Nicotine modulates multiple regions in the limbic stress network regulating activation of hypophysiotrophic neurons in hypothalamic paraventricular nucleus

Guoliang Yu, Burt Sharp

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

Nicotine intake affects CNS responses to stressors. We reported that nicotine self-administration (SA) augmented the hypothalamo-pituitary-adrenal (HPA) stress response, in part because of the altered neurotransmission and neuropeptide expression within hypothalamic paraventricular nucleus (PVN). Limbic-PVN interactions involving medial prefrontal cortex, amygdala, and bed nucleus of the stria terminalis (BST) greatly impact the HPA stress response. Therefore, we investigated the effects of nicotine SA on stress-induced neuronal activation in limbic-PVN network, using c-Fos protein immunohistochemistry and retrograde tracing. Nicotine decreased stress-induced c-Fos in prelimbic cortex (PrL), anteroventral BST (avBST), and peri-PVN, but increased c-Fos induction in medial amygdala (MeA), locus coeruleus, and PVN. Fluoro-gold (FG) was injected into avBST or PVN, as GABAergic neurons in avBST projecting to PVN corticotrophin-releasing factor neurons relay information from both PrL glutamatergic and MeA GABAergic neurons. The stress-induced c-Fos expression in retrograde-labeled FG+ neurons was decreased in PrL by nicotine, but increased in MeA, and also reduced in avBST. Therefore, within limbic-PVN network, nicotine SA exerts selective regional effects on neuronal activation by stress. These findings expand the mechanistic framework by demonstrating altered limbic-BST-PVN interactions underlying the disinhibition of PVN corticotrophin-releasing factor neurons, an essential component of the amplified HPA response to stress by nicotine. We determined the role of the limbic stress network in nicotine modulation of HPA axis. Nicotine self-administration markedly reduced footshock-induced c-Fos in Fluoro-gold (injected into BST) retrograde-labeled neurons in prelimbic cortex. Other limbic regions regulating GABAergic inputs to CRF neurons of HPA axis were also affected. Thus, nicotine modulates the activation of multiple limbic regions regulating HPA response to stress.

Original languageEnglish (US)
Pages (from-to)628-640
Number of pages13
JournalJournal of Neurochemistry
Volume122
Issue number3
DOIs
StatePublished - Aug 1 2012

Fingerprint

Paraventricular Hypothalamic Nucleus
Nicotine
Neurons
Chemical activation
Septal Nuclei
Self Administration
Amygdala
GABAergic Neurons
Corticotropin-Releasing Hormone
Proto-Oncogene Proteins c-fos
Locus Coeruleus
Prefrontal Cortex
Neuropeptides
Synaptic Transmission
Immunohistochemistry
Modulation

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Cellular and Molecular Neuroscience

Cite this

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title = "Nicotine modulates multiple regions in the limbic stress network regulating activation of hypophysiotrophic neurons in hypothalamic paraventricular nucleus",
abstract = "Nicotine intake affects CNS responses to stressors. We reported that nicotine self-administration (SA) augmented the hypothalamo-pituitary-adrenal (HPA) stress response, in part because of the altered neurotransmission and neuropeptide expression within hypothalamic paraventricular nucleus (PVN). Limbic-PVN interactions involving medial prefrontal cortex, amygdala, and bed nucleus of the stria terminalis (BST) greatly impact the HPA stress response. Therefore, we investigated the effects of nicotine SA on stress-induced neuronal activation in limbic-PVN network, using c-Fos protein immunohistochemistry and retrograde tracing. Nicotine decreased stress-induced c-Fos in prelimbic cortex (PrL), anteroventral BST (avBST), and peri-PVN, but increased c-Fos induction in medial amygdala (MeA), locus coeruleus, and PVN. Fluoro-gold (FG) was injected into avBST or PVN, as GABAergic neurons in avBST projecting to PVN corticotrophin-releasing factor neurons relay information from both PrL glutamatergic and MeA GABAergic neurons. The stress-induced c-Fos expression in retrograde-labeled FG+ neurons was decreased in PrL by nicotine, but increased in MeA, and also reduced in avBST. Therefore, within limbic-PVN network, nicotine SA exerts selective regional effects on neuronal activation by stress. These findings expand the mechanistic framework by demonstrating altered limbic-BST-PVN interactions underlying the disinhibition of PVN corticotrophin-releasing factor neurons, an essential component of the amplified HPA response to stress by nicotine. We determined the role of the limbic stress network in nicotine modulation of HPA axis. Nicotine self-administration markedly reduced footshock-induced c-Fos in Fluoro-gold (injected into BST) retrograde-labeled neurons in prelimbic cortex. Other limbic regions regulating GABAergic inputs to CRF neurons of HPA axis were also affected. Thus, nicotine modulates the activation of multiple limbic regions regulating HPA response to stress.",
author = "Guoliang Yu and Burt Sharp",
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