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Identification of neural cells activated by mating stimulus in the periaqueductal gray in female rats.

ABSTRACT: Induction of lordosis as typical female sexual behavior in rodents is dependent on a mount stimulus from males and blood levels of estrogen. Periaqueductal gray (PAG) efferent neurons have been suggested to be important for lordosis behavior; however, the neurochemical basis remains to be understood. In this study, we neuroanatomically examined (1) whether PAG neurons activated by mating stimulus project to the medullary reticular formation (MRF), which is also a required area for lordosis; and (2) whether these neurons are glutamatergic. Mating stimulus significantly increased the number of cFos-immunoreactive (ir) neurons in the PAG, particularly in its lateral region. Half of cFos-ir neurons in the lateral PAG were positive for a retrograde tracer (FluoroGold; FG) injected into the MRF. cFos-ir neurons also colocalized with mRNA of vesicular glutamate transporter 2 (vGLUT2), a molecular marker for glutamatergic neurons. Using retrograde tracing and in situ hybridization in conjunction with fluorescent microscopy, we also found FG and vGLUT2 mRNA double-positive neurons in the lateral PAG. These results suggest that glutamatergic neurons in the lateral PAG project to the MRF and are involved in lordosis behavior in female rats.

SUBMITTER: Yamada S

PROVIDER: S-EPMC4270180 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Identification of neural cells activated by mating stimulus in the periaqueductal gray in female rats.

Yamada Shunji S Kawata Mitsuhiro M

Frontiers in neuroscience 20141218

Induction of lordosis as typical female sexual behavior in rodents is dependent on a mount stimulus from males and blood levels of estrogen. Periaqueductal gray (PAG) efferent neurons have been suggested to be important for lordosis behavior; however, the neurochemical basis remains to be understood. In this study, we neuroanatomically examined (1) whether PAG neurons activated by mating stimulus project to the medullary reticular formation (MRF), which is also a required area for lordosis; and ...[more]

PMID: 25565950

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Project description:Background: Parkinson’s disease (PD) is a progressive, degenerative disease with early-stage pathology hypothesized to manifest in brainstem regions. Vocal deficits, including soft monotone speech, result in significant clinical and quality of life issues and are present in 90% of PD patients; yet, the underlying pathology mediating these significant voice deficits is unknown. The Pink1-/- rat is a valid model of early-onset PD that presents with analogous vocal communication deficits (e.g. reduced loudness). Previous work shows abnormal α-synuclein protein aggregation in the periaqueductal gray (PAG), a brain region critical and necessary to the modulation of mammalian vocal behavior. In this study, we used high-throughput RNA sequencing to examine gene expression within the PAG of both male and female Pink1-/- rats as compared to age-matched wildtype controls. We used a bioinformatic approach to (1) test the hypothesis that loss of Pink1 in the PAG will influence expression of genes that interact with Pink1, (2) highlight other key genes that relate to Mendelian PD, and (3) catalog molecular targets important for the production of rat vocalizations. Results: Knockout of the Pink1 gene resulted in differentially expressed genes for both male and female rats. Pathway analysis highlighted several significant metabolic pathways. Weighted gene co-expression network analysis (WGCNA) was used to identify gene nodes and their interactions in (A) males, (B) females, and (C) combined-sexes datasets. For each analysis, within the module containing the Pink1 gene, Pink1 itself was the central node with the highest number of interactions with other genes including solute carriers, glutamate metabotropic receptors, and genes associated with protein localization. Strong connections between Pink1 and Krt2 and Hfe were found in both males and female datasets. In females a number of modules were significantly correlated with vocalization traits. Of interest, gene enrichment of the key vocal Cyan module in females showed a significant number of neuromodulatory genes including Nts, Slc6a4, Slc10a4, Ndnf, and Gpr160, that may be responsible for the modulation of rat vocalizations. The top biological pathways within the female Cyan vocal module included the regulation of membrane depolarization, indolalkylamine metabolic process, and monoamine transport. Conclusions: Overall, this work supports the premise that gene expression changes in the PAG may contribute to the vocal behavioral and deficits observed in this PD rat model. Additionally, this dataset identifies genes that represent new therapeutic targets for PD voice disorders.

Project description:Neuroimmune signaling is increasingly identified as a critical component of various illnesses, including chronic pain, substance use disorder, and depression. However, the underlying neural mechanisms remain unclear. Proinflammatory cytokines, such as tumor necrosis factor-α (TNF-α), may play a role by modulating synaptic function and long-term plasticity. The midbrain structure periaqueductal gray (PAG) plays a well-established role in pain processing, and although TNF-α inhibitors have emerged as a therapeutic strategy for pain-related disorders, the impact of TNF-α on PAG neuronal activity has not been thoroughly characterized. Recent studies have identified subpopulations of ventrolateral PAG (vlPAG) with opposing effects on nociception, with dopamine (DA) neurons driving pain relief in contrast to GABA neurons. Therefore, we used slice physiology to examine the impact of TNF-α on neuronal activity of both these subpopulations. We focused on female mice since the PAG is a sexually dimorphic region and most studies use male subjects, limiting our understanding of mechanistic variations in females. We selectively targeted GABA and DA neurons using transgenic reporter lines. Following exposure to TNF-α, there was an increase in excitability of GABA neurons along with a reduction in glutamatergic synaptic transmission. In DA neurons, TNF-α exposure resulted in a robust decrease in excitability along with a modest reduction in glutamatergic synaptic transmission. Interestingly, TNF-α had no effect on inhibitory transmission onto DA neurons. Collectively, these data suggest that TNF-α differentially affects the function of GABA and DA neurons in female mice and enhances our understanding of how TNF-α-mediated signaling modulates vlPAG function.NEW & NOTEWORTHY This study describes the effects of TNF-α on two distinct subpopulations of neurons in the vlPAG. We show that TNF-α alters both neuronal excitability and glutamatergic synaptic transmission on GABA and dopamine neurons within the vlPAG of female mice. This provides critical new information on the role of TNF-α in the potential modulation of pain, since activation of vlPAG GABA neurons drives nociception, whereas activation of dopamine neurons drives analgesia.

Dataset Information

Identification of neural cells activated by mating stimulus in the periaqueductal gray in female rats.

Publications

Identification of neural cells activated by mating stimulus in the periaqueductal gray in female rats.

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