Stimulation of feeding by three different glucose-sensing mechanisms requires hindbrain catecholamine neurons

Li, Aijun; Wang, Qing; Dinh, Thu; Powers, Bethany; Ritter, Sue

doi:10.1152/ajpregu.00451.2013

Cited by 17 publications

(18 citation statements)

References 44 publications

(73 reference statements)

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“…The lesion of the rostrally projecting catecholamine neurons that innervate the PeFLH impaired the glucoprivic feeding response but did not impair the adrenal medullary blood glucose response. This is consistent with our previous work comparing spinal and hypothalamic DSAP injections (10,35) and with results using various other experimental approaches indicating that spinally projecting catecholamine neurons mediate the adrenal medullary response to glucose deficit (60,61). Orexin neurons also project spinally (62) and recent evidence suggests an independent role for these projections in controlling blood glucose (63).…”

supporting

confidence: 91%

Hindbrain Catecholamine Neurons Activate Orexin Neurons During Systemic Glucoprivation in Male Rats

Wang

Elsarelli

et al. 2015

Endocrinology

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Hindbrain catecholamine neurons are required for elicitation of feeding responses to glucose deficit, but the forebrain circuitry required for these responses is incompletely understood. Here we examined interactions of catecholamine and orexin neurons in eliciting glucoprivic feeding. Orexin neurons, located in the perifornical lateral hypothalamus (PeFLH), are heavily innervated by hindbrain catecholamine neurons, stimulate food intake, and increase arousal and behavioral activation. Orexin neurons may therefore contribute importantly to appetitive responses, such as food seeking, during glucoprivation. Retrograde tracing results showed that nearly all innervation of the PeFLH from the hindbrain originated from catecholamine neurons and some raphe nuclei. Results also suggested that many catecholamine neurons project collaterally to the PeFLH and paraventricular hypothalamic nucleus. Systemic administration of the antiglycolytic agent, 2-deoxy-D-glucose, increased food intake and c-Fos expression in orexin neurons. Both responses were eliminated by a lesion of catecholamine neurons innervating orexin neurons using the retrogradely transported immunotoxin, anti-dopamine-β-hydroxylase saporin, which is specifically internalized by dopamine-β-hydroxylase-expressing catecholamine neurons. Using designer receptors exclusively activated by designer drugs in transgenic rats expressing Cre recombinase under the control of tyrosine hydroxylase promoter, catecholamine neurons in cell groups A1 and C1 of the ventrolateral medulla were activated selectively by peripheral injection of clozapine-N-oxide. Clozapine-N-oxide injection increased food intake and c-Fos expression in PeFLH orexin neurons as well as in paraventricular hypothalamic nucleus neurons. In summary, catecholamine neurons are required for the activation of orexin neurons during glucoprivation. Activation of orexin neurons may contribute to appetitive responses required for glucoprivic feeding.

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supporting

confidence: 91%

Hindbrain Catecholamine Neurons Activate Orexin Neurons During Systemic Glucoprivation in Male Rats

Wang

Elsarelli

et al. 2015

Endocrinology

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“…In mammals, starvation results in an activation of central and sympathetic catecholaminergic neurons, which regulate the release of glucose into the blood and modulate feeding behavior ( Nonogaki, 2000 ; Ritter et al, 2001 , 2011 ; Li et al, 2014 ; Morton et al, 2014 ; Verberne et al, 2014 , 2016 ). Our results indicate that OA plays a role in regulating the honeybees’ energy state and behavior in response to starvation, supporting the hypothesis that OA is the functional homolog of adrenalin and noradrenalin.…”

Section: Discussionmentioning

confidence: 99%

“…During a glucose-deficit sympathetic activity increases hepatic glucose output, stimulates glucagon release from the pancreas, inhibits pancreatic insulin release, and blocks glucose uptake in skeletal muscles (reviewed in Nonogaki, 2000 ; Verberne et al, 2014 , 2016 ; Seoane-Collazo et al, 2015 ; Elliott et al, 2016 ). Furthermore, central noradrenergic neurons are involved in behavioral responses to a glucose deficit ( Ritter et al, 2001 , 2011 ; Li et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

Octopamine Underlies the Counter-Regulatory Response to a Glucose Deficit in Honeybees (Apis mellifera)

Buckemüller

Siehler

Göbel

et al. 2017

Front. Syst. Neurosci.

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An animal’s internal state is a critical parameter required for adaptation to a given environment. An important aspect of an animal’s internal state is the energy state that is adjusted to the needs of an animal by energy homeostasis. Glucose is one essential source of energy, especially for the brain. A shortage of glucose therefore triggers a complex response to restore the animal’s glucose supply. This counter-regulatory response to a glucose deficit includes metabolic responses like the mobilization of glucose from internal glucose stores and behavioral responses like increased foraging and a rapid intake of food. In mammals, the catecholamines adrenalin and noradrenalin take part in mediating these counter-regulatory responses to a glucose deficit. One candidate molecule that might play a role in these processes in insects is octopamine (OA). It is an invertebrate biogenic amine and has been suggested to derive from an ancestral pathway shared with adrenalin and noradrenalin. Thus, it could be hypothesized that OA plays a role in the insect’s counter-regulatory response to a glucose deficit. Here we tested this hypothesis in the honeybee (Apis mellifera), an insect that, as an adult, mainly feeds on carbohydrates and uses these as its main source of energy. We investigated alterations of the hemolymph glucose concentration, survival, and feeding behavior after starvation and examined the impact of OA on these processes in pharmacological experiments. We demonstrate an involvement of OA in these three processes in honeybees and conclude there is an involvement of OA in regulating a bee’s metabolic, physiological, and behavioral response following a phase of prolonged glucose deficit. Thus, OA in honeybees acts similarly to adrenalin and noradrenalin in mammals in regulating an animal’s counter-regulatory response.

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“…It appears that little is known about the relationships among sugars, appetite, and brain responses in humans, although this has been examined in animal models [28,29]. One stakeholder pointed out that the current evidence shows that appetite is mainly driven by brain mechanisms.…”

Section: Stakeholder Discussionmentioning

confidence: 99%

Research needs and prioritizations for studies linking dietary sugars and potentially related health outcomes

et al. 2016

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Background: Relationships among dietary sugars and a variety of chronic diseases have spawned interest in investigating the metabolic effects of dietary sugars. An approach developed by the Agency for Healthcare Research and Quality (AHRQ) for assessing Future Research Needs (FRN) was implemented with modifications that integrated an evidence mapping process. Methods: A panel of 14 stakeholders across 7 pre-defined areas of expertise (lay audience, policy makers, health providers, research funders, evidence-based methodologists, product makers, and researchers) was assembled to prioritize research needs. The panel was facilitated by an independent research team. A total of 213 studies were analyzed descriptively for evidence mapping, and the results were used to inform the stakeholder panel discussions on research needs. Results: The stakeholder panel identified and prioritized 14 sets of research questions. The top three high-priority FRN questions selected by the stakeholder panel focused on the effects of dietary sugars on body weight or body composition, fat deposition, and satiety and appetite. Research considerations for the top three research questions and crosscutting research design issues are discussed. Conclusion: Involving a multidisciplinary stakeholder panel to prioritize the direction of future research in this or other content areas has potential to add diverse perspectives to the determination of research needs, and to the development of public health policy.

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Stimulation of feeding by three different glucose-sensing mechanisms requires hindbrain catecholamine neurons

Cited by 17 publications

References 44 publications

Hindbrain Catecholamine Neurons Activate Orexin Neurons During Systemic Glucoprivation in Male Rats

Hindbrain Catecholamine Neurons Activate Orexin Neurons During Systemic Glucoprivation in Male Rats

Octopamine Underlies the Counter-Regulatory Response to a Glucose Deficit in Honeybees (Apis mellifera)

Research needs and prioritizations for studies linking dietary sugars and potentially related health outcomes

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