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Neuronal Control of Breathing: Sex and Stress Hormones

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Abstract

There is a growing public awareness that hormones can have a significant impact on most biological systems, including the control of breathing. This review will focus on the actions of two broad classes of hormones on the neuronal control of breathing: sex hormones and stress hormones. The majority of these hormones are steroids; a striking feature is that both groups are derived from cholesterol. Stress hormones also include many peptides which are produced primarily within the paraventricular nucleus of the hypothalamus (PVN) and secreted into the brain or into the circulatory system. In this article we will first review and discuss the role of sex hormones in respiratory control throughout life, emphasizing how natural fluctuations in hormones are reflected in ventilatory metrics and how disruption of their endogenous cycle can predispose to respiratory disease. These effects may be mediated directly by sex hormone receptors or indirectly by neurotransmitter systems. Next, we will discuss the origins of hypothalamic stress hormones and their relationship with the respiratory control system. This relationship is 2‐fold: (i) via direct anatomical connections to brainstem respiratory control centers, and (ii) via steroid hormones released from the adrenal gland in response to signals from the pituitary gland. Finally, the impact of stress on the development of neural circuits involved in breathing is evaluated in animal models, and the consequences of early stress on respiratory health and disease is discussed. © 2011 American Physiological Society. Compr Physiol 1:2101‐2139, 2011.

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Figure 1. Figure 1.

Origin of sex hormones and stress hormones. (Reused under a GNU free documentation license. All further use of this figure is free and must be under the same terms.)

Figure 2. Figure 2.

Age‐associated changes in ventilation. Differences in eupneic breathing, and in hypoxic and hypercapnic ventilatory responses (HCVRs) in young (Y, 3‐4 months), middle‐aged (MA, 12‐13 months), and old (O, >20 months) male (solid lines) and female (dashed lines) rats. Panels A and B show changes with age in eupneic breathing (A) and changes in arterial (B) at different ages in male and female rats. Panels C and D show the ventilatory response to hypoxia (C) and the change in ventilation with respect to the change in arterial PO2 (D). Panels E and F show the ventilatory response to hypercapnia (E) and the change in ventilation with respect to the change in arterial (F). Taken together, these data show that there are subtle changes in breathing during eupnea, and in response to hypoxia or hypercapnia as rats age. Furthermore, there are significant sex differences between breathing responses at specific ages. For example, the hypoxic ventilatory response (HVR) in female rats increases significantly from Y to MA, but do not change in male rats (C, D). In contrast, the HCVR in male rats decreases significantly from Y to MA, but not in female rats (E, F). *Male versus female (P < 0.05). Y versus MA female (P < 0.05). Y versus MA male (P < 0.05). (Adapted, with permission, from reference )

Figure 3. Figure 3.

Neuroanatomy of the paraventricular nucleus of the hypothalamus (PVN) and its interactions with the respiratory control system. Top panel: Coronal view of the PVN illustrating its main subdivisions and general projections [adapted, with permission, from Swanson and Sawchenko ]. Abbreviations: dp, dorsal parvocellular part; lp, lateral parvocellular part; mpd,v, dorsal and ventral subdivisions of the medial parvocellular part (CRH); pm,l, lateral (vasopressinergic) and medial (oxytocinergic) subdivisions of the posterior magnocellular part; pv, periventricular part. Lower panel: Saggital view of the rat brain showing projections from the paraventricular nucleus to key groups of neurons involved in the genesis and regulation of respiratory activity. The colors indicate the predominant transmitters identified. Note that the interaction between the PVN and some nuclei is bidirectional. Abbreviations: PBC, parabrachial complex; NTS, nucleus of the solitary tract; XII, hypoglossal motor nucleus; Pre‐Böt C, Pre‐Bötzinger complex.

Figure 4. Figure 4.

Neonatal maternal separation (NMS) and sex‐specific activation of the hypothalamo‐pituitary‐adrenal axis. Male/female comparisons of the effects of NMS on basal c‐fos mRNA signal in the PVN in adult rats. (A) Radiographs of PVN section for each group and (B) corresponding histograms showing mean optical density for controls (white bars) and rats previously subjected to NMS (black bars). Between group and between sex comparisons of (C) plasma ACTH concentrations and (D) plasma corticosterone concentrations. Data are expressed as means ± SEM. Statistically different from corresponding control value (P < 0.05) and *statistically different from females (P < 0.05). (Adapted with, permission, from reference )

Figure 5. Figure 5.

Sex‐specific effects of neonatal maternal separation (NMS) on the hypoxic ventilatory response. Comparison of the effects of NMS on HVR of (A) females and (B) male rats. For each group, selected ventilatory variables (minute ventilation, tidal volume, breathing frequency, and inspiratory flow) were measured after 20‐min exposure to moderate hypoxia ( = 0.12) and expressed as a percentage changes from normoxic baseline values. Opened bars represent control animals (males: n = 25 and females: n = 15) and black bars represent rats subjected to NMS (males: n = 15 and females: n = 18). Data are expressed as means ± SEM. Statistically different from corresponding control value (P < 0.05). Indicate a value statistically different from corresponding control value (P = 0.06). (Adapted, with permission, from reference )

Figure 6. Figure 6.

Neonatal maternal separation (NMS) and phrenic nerve responses to hypoxia: the role of GABAergic neurotransmission. Integrated phrenic neurograms comparing the effects of (A) vehicle (phosphate buffered saline; 50 nl) and (B) GABA (50 nl, 5 mM) microinjection in the NTS on the time course of the phrenic burst frequency response to hypoxia ( = 0.12) in male rats between controls (left panels) and animals previously subjected to NMS (right panels). Microinjections were performed 5 min prior to the onset of hypoxia. Panel C shows the mean phrenic burst frequency measured in control (left; circles) and NMS‐treated rats (right; triangles) following microinjection of vehicle (opened symbols) or GABA (black symbols). Frequency values were obtained under baseline conditions and every 20 s during isocapnic hypoxia ( = 0.12; 5 min) for both groups of rats. All data are presented as means ± 1 SEM. *Indicates means that are statistically different from baseline value at P < 0.05. Indicates means that are statistically different from corresponding vehicle value at P < 0.05. (Adapted, with permission, from reference )

Figure 7. Figure 7.

Neonatal maternal separation (NMS) augments hypoxia‐induced NTS activation. Comparison of c‐fos m‐RNA expression levels in the caudal NTS of awake male animals between control and NMS rats following exposure to one of three fraction of inspired O2 level ( ) for 20 min: normoxia ( = 0.21), moderate hypoxia ( = 0.12), or severe hypoxia ( = 0.08). Top panels: Representative photomicrographs comparing c‐fos m‐RNA in situ hybridization signal after exposure to severe hypoxia ( = 0.08) between control rats (left) and rats subjected to NMS (right). The dotted circle represents the central canal. Lower panel: Relationship between the number of c‐fos mRNA‐positive neurons within the NTS and inspired O2 level for controls (open circles) and NMS rats (closed triangles) in the caudal NTS. Data are expressed as means ± SEM. Each value represents the mean number of c‐fos mRNA‐containing perikarya that were counted bilaterally from sections corresponding to the rostro‐caudal coordinates −14.3 to −14.60 from bregma for each experimental condition. For each mean value, the number of rat per condition ranged between 3 and 6. For each rat, a mean number of c‐fos‐positive neurons was obtained by averaging perikarya counted for several sections (the number of sections ranged between 1 and 3). *Indicates means that are statistically different from baseline value at P < 0.05. Indicates means that are statistically different from corresponding control value at P < 0.05. (Adapted, with permission, from reference )

Figure 8. Figure 8.

Sex‐specific effects of neonatal maternal separation (NMS) on the hypercapnic ventilatory response (HCVR). Top panels: Effects of NMS on the time‐course of the breathing frequency response to moderate hypercapnia ( = 0.05) in adult females (A) and males rats (B). Graphics show breathing frequency data (in breaths/min) from controls (opened circles; males: n = 8 and females: n = 11) and rats previously subjected to NMS (black triangles; males: n = 10 and females: n = 16). All values are different from baseline (P < 0.05); however, no symbols are shown for clarity. Lower panels: Effects of NMS on HCVR of adult female (C) and male (D) rats. For each group, selected ventilatory variables (minute ventilation, tidal volume, breathing frequency, and inspiratory flow) were measured after 20 min of exposure to moderate hypercapnia ( = 0.05) and expressed as a percentage changes from normoxic baseline values. Data are compared between controls (open bars; males: n = 8 and females: n = 11) and rats previously subjected to NMS (black bars; males: n = 10 and females: n = 16). Values are expressed as mean ± SEM. Statistically different from corresponding control value (P < 0.05) and *statistically different from baseline (P < 0.05). Data are expressed as means ± SEM. (Adapted, with permission, from reference )



Figure 1.

Origin of sex hormones and stress hormones. (Reused under a GNU free documentation license. All further use of this figure is free and must be under the same terms.)



Figure 2.

Age‐associated changes in ventilation. Differences in eupneic breathing, and in hypoxic and hypercapnic ventilatory responses (HCVRs) in young (Y, 3‐4 months), middle‐aged (MA, 12‐13 months), and old (O, >20 months) male (solid lines) and female (dashed lines) rats. Panels A and B show changes with age in eupneic breathing (A) and changes in arterial (B) at different ages in male and female rats. Panels C and D show the ventilatory response to hypoxia (C) and the change in ventilation with respect to the change in arterial PO2 (D). Panels E and F show the ventilatory response to hypercapnia (E) and the change in ventilation with respect to the change in arterial (F). Taken together, these data show that there are subtle changes in breathing during eupnea, and in response to hypoxia or hypercapnia as rats age. Furthermore, there are significant sex differences between breathing responses at specific ages. For example, the hypoxic ventilatory response (HVR) in female rats increases significantly from Y to MA, but do not change in male rats (C, D). In contrast, the HCVR in male rats decreases significantly from Y to MA, but not in female rats (E, F). *Male versus female (P < 0.05). Y versus MA female (P < 0.05). Y versus MA male (P < 0.05). (Adapted, with permission, from reference )



Figure 3.

Neuroanatomy of the paraventricular nucleus of the hypothalamus (PVN) and its interactions with the respiratory control system. Top panel: Coronal view of the PVN illustrating its main subdivisions and general projections [adapted, with permission, from Swanson and Sawchenko ]. Abbreviations: dp, dorsal parvocellular part; lp, lateral parvocellular part; mpd,v, dorsal and ventral subdivisions of the medial parvocellular part (CRH); pm,l, lateral (vasopressinergic) and medial (oxytocinergic) subdivisions of the posterior magnocellular part; pv, periventricular part. Lower panel: Saggital view of the rat brain showing projections from the paraventricular nucleus to key groups of neurons involved in the genesis and regulation of respiratory activity. The colors indicate the predominant transmitters identified. Note that the interaction between the PVN and some nuclei is bidirectional. Abbreviations: PBC, parabrachial complex; NTS, nucleus of the solitary tract; XII, hypoglossal motor nucleus; Pre‐Böt C, Pre‐Bötzinger complex.



Figure 4.

Neonatal maternal separation (NMS) and sex‐specific activation of the hypothalamo‐pituitary‐adrenal axis. Male/female comparisons of the effects of NMS on basal c‐fos mRNA signal in the PVN in adult rats. (A) Radiographs of PVN section for each group and (B) corresponding histograms showing mean optical density for controls (white bars) and rats previously subjected to NMS (black bars). Between group and between sex comparisons of (C) plasma ACTH concentrations and (D) plasma corticosterone concentrations. Data are expressed as means ± SEM. Statistically different from corresponding control value (P < 0.05) and *statistically different from females (P < 0.05). (Adapted with, permission, from reference )



Figure 5.

Sex‐specific effects of neonatal maternal separation (NMS) on the hypoxic ventilatory response. Comparison of the effects of NMS on HVR of (A) females and (B) male rats. For each group, selected ventilatory variables (minute ventilation, tidal volume, breathing frequency, and inspiratory flow) were measured after 20‐min exposure to moderate hypoxia ( = 0.12) and expressed as a percentage changes from normoxic baseline values. Opened bars represent control animals (males: n = 25 and females: n = 15) and black bars represent rats subjected to NMS (males: n = 15 and females: n = 18). Data are expressed as means ± SEM. Statistically different from corresponding control value (P < 0.05). Indicate a value statistically different from corresponding control value (P = 0.06). (Adapted, with permission, from reference )



Figure 6.

Neonatal maternal separation (NMS) and phrenic nerve responses to hypoxia: the role of GABAergic neurotransmission. Integrated phrenic neurograms comparing the effects of (A) vehicle (phosphate buffered saline; 50 nl) and (B) GABA (50 nl, 5 mM) microinjection in the NTS on the time course of the phrenic burst frequency response to hypoxia ( = 0.12) in male rats between controls (left panels) and animals previously subjected to NMS (right panels). Microinjections were performed 5 min prior to the onset of hypoxia. Panel C shows the mean phrenic burst frequency measured in control (left; circles) and NMS‐treated rats (right; triangles) following microinjection of vehicle (opened symbols) or GABA (black symbols). Frequency values were obtained under baseline conditions and every 20 s during isocapnic hypoxia ( = 0.12; 5 min) for both groups of rats. All data are presented as means ± 1 SEM. *Indicates means that are statistically different from baseline value at P < 0.05. Indicates means that are statistically different from corresponding vehicle value at P < 0.05. (Adapted, with permission, from reference )



Figure 7.

Neonatal maternal separation (NMS) augments hypoxia‐induced NTS activation. Comparison of c‐fos m‐RNA expression levels in the caudal NTS of awake male animals between control and NMS rats following exposure to one of three fraction of inspired O2 level ( ) for 20 min: normoxia ( = 0.21), moderate hypoxia ( = 0.12), or severe hypoxia ( = 0.08). Top panels: Representative photomicrographs comparing c‐fos m‐RNA in situ hybridization signal after exposure to severe hypoxia ( = 0.08) between control rats (left) and rats subjected to NMS (right). The dotted circle represents the central canal. Lower panel: Relationship between the number of c‐fos mRNA‐positive neurons within the NTS and inspired O2 level for controls (open circles) and NMS rats (closed triangles) in the caudal NTS. Data are expressed as means ± SEM. Each value represents the mean number of c‐fos mRNA‐containing perikarya that were counted bilaterally from sections corresponding to the rostro‐caudal coordinates −14.3 to −14.60 from bregma for each experimental condition. For each mean value, the number of rat per condition ranged between 3 and 6. For each rat, a mean number of c‐fos‐positive neurons was obtained by averaging perikarya counted for several sections (the number of sections ranged between 1 and 3). *Indicates means that are statistically different from baseline value at P < 0.05. Indicates means that are statistically different from corresponding control value at P < 0.05. (Adapted, with permission, from reference )



Figure 8.

Sex‐specific effects of neonatal maternal separation (NMS) on the hypercapnic ventilatory response (HCVR). Top panels: Effects of NMS on the time‐course of the breathing frequency response to moderate hypercapnia ( = 0.05) in adult females (A) and males rats (B). Graphics show breathing frequency data (in breaths/min) from controls (opened circles; males: n = 8 and females: n = 11) and rats previously subjected to NMS (black triangles; males: n = 10 and females: n = 16). All values are different from baseline (P < 0.05); however, no symbols are shown for clarity. Lower panels: Effects of NMS on HCVR of adult female (C) and male (D) rats. For each group, selected ventilatory variables (minute ventilation, tidal volume, breathing frequency, and inspiratory flow) were measured after 20 min of exposure to moderate hypercapnia ( = 0.05) and expressed as a percentage changes from normoxic baseline values. Data are compared between controls (open bars; males: n = 8 and females: n = 11) and rats previously subjected to NMS (black bars; males: n = 10 and females: n = 16). Values are expressed as mean ± SEM. Statistically different from corresponding control value (P < 0.05) and *statistically different from baseline (P < 0.05). Data are expressed as means ± SEM. (Adapted, with permission, from reference )

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Mary Behan, Richard Kinkead. Neuronal Control of Breathing: Sex and Stress Hormones. Compr Physiol 2011, 1: 2101-2139. doi: 10.1002/cphy.c100027