Stress, prolactin and hypothalamic dopaminergic neurons

doi:10.1016/0028-3908(87)90055-4

Neuropharmacology

Volume 26, Issue 7, Part 2, July 1987, Pages 801-808

https://doi.org/10.1016/0028-3908(87)90055-4 Get rights and content

Abstract

Most of what is known about dopamine (DA)-containing neurons in the brain has been learned from studies on the nigrostriatal system, although it is misleading to consider a neuron in this system as a “model” for other DA neurons in the brain. In this presentation the properties of nigrostriatal DA neurons are compared with those hypothalamic DA neurons that comprise the tuberoinfundibular system. These latter neurons, which have cell bodies in the arcuate nucleus and short axons which terminate in the median eminence, function to inhibit the release of prolactin from the anterior pituitary. The activities of the nigrostriatal and tuberoinfundibular DA neurons were estimated biochemically by measuring the rates of synthesis (accumulation of DOPA after the administration of a decarboxylase inhibitor, NSD 1015), turnover (decline of DA after the administration of a tyrosine hydroxylase inhibitor, α-methyltyrosine) and metabolism (concentrations of dihydroxyphenylacetic acid) of DA in regions of the brain that contain the terminals of these neurons (striatum and median eminence, respectively). Tuberoinfundibular DA neurons differ from nigrostriatal DA neurons in that the former neurons: (1) are not directly regulated by DA receptor-mediated mechanisms, (2) are stimulated by prolactin, (3) exhibit a sexual difference with activity being 2–3 times greater in females and (4) are inhibited by afferent neuronal circuits that are activated by suckling and restraint stress.

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Dopamine is present in all vertebrates and the functional roles of the subsystems are assumed to be similar. Whereas the effect of dopaminergic modulation is well investigated in different target systems, less is known about the factors that are causing the modulation of dopaminergic cells. Using the zebra mbuna, Pseudotropheus zebra, a cichlid fish from Lake Malawi as a model system, we investigated the activation of specific dopaminergic cell populations detected by double-labeling with TH and pS6 antibodies while the animals were solving different learning tasks. Specifically, we compared an intense avoidance learning situation, an instrumental learning task, and a non-learning isolated group and found strong activation of different dopaminergic cell populations. Preoptic-hypothalamic cell populations respond to the stress component in the avoidance task, and the forced movement/locomotion may be responsible for activation in the posterior tubercle. The instrumental learning task had little stress component, but the activation of the raphe superior in this group may be correlated with attention or arousal during the training sessions. At the same time, the weaker activation of the nucleus of the posterior commissure may be related to positive reward acting onto tectal circuits. Finally, we examined the co-activation patterns across all dopaminergic cell populations and recovered robust differences across experimental groups, largely driven by hypothalamic, posterior tubercle, and brain stem regions possibly encoding the valence and salience associated with stressful stimuli. Taken together, our results offer some insights into the different functions of the dopaminergic cell populations in the brain of a non-mammalian vertebrate in correlation with different behavioral conditions, extending our knowledge for a more comprehensive view of the mechanisms of dopaminergic modulation in vertebrates.
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Thus, PRLR-L DRG expression inhibits the effects of high levels of circulating PRL signaling at PRLR-S and limits spinal glutamate/NMDA signaling, preventing nociceptor sensitization and pain transmission in females. Physical and psychological stress, surgical trauma, and chronic inflammation can profoundly trigger systemic PRL release through activation of the hypothalamic–pituitary–adrenal (HPA) axis [54–58]. Stress may promote PRL release through disinhibition of pituitary lactotrophs, resulting from the inhibitory actions of endogenous opioids on TIDA cells [58,59].
Women experience many pain conditions more frequently when compared with men, but the biological mechanisms underlying sex differences in pain remain poorly understood. In particular, little is known about possible sex differences in peripheral nociceptors, the fundamental building blocks of pain transmission. Emerging evidence reveals that prolactin (PRL) signaling at its cognate prolactin receptor (PRLR) in primary afferents promotes nociceptor sensitization and pain in a female-selective fashion. In this review, we summarize recent progress in understanding the female-selective role of PRL/PRLR in nociceptor sensitization and in pathological pain conditions, including postoperative, inflammatory, neuropathic, and migraine pain, as well as opioid-induced hyperalgesia. The clinical implications of the peripheral PRL/PRLR system for the discovery of new therapies for pain control in women are also discussed.
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Overtraining syndrome (OTS) leads to worsened sports performance and fatigue. The pathophysiology of OTS has not been entirely elucidated, and there is a lack of accurate markers for its diagnosis. Changes in hormonal responses implicated in OTS were stimulated by exercise, which has limited their interpretation. Hence, we aimed to evaluate growth hormone (GH) and prolactin responses to a gold-standard and exercise-independent stimulation test, the insulin tolerance test (ITT).
Volunteers were recruited and divided into OTS-affected athletes (OTS), healthy athletes (ATL), and healthy non-active subjects (NCS) groups, after general and specific inclusion and exclusion criteria.
We evaluated the responses of growth hormone (GH) and prolactin to the ITT, and compared between groups.
A total of 51 subjects were included (OTS, n = 14, ATL, n = 25, and NCS, n = 12). OTS disclosed significantly lower basal levels of GH (p = 0.003) and prolactin (p = 0.048), and GH (p = 0.001) and prolactin (p < 0.001) responses to ITT (p = 0.001), compared to ATL, but similar to NCS. OTS showed a later rise in GH levels in response to hypoglycemia, compared to ATL, but not to NCS. We suggest cutoffs for GH and prolactin levels to aid in the diagnosis of OTS.
OTS-affected athletes show reduced GH and prolactin basal levels and responses to a non-exercise stress test compared to healthy athletes, but not to sedentary subjects.
Changes in the female arcuate nucleus morphology and neurochemistry after chronic ethanol consumption and long-term withdrawal
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This nucleus is one of the main central modulators of food intake (Bouret et al., 2004; Morton et al., 2006) and shares connections with other nuclei involved in the control of feeding behavior and ethanol consumption (Thiele et al., 2003; Valassi et al., 2008; Volkow et al., 2011). Moreover, ARN neurons release dopamine (Moore et al., 1987) and express dopamine receptors (Kim et al., 2010; Romero-Fernandez et al., 2014), whose activation decreases food intake and body weight (Guo et al., 2014; van de Giessen et al., 2014; Volkow et al., 2011). Estradiol is the most relevant hormone affecting feeding behavior and body weight both in women (Racine et al., 2012) and female rats (Butera, 2010).
Ethanol is a macronutrient whose intake is a form of ingestive behavior, sharing physiological mechanisms with food intake. Chronic ethanol consumption is detrimental to the brain, inducing gender-dependent neuronal damage. The hypothalamic arcuate nucleus (ARN) is a modulator of food intake that expresses feeding-regulatory neuropeptides, such as alpha melanocyte-stimulating hormone (α-MSH) and neuropeptide Y (NPY). Despite its involvement in pathways associated with eating disorders and ethanol abuse, the impact of ethanol consumption and withdrawal in the ARN structure and neurochemistry in females is unknown. We used female rat models of 20% ethanol consumption for six months and of subsequent ethanol withdrawal for two months. Food intake and body weights were measured. ARN morphology was stereologically analyzed to estimate its volume, total number of neurons and total number of neurons expressing NPY, α-MSH, tyrosine hydroxylase (TH) and estrogen receptor alpha (ERα). Ethanol decreased energy intake and body weights. However, it did not change the ARN morphology or the expression of NPY, α-MSH and TH, while increasing ERα expression. Withdrawal induced a significant volume and neuron loss that was accompanied by an increase in NPY expression without affecting α-MSH and TH expression. These findings indicate that the female ARN is more vulnerable to withdrawal than to excess alcohol. The data also support the hypothesis that the same pathways that regulate the expression of NPY and α-MSH in long-term ethanol intake may regulate food intake. The present model of long-term ethanol intake and withdrawal induces new physiological conditions with adaptive responses.
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Citation Excerpt :
Studies of the regulation of TIDA cells have primarily involved measuring dopamine turnover in the median eminence or pituitary and the underlying transcriptional and enzymatic mechanisms. Analysis of dopamine metabolites was highly successful in revealing the dynamic changes of TIDA activity in various physiological and pathological states but these investigations were limited in that they often required the pharmacological inhibition of dopamine-synthesizing enzymes (see Moore et al., 1987). This manipulation removes the TIDA-mediated brake on prolactin secretion, leading to a hyperprolactinaemia that complicates interpretation of the results.
Neuroendocrine tuberoinfundibular dopamine (TIDA) neurons tonically inhibit pituitary release of the hormone, prolactin. Through the powerful actions of prolactin in promoting lactation and maternal behaviour while suppressing sexual drive and fertility, TIDA neurons play a key role in reproduction. We summarize insights from recent in vitro studies into the membrane properties and network behaviour of TIDA neurons including the observations that TIDA neurons exhibit a robust oscillation that is synchronized between cells and depends on intact gap junction communication. Comparisons are made with phasic firing patterns in other neuronal populations. Modulators involved in the control of lactation – including serotonin, thyrotropin-releasing hormone and prolactin itself – have been shown to change the electrical behaviour of TIDA cells. We propose that TIDA discharge mode may play a central role in tuning the amount of dopamine delivered to the pituitary and hence circulating prolactin concentrations in different reproductive states and pathological conditions.

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Stress, prolactin and hypothalamic dopaminergic neurons

Abstract

Brain Res.

Brain Res.

Eur. J. Pharmac.

Neurosci. Lett.

The effects of stress and nembutal on plasma levels of gonadotropins and prolactin in ovariectomized rats

Endocrinology

Prolactin in CSF selectively increases dopamine turnover in the median eminence

Life Sci.

Dopamine in hypophysial portal blood of the rat during the estrous cycle and throughout pregnancy

Endocrinology

Dopaminergic neurons: Effect of antipsychotic drugs and amphetamine on single cell activity

J. Pharmac. exp. Ther.

Evidence for the existence of monoamine-containing neurons in the central nervous system

Acta physiol. scand.

Biochemical indices of tuberoinfundibular dopaminergic neuronal activity during lactation: A lack of response to prolactin

Neuroendocrinology

Comparison of dopamine synthesis regulation in terminals of nigrostriatal, mesolimbic, tuberoinfundibular and tuberohypophysial neurons

J. Neural Trans.

Accumulation of l-dopa in the median eminence: An index of tuberoinfundibular dopaminergic nerve activity

Endocrinology

Sexual differences in the sensitivity of tuberoinfundibular dopamine neurons to the actions of prolactin

Neuroendocrinology