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Neonatal Maternal Separation Augments Carotid Body Response to Hypoxia in Adult Males but Not Female Rats

View Article: PubMed Central - PubMed

ABSTRACT

Perinatal exposure to adverse experiences disrupts brain development, including the brainstem network that regulates breathing. At adulthood, rats previously subjected to stress (in the form of neonatal maternal separation; NMS) display features reported in patients suffering from sleep disordered breathing, including an increased hypoxic ventilatory response and hypertension. This effect is also sex-specific (males only). Based on these observations, we hypothesized that NMS augments the carotid body's O2-chemosensitivity. Using an isolated and perfused ex vivo carotid body preparation from adult rats we compared carotid sinus nerve (CSN) responses to hypoxia and hypercapnia in carotid bodies harvested from adult rats that either experienced control conditions (no experimental manipulation) or were subjected to NMS (3 h/day from postnatal days 3 to 12). In males, the CSN response to hypoxia measured in preparations from NMS males was 1.5 fold higher than controls. In control rats, the female's response was similar to that of males; however, the increase in CSN activity measured in NMS females was 3.0 times lower than controls. The CSN response to hypercapnia was not influenced by stress or sex. We conclude that NMS is sufficient to have persistent and sex-specific effects on the carotid body's response to hypoxia. Because NMS also has sex-specific effects on the neuroendocrine response to stress, we propose that carotid body function is influenced by stress hormones. This, in turn, leads to a predisposition toward cardio-respiratory disorders.

No MeSH data available.


Related in: MedlinePlus

Neonatal maternal separation (NMS) increases carotid sinus nerve (CSN) response to hypoxia in male rats. (A) Original recordings comparing CSN activity from ex vivo preparations of perfused carotid body/CSN from control and NMS males under hyperoxia (FiO2 = 0.95), hypoxia (FiO2 = 0.0) and hyperoxic after hypoxia (recovery). (B) Comparison of the mean carotid sinus nerve activity (imp/sec) over the course of the hypoxic protocol between carotid bodies from control (open squares; n = 8) and NMS rats (black squares; n = 8). Hypoxia begins at T = 0 and is maintained until T = 500 s (end of plateau phase), followed by hyperoxic recovery; each data point represents the mean value on a second by second basis. (C) Histograms comparing mean CSN activity for each specific experimental condition between control (white bars; n = 8) and NMS (black bars; n = 8) male rats. Data are reported as means ± SD. *indicates a value statistically different from control at p ≤ 0.05.
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Figure 1: Neonatal maternal separation (NMS) increases carotid sinus nerve (CSN) response to hypoxia in male rats. (A) Original recordings comparing CSN activity from ex vivo preparations of perfused carotid body/CSN from control and NMS males under hyperoxia (FiO2 = 0.95), hypoxia (FiO2 = 0.0) and hyperoxic after hypoxia (recovery). (B) Comparison of the mean carotid sinus nerve activity (imp/sec) over the course of the hypoxic protocol between carotid bodies from control (open squares; n = 8) and NMS rats (black squares; n = 8). Hypoxia begins at T = 0 and is maintained until T = 500 s (end of plateau phase), followed by hyperoxic recovery; each data point represents the mean value on a second by second basis. (C) Histograms comparing mean CSN activity for each specific experimental condition between control (white bars; n = 8) and NMS (black bars; n = 8) male rats. Data are reported as means ± SD. *indicates a value statistically different from control at p ≤ 0.05.

Mentions: Prior to the onset of the stimulation protocol, carotid body preparations perfused with a hyperoxic solution showed discharge rates of ~5 impulses/sec (range: 1.6–7.9 impulses/sec). This basal activity did not differ between groups and was not influenced by sex (Figures 1–4).


Neonatal Maternal Separation Augments Carotid Body Response to Hypoxia in Adult Males but Not Female Rats
Neonatal maternal separation (NMS) increases carotid sinus nerve (CSN) response to hypoxia in male rats. (A) Original recordings comparing CSN activity from ex vivo preparations of perfused carotid body/CSN from control and NMS males under hyperoxia (FiO2 = 0.95), hypoxia (FiO2 = 0.0) and hyperoxic after hypoxia (recovery). (B) Comparison of the mean carotid sinus nerve activity (imp/sec) over the course of the hypoxic protocol between carotid bodies from control (open squares; n = 8) and NMS rats (black squares; n = 8). Hypoxia begins at T = 0 and is maintained until T = 500 s (end of plateau phase), followed by hyperoxic recovery; each data point represents the mean value on a second by second basis. (C) Histograms comparing mean CSN activity for each specific experimental condition between control (white bars; n = 8) and NMS (black bars; n = 8) male rats. Data are reported as means ± SD. *indicates a value statistically different from control at p ≤ 0.05.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5037225&req=5

Figure 1: Neonatal maternal separation (NMS) increases carotid sinus nerve (CSN) response to hypoxia in male rats. (A) Original recordings comparing CSN activity from ex vivo preparations of perfused carotid body/CSN from control and NMS males under hyperoxia (FiO2 = 0.95), hypoxia (FiO2 = 0.0) and hyperoxic after hypoxia (recovery). (B) Comparison of the mean carotid sinus nerve activity (imp/sec) over the course of the hypoxic protocol between carotid bodies from control (open squares; n = 8) and NMS rats (black squares; n = 8). Hypoxia begins at T = 0 and is maintained until T = 500 s (end of plateau phase), followed by hyperoxic recovery; each data point represents the mean value on a second by second basis. (C) Histograms comparing mean CSN activity for each specific experimental condition between control (white bars; n = 8) and NMS (black bars; n = 8) male rats. Data are reported as means ± SD. *indicates a value statistically different from control at p ≤ 0.05.
Mentions: Prior to the onset of the stimulation protocol, carotid body preparations perfused with a hyperoxic solution showed discharge rates of ~5 impulses/sec (range: 1.6–7.9 impulses/sec). This basal activity did not differ between groups and was not influenced by sex (Figures 1–4).

View Article: PubMed Central - PubMed

ABSTRACT

Perinatal exposure to adverse experiences disrupts brain development, including the brainstem network that regulates breathing. At adulthood, rats previously subjected to stress (in the form of neonatal maternal separation; NMS) display features reported in patients suffering from sleep disordered breathing, including an increased hypoxic ventilatory response and hypertension. This effect is also sex-specific (males only). Based on these observations, we hypothesized that NMS augments the carotid body's O2-chemosensitivity. Using an isolated and perfused ex vivo carotid body preparation from adult rats we compared carotid sinus nerve (CSN) responses to hypoxia and hypercapnia in carotid bodies harvested from adult rats that either experienced control conditions (no experimental manipulation) or were subjected to NMS (3 h/day from postnatal days 3 to 12). In males, the CSN response to hypoxia measured in preparations from NMS males was 1.5 fold higher than controls. In control rats, the female's response was similar to that of males; however, the increase in CSN activity measured in NMS females was 3.0 times lower than controls. The CSN response to hypercapnia was not influenced by stress or sex. We conclude that NMS is sufficient to have persistent and sex-specific effects on the carotid body's response to hypoxia. Because NMS also has sex-specific effects on the neuroendocrine response to stress, we propose that carotid body function is influenced by stress hormones. This, in turn, leads to a predisposition toward cardio-respiratory disorders.

No MeSH data available.


Related in: MedlinePlus