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Evidence That the Caudal Brainstem Is a Target for the Inhibitory Effect of Leptin on Food Intake
Abstract
Three experiments were performed to investigate the hypothesis that leptin action within the caudal brain stem (CBS) contributes to its intake inhibitory effects. The first experiment evaluated the anatomical distribution of leptin receptor mRNA in rat CBS using a sensitive fluorescence in situ hybridization method with a riboprobe specific for the long form of the leptin receptor (Ob-Rb). An Ob-Rb mRNA hybridization signal was detected in neurons of several CBS nuclei involved in the control of food intake, including the dorsal vagal complex and parabrachial nucleus. A strong hybridization signal was also obtained from neuronal cell bodies of a number of other structures including the hypoglossal, trigeminal, lateral reticular, and cochlear nuclei; locus ceruleus; and inferior olive. The anatomical profile revealed by fluorescence in situ hybridization was in good agreement with immunocytochemical analysis with an antibody specific to Ob-Rb. In a second experiment, exploring the relevance of CBS Ob-Rb to feeding behavior, rats were given a fourth intracerebroventricular (i.c.v.) injection of leptin (0.1, 0.83, or 5.0μ g; n = 9–11/group) or vehicle 30 min before lights-out on three consecutive days The two higher doses reduced food intake significantly at 2, 4, and 24 h after injection and caused significant reductions of body weight. The dose-response profiles for fourth i.c.v. administration were indistinguishable from those obtained from separate groups of rats that received leptin via a lateral i.c.v. cannula. In the last experiment, a ventricle-subthreshold dose of leptin (0.1 μg) microinjected unilaterally into the dorsal vagal complex suppressed food intake at 2, 4, and 24 h. The results indicate that the CBS contains neurons that are potentially direct targets for the action of leptin in the control of energy homeostasis.
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“functional leptin receptors are expressed in the hippocampus, hindbrain (including the nucleus of the solitary tract (NTS)), pyriform cortex and other olfactory processing areas, and in mesolimbic areas involved in reward including the ventral tegmental area (VTA) and substantia nigra (SN) (61, 72).”
From Leptin and the Central Nervous System Control of Glucose Metabolism (2011) · cites this paper as [72]
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Integrative capacity of the caudal brainstem in the control of food intake
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“Rats that were to receive fourth ventricular infusions were implanted with a stainless steel 24-gauge guide cannula secured 2 mm above the target site (AP: average of 11.6 mm from bregma and + 2.5 mm from the occipital crest, ML: 0.0 mm (midline), DV: 4.5 mm from dura; Grill et al, 2002).”
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“Interestingly, these latter neurons are also responsive to gastric distention in rats,(24) and intraparenchymal NTS administration of leptin acutely reduces food intake and body weight.(33) These latter data combined suggest that the effects of leptin on food intake in the hindbrain may result from modulation of gastr…”
BackgroundThe effects of high fat diets on the blood–brain barrier transport of leptin: Failure or adaptation?
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TRAP-seq defines markers for novel populations of hypothalamic and brainstem LepRb neurons
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“caudal brain stem (14) and reward-related brain structures (15).”
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Self-citationMcKinley, M. J., Denton, D. A., Ryan, P. J., Yao, S. T., Stefanidis, A., & Oldfield, B. J. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12689 · Cited by 79
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“Leptin Acts in the lPBN to Alter Food Intake, but Not Body Temperature Leptin receptor is expressed in the PBN of mice and rats (Elmquist et al., 1998; Grill et al., 2002) and phosphorylation of STAT3 can be induced in the lPBN by peripheral leptin administration (Hosoi et al.”
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“Leptin receptors are present in the NTS and leptin-responsive neurons exist in this region (Elias et al., 2000; Grill et al., 2002; Hosoi et al., 2002).”
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Self-citationRapid Inhibition of Neurons in the Dorsal Motor Nucleus of the Vagus by Leptin
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Leptin, An Adipokine With Central Importance in the Global Obesity Problem
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BackgroundNeurobiology Driving Hyperactivity in Activity-Based Anorexia
Adan, R. A. H., Hillebrand, J. J., Danner, U. N., Cano, S. C., Kas, M. J., & Verhagen, L. A. W. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_77 · Cited by 75
Leptin Impairs Cardiovagal Baroreflex Function at the Level of the Solitary Tract Nucleus
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“Studies also support the role of NTS vagus afferent in response to leptin [60,61].”
ResultFeeding circuit development and early-life influences on future feeding behaviour
Zeltser, L. M. (2018) · Nature reviews. Neuroscience · doi:10.1038/nrn.2018.23 · Cited by 74
Obesity-associated mutations in the human melanocortin-4 receptor gene
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The subfornical organ: a central nervous system site for actions of circulating leptin
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“These findings were not completely unexpected, as previous studies have shown that OB-Rb is expressed in both neurons (8, 17, 32) and primary glial cell cultures (22).”
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“For example, administration of leptin in the fourth ventricle or directly in the DVC, area postrema, and dorsal motor nucleus inhibits food intake (115).”
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Bartness, T. J., Keen‐Rhinehart, E., Dailey, M. J., & Teubner, B. J. W. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00137.2011 · Cited by 64
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“described above and by Grill et al. (2002) ] were adapted to handling and tospendingseveralhoursinthemetabolicchamberbeforethebeginning of the experimental sequence.”
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Modulation of the satiating effect of amylin by central ghrelin, leptin and insulin
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“…and rewarding aspects of food intake, as well as in extra-ARC hypothalamic nuclei (Leinninger et al, 2009; Zhang et al, 2011) and hindbrain nuclei (Grill et al, 2002b; Huo et al, 2007; Schwartz and Moran, 2002; Skibicka and Grill, 2009) whose neural processing is typically associated with the…”
BackgroundSelf-citationThe influence of leptin on the dopamine system and implications for ingestive behavior
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“parameters (11), whereas via peripheral application, doses of”
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The role of leptin-->STAT3 signaling in neuroendocrine function: an integrative perspective
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“…action on brainstem LRb-expressing neurones as well as indirect leptin action via ARC LRb neurones that project to the brainstem may contribute to the satiety effects of leptin (Elmquist et al. 1998a, Grill et al. 2002, Ellacott et al. 2006a,b, Grill 2006, Leshan et al. 2006, Huo et al. 2007).”
BackgroundErichsen, J. M., Fadel, J. R., & Reagan, L. P. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108877 · Cited by 58
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BackgroundHindbrain leptin receptor stimulation enhances the anorexic response to cholecystokinin
Williams, D. L., Baskin, D. G., & Schwartz, M. W. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00182.2009 · Cited by 52
Self-citationPeptide signals regulating food intake and energy homeostasis
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Self-citationMarty, V. N., Hachmane, M. F. E., & Amédée, T. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06296.x · Cited by 56
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BackgroundFaulconbridge, L. F., Grill, H. J., & Kaplan, J. M. (2005) · Diabetes · doi:10.2337/diabetes.54.7.1985 · Cited by 50
“, leptin [47]) or peptide mediator (e.”
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BackgroundThe melanocortin system as a central integrator of direct and indirect controls of food intake
Williams, D. L., & Schwartz, M. W. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00226.2005 · Cited by 50
“Although leptin and insulin receptors are present in the NTS (11, 14, 22), and while intra-DVC leptin treatment effectively reduces food intake (11), additional studies are required to determine whether NTS POMC cells respond directly to these hormones and thus serve as a central mediator of indirect controls of meal…”
BackgroundSelf-citationGenetic Dissection of Neuronal Pathways Controlling Energy Homeostasis
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BackgroundOverview of the Physiological Control of Eating
Langhans, W., & Geary, N. (2009) · Forum of nutrition/Bibliotheca Nutritio et dieta · doi:10.1159/000264392 · Cited by 49
Amylin and Leptin: Co-Regulators of Energy Homeostasis and Neuronal Development
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Leptin signaling and leptin resistance
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“Leptin receptors are expressed in vagal afferent nerves and a population of NTS neurons, and leptin signaling within the NTS contributes to the reduction of food intake and body weight [52, 53].”
BackgroundAkieda‐Asai, S., Poleni, P.-E., & Date, Y. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00664.2013 · Cited by 48
“Indeed, previous studies have shown that the potentiating effect of leptin on CCK-induced satiety involves local actions of leptin on CCKsensitive neurons within the nodose ganglion and the hindbrain (19, 32).”
BackgroundHypertension in obesity: is leptin the culprit?
Simonds, S. E., & Cowley, M. A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.01.004 · Cited by 50
Plasticity of central autonomic neural circuits in diabetes
Zsombok, A., & Smith, B. N. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.12.001 · Cited by 48
“Synaptic balance is altered in the DVC of hyperglycemic/hypoinsulemic mice [73] .”
InfluentialPhysiological mechanisms for food-hoarding motivation in animals
Keen‐Rhinehart, E., Dailey, M. J., & Bartness, T. J. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0225 · Cited by 47
Bassi, M., Giusti, H., Leite, C. M., Anselmo-Franci, J. A., do Carmo, J. M., da Silva, A. A., Hall, J. E., Colombari, E., & Glass, M. L. (2012) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-012-1111-1 · Cited by 46
“food intake [12, 16], few studies have examined whether this effect is maintained when leptin is administered over several days.”
Leptin, diabetes, and the brain
Morton, G. J., & Meek, T. H. (2012) · Indian Journal of Endocrinology and Metabolism · doi:10.4103/2230-8210.105568 · Cited by 47
“While leptin receptors are expressed in several hypothalamic[49,50] and extrahypothalamic areas[51,52] involved in the control of energy balance and autonomic function, several observations implicate the hypothalamic arcuate nucleus (ARC) as an important site for leptin-mediated effects on glucose metabolism.”
BackgroundBalsevich, G., Sticht, M. A., Bowles, N. P., Singh, A., Lee, T. T.-Y., Li, Z., Chelikani, P. K., Lee, F. S., Borgland, S. L., Hillard, C. J., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1802251115 · Cited by 46
Molecular Targets for Obesity Therapy in the Brain
Obici, S. (2009) · Endocrinology · doi:10.1210/en.2009-0409 · Cited by 45
Alhadeff, A. L., Hayes, M. R., & Grill, H. J. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00329.2014 · Cited by 43
Self-citationLeptin inhibits and ghrelin augments hypothalamic noradrenaline release after stress
Kawakami, A., Kawakami, A., Okada, N., Rokkaku, K., Honda, K., Ishibashi, S., & Onaka, T. (2008) · Stress · doi:10.1080/10253890701820257 · Cited by 43
“Leptin receptors are present in cells of the nucleus of the solitary tract (Elmquist et al. 2000; Mercer et al. 1998; Grill et al. 2002) and some of these cells are catecholaminergic neurones (Hay-Schmidt et al. 2001).”
BackgroundBiology of Eating Behavior in Obesity
Schwartz, G. J. (2004) · Obesity Research · doi:10.1038/oby.2004.274 · Cited by 43
ICV leptin effects on spontaneous physical activity and feeding behavior in rats
Choi, Y., Li, C., Hartzell, D. L., Little, D. E., Della‐Fera, M. A., & Baile, C. A. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.10.024 · Cited by 41
“Little a, Mary Anne Della-Fera a, Clifton A. Baile a,b,∗ a Department of Animal and Dairy Science, University of Georgia, Athens, GA 30602-2771, USA b Department of Food and Nutrition, University of Georgia, Athens, GA 30602-2771, USA c Department of Animal Science and Institute of Agriculture &…”
BackgroundInfluentialAnorectic brainstem peptides: more pieces to the puzzle
Luckman, S. M., & Lawrence, C. B. (2003) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(02)00033-4 · Cited by 45
Bello, N. T., Coughlin, J. W., Redgrave, G. W., Ladenheim, E. E., Moran, T. H., & Guarda, Á. S. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.09.021 · Cited by 40
“Gastrointestinal sensory input is conveyed to the NTS predominately by vagal afferent and afferent responsivity is often measured by gene expression in the soma region or nodose ganglion [58-61].”
BackgroundGustatory and reward brain circuits in the control of food intake
Oliveira-Maia, A. J., Roberts, C. D., Simon, S. A., & Nicolelis, M. A. L. (2010) · Advances and technical standards in neurosurgery · doi:10.1007/978-3-7091-0179-7_3 · Cited by 43
Neuroanatomical determinants of the sympathetic nerve responses evoked by leptin
Harlan, S. M., & Rahmouni, K. (2012) · Clinical Autonomic Research · doi:10.1007/s10286-012-0168-4 · Cited by 39
Food restriction and leptin impact brain reward circuitry in lean and obese Zucker rats
Fulton, S. E., Richard, D., Woodside, B. C., & Shizgal, P. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.05.021 · Cited by 39
Leptin Sensitizes NTS Neurons to Vagal Input by Increasing Postsynaptic NMDA Receptor Currents
Neyens, D. M., Zhao, H., Huston, N. J., Wayman, G. A., Ritter, R. C., & Appleyard, S. M. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1865-19.2020 · Cited by 37
“6), similar to what has been reported previously (Grill et al., 2002).”
BackgroundResultThe Caudal Brainstem and the Control of Food Intake and Energy Balance
Berthoud, H. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-48643-1_9 · Cited by 38
Dallaporta, M., Pecchi, É., Pio, J., Jean, A., Horner, K. C., & Troadec, J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01799.x · Cited by 37
Rupprecht, L. E., Mietlicki‐Baase, E. G., Zimmer, D. J., McGrath, L. E., Olivos, D. R., & Hayes, M. R. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00367.2013 · Cited by 37
Novel mechanisms involved in leptin sensitization in obesity
Pena-León, V., Pérez-Lois, R., Villalón, M. C., Prida, E., Muñoz-Moreno, D., Fernø, J., Quiñones, M., Al–Massadi, O., & Seoane, L. M. (2024) · Biochemical Pharmacology · doi:10.1016/j.bcp.2024.116129 · Cited by 43
Deng, C., Weston–Green, K., Han, M., & Huang, X. (2007) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2007.02.009 · Cited by 35
Jonghe, B. C. D., Hayes, M. R., Zimmer, D. J., Kanoski, S. E., Grill, H. J., & Bence, K. K. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00009.2012 · Cited by 35
Self-citationThe retrotrapezoid nucleus and the neuromodulation of breathing
Moreira, T. S., Sobrinho, C. R., Falquetto, B., Oliveira, L. M., Lima, J. D., Mulkey, D. K., & Takakura, A. C. T. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00497.2020 · Cited by 36
Zorrilla, E. P., Inoue, K., Valdez, G. R., Tabarin, A., & Koob, G. F. (2004) · Psychopharmacology · doi:10.1007/s00213-004-1952-1 · Cited by 35
“For example, perhaps intracerebroventricular leptin administration recruits extra-arcuate regions, such as the caudal hindbrain (Grill et al. 2002), to a greater degree than systemic infusion.”
BackgroundAre microRNAs the Molecular Link Between Metabolic Syndrome and Alzheimer’s Disease?
Codocedo, J. F., Ríos, J. A., Godoy, J. A., & Inestrosa, N. C. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9201-7 · Cited by 34
“the brain illustrates its potential for being involved in multiple mechanisms related to brain function and structure in many rodent models [158–161].”
BackgroundGenetic Variation and Effects on Human Eating Behavior
de Krom, M., Bauer, F., Collier, D. A., Adan, R. A. H., & la Fleur, S. E. (2009) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-080508-141124 · Cited by 34
Facilitation of breathing by leptin effects in the central nervous system
Bassi, M., Furuya, W. I., Zoccal, D. B., Menani, J. V., Colombari, D. S. A., Mulkey, D. K., & Colombari, E. (2015) · The Journal of Physiology · doi:10.1113/jp270308 · Cited by 35
“…receptor-mediated transport system (Morris & Rui, 2009) to enter the central nervous system (CNS) and regulate neural pathways that control appetite (Grill et al. 2002), sympathetic nerve activity (SNA), thermogenesis (Rahmouni & Morgan, 2007; Mark et al. 2009) and potentially ventilatory function…”
Background
Metadata
- Authors
- Grill, H. J., Schwartz, M. W., Kaplan, J. M., Foxhall, J. S., Breininger, J., & Baskin, D. G.
- Affiliations
- University of Pennsylvania (US)
- University of Washington (US)
- Corresponding author
- Grill, Harvey J.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2002-01-01
- Volume
- 143
- Issue
- 1
- Pages
- 239-246
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W1976978438
- Cited by
- 395
- References
- 51
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 8 · 2023: 6 · 2022: 6 · 2021: 8 · 2020: 12 · 2019: 8 · 2018: 14 · 2017: 8 · 2016: 11 · 2015: 11 · 2014: 20 · 2013: 22 · 2012: 28
- FWCI
- 7.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs
- University of Pennsylvania
- University of Washington (DK17047)
- National Institutes of Health (2r01dk012829-36, DK21397)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 12829, R01DK042284, R01DK052989, DK-42284, DK-52989, DK-17047, DK 21397, P30DK017047)
- National Institute of Neurological Disorders and Stroke (NS-32272)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- leptin, caudal brainstem, food intake regulation, dorsal vagal complex, parabrachial nucleus, energy homeostasis, weight loss, hypothalamic-pituitary-thyroid axis
- MeSH terms
- Animals, Brain Stem, Carrier Proteins, Eating, Injections, Intraventricular, Male, Receptors, Cell Surface, Tissue Distribution, Vagus Nerve, Rats, Wistar, Protein Isoforms, Fourth Ventricle, Lateral Ventricles, Leptin, Rats, Receptors, Leptin
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