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Neuroendocrine Regulation of Lactation and Milk Production

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Abstract

Prolactin (PRL) released from lactotrophs of the anterior pituitary gland in response to the suckling by the offspring is the major hormonal signal responsible for stimulation of milk synthesis in the mammary glands. PRL secretion is under chronic inhibition exerted by dopamine (DA), which is released from neurons of the arcuate nucleus of the hypothalamus into the hypophyseal portal vasculature. Suckling by the young activates ascending systems that decrease the release of DA from this system, resulting in enhanced responsiveness to one or more PRL‐releasing hormones, such as thyrotropin‐releasing hormone. The neuropeptide oxytocin (OT), synthesized in magnocellular neurons of the hypothalamic supraoptic, paraventricular, and several accessory nuclei, is responsible for contracting the myoepithelial cells of the mammary gland to produce milk ejection. Electrophysiological recordings demonstrate that shortly before each milk ejection, the entire neurosecretory OT population fires a synchronized burst of action potentials (the milk ejection burst), resulting in release of OT from nerve terminals in the neurohypophysis. Both of these neuroendocrine systems undergo alterations in late gestation that prepare them for the secretory demands of lactation, and that reduce their responsiveness to stimuli other than suckling, especially physical stressors. The demands of milk synthesis and release produce a condition of negative energy balance in the suckled mother, and, in laboratory rodents, are accompanied by a dramatic hyperphagia. The reduction in secretion of the adipocyte hormone, leptin, a hallmark of negative energy balance, may be an important endocrine signal to hypothalamic systems that integrate lactation‐associated food intake with neuroendocrine systems. © 2015 American Physiological Society. Compr Physiol 5:255‐291, 2015.

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Figure 1. Figure 1. Typical plasma profiles of oxytocin, PRL, an epinephrine (EPI) and milk yield in a standard suckling test (eight pups after 6‐8 h separation) in female rats. Oxytocin release episodes are presented as black bars. For experimental details, see references in . Reproduced with permission.
Figure 2. Figure 2. Key structures in the suckling‐activated afferent pathway to the neuroendocrine hypothalamus. See text for details on experimental approaches. Abbreviations: AP, anterior pituitary gland; ARC: arcuate nucleus of the hypothalamus; DCA: dorsochiasmatic area; DHsc: dorsal horn of the spinal cord; DMN: dorsomedial nucleus of the hypothalamus; LC: locus coreruleus; LCN: lateral cervical nucleus; LS/BNST: lateral septum/bed nucleus of the stria terminalis; Mam B: mammillary body complex; ME: median eminence; MFB: medial forebrain bundle; MPOA: medial preoptic area; NE: norepinephrine; NTS: nucleus tractus solitaries; PAG/DR: periacqueductal gray/dorsal raphe nucleus; PB; parabrachial nucleus; PIL: posterior intralaminar complex; PL: paralemniscal nucleus; pnr: perinuclear regions with glutamatergic (Glu) and GABAergic (GABA) neurons; PVN: paraventricular nucleus of the hypothalamus; SON: supraoptic nucleus; TIP39: tuberoinfundibular peptide of 39 residues; VLM: ventrolateral medulla; VMM: ventromedial medulla; ZI/FoF: zona incerta/Fields of Forel; 5‐HT: serotonin
Figure 3. Figure 3. Hypothesized signal transduction mechanisms for the potentiation of TRH stimulation of PRL release by DA withdrawal. See text for details. The reduction in DA secretion into the portal vasculature in response to suckling activates phospholipase C, via disinhibition, resulting in increased formation of inositol 1,4,5‐trisphosphate (IP3), which increases mobilization of Ca2+ from intracellular sources, and of diacylglycerol (DAG), which activates protein kinase C (PKC), resulting in increased entry of Ca2+ via voltage‐regulated calcium channels. DA withdrawal per se most likely also leads to increased extracellular Ca2+ entry. TRH receptors are positively coupled to generation of these intracellular messengers, and the increased release of TRH in response to suckling thus enhances the rise in intracellular Ca2+ concentrations ([Ca2+]i) resulting from DA withdrawal, leading to the exocytosis of PRL.
Figure 4. Figure 4. Some identified neurochemical inputs to the neuroendocrine hypothalamus activated by suckling to stimulate PRL secretion. See text for details. See Figure for abbreviations.
Figure 5. Figure 5. Local neurochemical circuitry in the arcuate nucleus regulating PRL secretion during lactation. Hypophysiotropic dopamine (DA) neurons in the arcuate nucleus that also express neuropeptide Y (NPY) are the major inhibitory regulators of PRL at the lactotroph. The activity of the DA/NPY cells can be inhibited by actions of GABAergic and endogenous opioid peptidergic (dynorphin, β‐endorphin and met‐enkephalin) neurons present within the arcuate nucleus. Dynorphin neurons, in turn, are activated by neurons of the posterior intralaminar (PIL) complex, known to be activated by suckling and to express TIP39. Serotoninergic neurons (5‐HT) of the dorsal raphe, also activated by suckling, also innervate and inhibit the DA/NPY cells. The inhibitory EOP influence on DA/NPY neurons is also mediated in part by enhanced 5‐HT release.
Figure 6. Figure 6. Intrahypothalamic circuitry and sources of excitatory and inhibitory amino acid inputs to OT neurons in the magnocellular nuclei. See Figure for abbreviations. Glutamate neurons innervating the PVN and SON are located in the LS/BNST, DMN and Mam B, and also in perinuclear regions (PNR) adjacent to each magnocellular nucleus. GABA innervation to OT neurons also largely emanates from adjacent PNRs. Arrows also show bilateral inputs to PVN and SON from the DCA; reciprocal connections between the PVN and SON ipsilaterally, and bilateral PVN‐PVN and SON‐SON interconnections, which are believed to participate in synchronization of milk ejection bursts (see text for details).
Figure 7. Figure 7. Long‐range, direct inputs from brainstem nuclei to the PVN and SON. Abbreviations: Acc: accessory magnocellular OT neurons; NL: neural lobe. See Figure for other abbreviations. Noradrenergic neurons in the A1 (VLM) and A2 (NTS) cell groups directly innervate OT neurons in PVN and SON, and probably also the accessory OT populations. The PVN also receives noradrenergic input from the LC. Also depicted are the direct connections from neurochemically unidentified VMM neurons, passing through the DCA to PVN and SON.
Figure 8. Figure 8. Integration by arcuate NPY/AgRP neurons of hyperphagia and neuroendocrine adaptations to the negative energy balance in lactation. The negative energy balance due to the demands of milk synthesis and secretion, results in decreased leptin secretion from adipose tissue. Hypo‐leptinemia provides an important signal to stimulate the expression of NPY and AgRP in arcuate neurons, which mediate in part the hyperphagia of lactation as well as increased secretion of ACTH and decrease in TSH and LH secretion. PRL released in response to suckling also contributes significantly to lactational hyperphagia. These mechanisms depend upon the suckling stimulus.


Figure 1. Typical plasma profiles of oxytocin, PRL, an epinephrine (EPI) and milk yield in a standard suckling test (eight pups after 6‐8 h separation) in female rats. Oxytocin release episodes are presented as black bars. For experimental details, see references in . Reproduced with permission.


Figure 2. Key structures in the suckling‐activated afferent pathway to the neuroendocrine hypothalamus. See text for details on experimental approaches. Abbreviations: AP, anterior pituitary gland; ARC: arcuate nucleus of the hypothalamus; DCA: dorsochiasmatic area; DHsc: dorsal horn of the spinal cord; DMN: dorsomedial nucleus of the hypothalamus; LC: locus coreruleus; LCN: lateral cervical nucleus; LS/BNST: lateral septum/bed nucleus of the stria terminalis; Mam B: mammillary body complex; ME: median eminence; MFB: medial forebrain bundle; MPOA: medial preoptic area; NE: norepinephrine; NTS: nucleus tractus solitaries; PAG/DR: periacqueductal gray/dorsal raphe nucleus; PB; parabrachial nucleus; PIL: posterior intralaminar complex; PL: paralemniscal nucleus; pnr: perinuclear regions with glutamatergic (Glu) and GABAergic (GABA) neurons; PVN: paraventricular nucleus of the hypothalamus; SON: supraoptic nucleus; TIP39: tuberoinfundibular peptide of 39 residues; VLM: ventrolateral medulla; VMM: ventromedial medulla; ZI/FoF: zona incerta/Fields of Forel; 5‐HT: serotonin


Figure 3. Hypothesized signal transduction mechanisms for the potentiation of TRH stimulation of PRL release by DA withdrawal. See text for details. The reduction in DA secretion into the portal vasculature in response to suckling activates phospholipase C, via disinhibition, resulting in increased formation of inositol 1,4,5‐trisphosphate (IP3), which increases mobilization of Ca2+ from intracellular sources, and of diacylglycerol (DAG), which activates protein kinase C (PKC), resulting in increased entry of Ca2+ via voltage‐regulated calcium channels. DA withdrawal per se most likely also leads to increased extracellular Ca2+ entry. TRH receptors are positively coupled to generation of these intracellular messengers, and the increased release of TRH in response to suckling thus enhances the rise in intracellular Ca2+ concentrations ([Ca2+]i) resulting from DA withdrawal, leading to the exocytosis of PRL.


Figure 4. Some identified neurochemical inputs to the neuroendocrine hypothalamus activated by suckling to stimulate PRL secretion. See text for details. See Figure for abbreviations.


Figure 5. Local neurochemical circuitry in the arcuate nucleus regulating PRL secretion during lactation. Hypophysiotropic dopamine (DA) neurons in the arcuate nucleus that also express neuropeptide Y (NPY) are the major inhibitory regulators of PRL at the lactotroph. The activity of the DA/NPY cells can be inhibited by actions of GABAergic and endogenous opioid peptidergic (dynorphin, β‐endorphin and met‐enkephalin) neurons present within the arcuate nucleus. Dynorphin neurons, in turn, are activated by neurons of the posterior intralaminar (PIL) complex, known to be activated by suckling and to express TIP39. Serotoninergic neurons (5‐HT) of the dorsal raphe, also activated by suckling, also innervate and inhibit the DA/NPY cells. The inhibitory EOP influence on DA/NPY neurons is also mediated in part by enhanced 5‐HT release.


Figure 6. Intrahypothalamic circuitry and sources of excitatory and inhibitory amino acid inputs to OT neurons in the magnocellular nuclei. See Figure for abbreviations. Glutamate neurons innervating the PVN and SON are located in the LS/BNST, DMN and Mam B, and also in perinuclear regions (PNR) adjacent to each magnocellular nucleus. GABA innervation to OT neurons also largely emanates from adjacent PNRs. Arrows also show bilateral inputs to PVN and SON from the DCA; reciprocal connections between the PVN and SON ipsilaterally, and bilateral PVN‐PVN and SON‐SON interconnections, which are believed to participate in synchronization of milk ejection bursts (see text for details).


Figure 7. Long‐range, direct inputs from brainstem nuclei to the PVN and SON. Abbreviations: Acc: accessory magnocellular OT neurons; NL: neural lobe. See Figure for other abbreviations. Noradrenergic neurons in the A1 (VLM) and A2 (NTS) cell groups directly innervate OT neurons in PVN and SON, and probably also the accessory OT populations. The PVN also receives noradrenergic input from the LC. Also depicted are the direct connections from neurochemically unidentified VMM neurons, passing through the DCA to PVN and SON.


Figure 8. Integration by arcuate NPY/AgRP neurons of hyperphagia and neuroendocrine adaptations to the negative energy balance in lactation. The negative energy balance due to the demands of milk synthesis and secretion, results in decreased leptin secretion from adipose tissue. Hypo‐leptinemia provides an important signal to stimulate the expression of NPY and AgRP in arcuate neurons, which mediate in part the hyperphagia of lactation as well as increased secretion of ACTH and decrease in TSH and LH secretion. PRL released in response to suckling also contributes significantly to lactational hyperphagia. These mechanisms depend upon the suckling stimulus.
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William R. Crowley. Neuroendocrine Regulation of Lactation and Milk Production. Compr Physiol 2014, 5: 255-291. doi: 10.1002/cphy.c140029