, was able to modify the network.GRAPHICAL ABSTRACTGRAPHICAL ABSTRACT TEXTIn this study, using immunohistochemical staining of the immediate early gene c-fos and graph theory-based functional correlational analyses, we aimed at unravelling the possible engagement of the lateral habenula (LHb) within the stress response network during acute stress exposure (10-min restraint) in rats. We found that the medial part of the LHb (LHbM) was preferentially engaged, and that this engagement was concomitant to this of structures such as the medial prefrontal cortex (mPFC), the insular cortex (Ins), hypothalamic (PVH) and thalamic (PVT) paraventricular nuclei, the extended amygdala, comprising the Bed nucleus of the stria terminalis (BNST) and the entire amygdala (AMG), as well as the dopaminergic ventral tegmental area (VTA) and the serotonergic dorsal raphe nucleus (RD). This suggests upon stressful situations the LHbM serves as a relay of cortical, thalamic, hypothalamic and temporal information, further transmitted to midbrain monoaminergic systems to probably initiate coping strategies.

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“…In another study using rats, stimulation of the Ic was associated with atrioventricular block, QT prolongation, asystole, and death, along with an elevation in the plasma norepinephrine level as well as myocardial cytolysis [ 15 ]. In a rat model of electrical kindling, Ming et al [ 16 ] implanted electrodes in the granular layer of the Ic, and in 92.3% of the rats, a seizure was induced. In older rats, the stimulation was associated with a greater heart rate (HR) reduction, and the 25% of the kindled rats died.…”

Section: The Brain–heart Connectionmentioning

confidence: 99%

Sex Hormone-Specific Neuroanatomy of Takotsubo Syndrome: Is the Insular Cortex a Moderator?

2022

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Takotsubo syndrome (TTS), a transient form of dysfunction in the heart’s left ventricle, occurs predominantly in postmenopausal women who have emotional stress. Earlier studies support the concept that the human circulatory system is modulated by a cortical network (consisting of the anterior cingulate gyrus, amygdala, and insular cortex (Ic)) that plays a pivotal role in the central autonomic nervous system in relation to emotional stressors. The Ic plays a crucial role in the sympathovagal balance, and decreased levels of female sex hormones have been speculated to change functional cerebral asymmetry, with a possible link to autonomic instability. In this review, we focus on the Ic as an important moderator of the human brain–heart axis in association with sex hormones. We also summarize the current knowledge regarding the sex-specific neuroanatomy in TTS.

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Changes in autonomic nervous function and influencing factors in a rat insular cortex electrical kindling model

Cited by 4 publications

References 34 publications

Functional brain‐wide network mapping during acute stress exposure in rats: Interaction between the lateral habenula and cortical, amygdalar, hypothalamic and monoaminergic regions

Functional brain‐wide network mapping during acute stress exposure in rats: Interaction between the lateral habenula and cortical, amygdalar, hypothalamic and monoaminergic regions

Functional brain-wide network mapping during acute stress exposure in rats: Interaction between the lateral habenula and cortical, amygdalar, hypothalamic and monoaminergic regions

Sex Hormone-Specific Neuroanatomy of Takotsubo Syndrome: Is the Insular Cortex a Moderator?

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