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 NTS, pyriform cortex and other olfactory processing areas, and mesolimbic reward areas including the VTA and SN.
“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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“Hypothalamic arcuate nuclei projections to the brainstem signal to vagal hepatic efferents (Schwartz et al., 2000; Grill et al., 2002) to regulate blood glucose levels (Lam et al., 2005) and insulin signaling (Pocai et al., 2005).”
BackgroundBrain regulation of food intake and appetite: molecules and networks
Broberger, C. (2005) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2005.01553.x · Cited by 267 · see citing works
Energy Homeostasis, Obesity and Eating Disorders: Recent Advances in Endocrinology
Gale, S. M., Castracane, V. D., & Mantzoros, C. S. (2004) · Journal of Nutrition · doi:10.1093/jn/134.2.295 · Cited by 263 · see citing works
Stengel, A., Goebel, M., Wang, L., Rivier, J., Kobelt, P., Mönnikes, H., Lambrecht, N. W. G., & Taché, Y. (2009) · Endocrinology · doi:10.1210/en.2009-0578 · Cited by 262 · see citing works
“Implanting cannulas into the right lateral (icv) or 4v and ic injections in 5 l were performed as previously described (23, 24).”
MethodEllacott, K. L. J. (2004) · Recent Progress in Hormone Research · doi:10.1210/rp.59.1.395 · Cited by 262 · see citing works
“These neurons have been shown to be able to mediate the inhibitory effects of leptin on food intake and body weight gain following fourth ventricle administration (Grill et al., 2002).”
BackgroundMind versus metabolism in the control of food intake and energy balance
Berthoud, H. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.04.034 · Cited by 259 · see citing works
“Leptin receptors are also expressed in various telencephalic structures, such as hippocampus and neocortex [36], the nucleus accumbens and ventral tegmental area [31], thalamus [28] in the caudal brainstem [42], in primary vagal afferent neurons [9], and even in taste receptor cells [53].”
BackgroundLeptin action in the forebrain regulates the hindbrain response to satiety signals
Morton, G. J., Blevins, J. E., Williams, D. L., Niswender, K. D., Gelling, R. W., Rhodes, C. J., Baskin, D. G., & Schwartz, M. W. (2005) · Journal of Clinical Investigation · doi:10.1172/jci22081 · Cited by 253 · see citing works
Self-citationKievit, P., Howard, J. K., Badman, M. K., Balthasar, N., Coppari, R., Mori, H., Lee, C. E., Elmquist, J. K., Yoshimura, A., & Flier, J. S. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.06.010 · Cited by 242 · see citing works
Leptin receptor signaling and the regulation of mammalian physiology
Villanueva, E. C., & Myers, M. G. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.232 · Cited by 231 · see citing works
Hayes, M. R., Bradley, L. E., & Grill, H. J. (2009) · Endocrinology · doi:10.1210/en.2008-1479 · Cited by 228 · see citing works
Self-citationMonitoring of stored and available fuel by the CNS: implications for obesity
Seeley, R. J., & Woods, S. C. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1245 · Cited by 228 · see citing works
“It might be assumed that these populations reside entirely within the hypothalamus, although leptin and insulin receptors, as well as glucose responsive neurons, are also found within the caudal brainste”
BackgroundObesity and dementia: Adipokines interact with the brain
Arnoldussen, I. A. C., Kiliaan, A. J., & Gustafson, D. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.03.002 · Cited by 219 · see citing works
“…of leptin receptors in specific regions of the brain illustrates its potential for being involved in multiple mechanisms related to brain function and structure in many rodent models (Banks, 2006; Banks et al., 2000; Grill et al., 2002; Guan et al., 1997; Huang et al., 1996; Shioda et al., 1998).”
BackgroundAdiposity signals and food reward: expanding the CNS roles of insulin and leptin
Figlewicz, D. P. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00602.2002 · Cited by 221 · see citing works
“85), and leptin receptors (54) and leptin enhancement of neural activation (39) have been observed in the brain stem.”
BackgroundStefater, M. A., Pérez–Tilve, D., Chambers, A. P., Wilson, H., Sandoval, D. A., Berger, J., Toure, M. H., Tschöp, M. H., Woods, S. C., & Seeley, R. J. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.02.059 · Cited by 222 · see citing works
Brain-derived neurotrophic factor (BDNF) and food intake regulation: A minireview
Lebrun, B., Bariohay, B., Moyse, E., & Jean, A. (2006) · Autonomic Neuroscience · doi:10.1016/j.autneu.2006.02.027 · Cited by 219 · see citing works
“Conversely, leptin, the archetype of long-term food intake regulator, also acts directly within the DVC (Grill et al., 2002; Hosoi et al., 2002).”
BackgroundLeptin signaling in brain: A link between nutrition and cognition?
Morrison, C. D. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.12.004 · Cited by 218 · see citing works
“The NTS is classically associated with satiety and meal termination, and local injections of leptin into the brainstem produce reductions in food intake that are similar in magnitude to injections into the forebrain [41,42].”
BackgroundInsulin, leptin, and food reward: update 2008
Figlewicz, D. P., & Benoit, S. C. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90725.2008 · Cited by 202 · see citing works
“Other CNS sites and neural systems are targets for insulin and leptin action (73, 81, 86, 126).”
BackgroundAppleyard, S. M., Bailey, T. W., Doyle, M. W., Jin, Y., Smart, J. L., Low, M. J., & Andresen, M. C. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4177-04.2005 · Cited by 195 · see citing works
“Actions in the brainstem are also important for the effects of many other regulators of energy homeostasis, and future studies will need to address whether these factors also regulate NTS POMC neurons (Grill and Kaplan, 2002; Grill et al., 2002, 2004; Faulconbridge et al., 2003).”
BackgroundThe regulation of food intake by the gut-brain axis: implications for obesity
Hussain, S., & Bloom, S. R. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.93 · Cited by 195 · see citing works
Distributed Neural Control of Energy Balance: Contributions from Hindbrain and Hypothalamus
Grill, H. J. (2006) · Obesity · doi:10.1038/oby.2006.312 · Cited by 192 · see citing works
“Leptin receptors, however, are also found on NTS neurons (19,20), and low-dose leptin injected directly into this region reduced short- and longer-term food intake (19).”
BackgroundSelf-citationScott, M. M., Williams, K. W., Rossi, J., Lee, C. E., & Elmquist, J. K. (2011) · Journal of Clinical Investigation · doi:10.1172/jci43703 · Cited by 191 · see citing works
Ontogeny of the hypothalamic neuropeptide Y system
Grove, K. L., & Smith, M. S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00104-5 · Cited by 190 · see citing works
Brain regulation of food intake and appetite: molecules and networks
Roberger, C. B. (2005) · Cited by 191 · see citing works
Signalling from the periphery to the brain that regulates energy homeostasis
Kim, K., Seeley, R. J., & Sandoval, D. A. (2018) · Nature reviews. Neuroscience · doi:10.1038/nrn.2018.8 · Cited by 181 · see citing works
Harrold, J. A., Dovey, T. M., Blundell, J. E., & Halford, J. C. G. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.01.007 · Cited by 177 · see citing works
“, 2005); (2) through leptin receptors on neurones in the brain stem (Grill et al., 2002); or (3) through peripheral leptin receptors on vagal afferents (Peters et al.”
Minireview: CNS Mechanisms of Leptin Action
Flak, J. N., & Myers, M. G. (2015) · Molecular Endocrinology · doi:10.1210/me.2015-1232 · Cited by 175 · see citing works
Role of the glucagon-like-peptide-1 receptor in the control of energy balance
Hayes, M. R., De Jonghe, B. C., & Kanoski, S. E. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.02.029 · Cited by 173 · see citing works
Oxytocin innervation of caudal brainstem nuclei activated by cholecystokinin
Blevins, J. E., Eakin, T. J., Murphy, J. A., Schwartz, M. W., & Baskin, D. G. (2003) · Brain Research · doi:10.1016/j.brainres.2003.08.036 · Cited by 164 · see citing works
Self-citationGerman, J., Kim, F., Schwartz, G. J., Havel, P. J., Rhodes, C. J., Schwartz, M. W., & Morton, G. J. (2009) · Endocrinology · doi:10.1210/en.2009-0445 · Cited by 164 · see citing works
“areas as well as extrahypothalamic sites (29, 41, 42), and”
BackgroundSelf-citationSelective leptin resistance revisited
Mark, A. L. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00180.2013 · Cited by 162 · see citing works
“Given the initial evidence for the hypothalamic arcuate nucleus as the linchpin of leptin action, the rapid emergence of evidence for a distributed brain network of leptin action has been staggering (44, 57, 103, 134).”
Brain-Derived Neurotrophic Factor Plays a Role as an Anorexigenic Factor in the Dorsal Vagal Complex
Bariohay, B., Lebrun, B., Moyse, E., & Jean, A. (2005) · Endocrinology · doi:10.1210/en.2005-0419 · Cited by 162 · see citing works
“The DVC is indeed a direct target site for leptin (6, 7).”
BackgroundThe Paraventricular Nucleus of the Hypothalamus: Development, Function, and Human Diseases
Qin, C., Li, J., & Tang, K. (2018) · Endocrinology · doi:10.1210/en.2018-00453 · Cited by 164 · see citing works
Hippocampal Leptin Signaling Reduces Food Intake and Modulates Food-Related Memory Processing
Kanoski, S. E., Hayes, M. R., Greenwald, H. S., Fortin, S. M., Gianessi, C. A., Gilbert, J. R., & Grill, H. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.70 · Cited by 159 · see citing works
“The importance of leptin signaling in the hypothalamus (Balthasar et al, 2004; Dhillon et al, 2006; Leinninger et al, 2009) and the caudal brainstem (Grill et al, 2002; Huo et al, 2007; Hayes et al, 2010) is established for the homeostatic or need-based control of food intake.”
BackgroundSelf-citationMorton, G. J., Niswender, K. D., Rhodes, C. J., Myers, M. G., Blevins, J. E., Baskin, D. G., & Schwartz, M. W. (2003) · Endocrinology · doi:10.1210/en.2002-0115 · Cited by 158 · see citing works
“leptin action in other brain areas in the control of energy homeostasis can be inferred (41, 42).”
BackgroundSelf-citationPrior, L. J., Eikelis, N., Armitage, J. A., Davern, P. J., Burke, S. L., Montani, J.-P., Barzel, B., & Head, G. A. (2010) · Hypertension · doi:10.1161/hypertensionaha.109.141119 · Cited by 157 · see citing works
Early life programming of obesity and metabolic disease
Cottrell, E. C., & Ozanne, S. E. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.11.017 · Cited by 155 · see citing works
Neuronal control of energy homeostasis
Gao, Q., & Horváth, T. L. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.11.063 · Cited by 153 · see citing works
Molecular mapping of mouse brain regions innervated by leptin receptor-expressing cells
Patterson, C. M., Leshan, R. L., Jones, J. C., & Myers, M. G. (2011) · Brain Research · doi:10.1016/j.brainres.2011.01.010 · Cited by 150 · see citing works
“…LepRb neurons, including elsewhere in the hypothalamus, including the lateral hypothalamic area (LHA), as well as in the midbrain and brainstem (Grill et al., 2002; Hayes et al., 2010; Hommel et al., 2006; Leinninger et al., 2009; Leinninger and Myers, 2008; Leshan et al., 2009; Leshan et al.,…”
BackgroundDistribution of leptin‐sensitive cells in the postnatal and adult mouse brain
Caron, É., Sachot, C., Prévot, V., & Bouret, S. G. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22219 · Cited by 147 · see citing works
“Single-label in situ hybridization was performed as previously reported by our laboratories (Gu et al., 1999; Bouret et al., 2004a).”
MethodBrainstem Nutrient Sensing in the Nucleus of the Solitary Tract Inhibits Feeding
Blouet, C., & Schwartz, G. J. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.10.003 · Cited by 145 · see citing works
“…establishing the role of direct NTS leptin, GLP-1 and ghrelin sensing in the homeostatic regulation of food intake (Faulconbridge et al., 2003; Grill et al., 2002; Hayes et al., 2009; Hayes et al., 2011b), these data support a role for the cmNTS as an important metabolicsensing niche in the…”
BackgroundInfluentialCentral Nervous System Regulation of Food Intake
Schwartz, M. W. (2006) · Obesity · doi:10.1038/oby.2006.275 · Cited by 146 · see citing works
“The response to input from satiety-related signals is, therefore, hypothesized to be regulated by input from adiposity-related signals, but whether this effect involves hypothalamic input from adiposity signals or a direct action of leptin in the hindbrain (62) awaits further study.”
BackgroundSelf-citationDevelopment of Leptin‐Sensitive Circuits
Bouret, S. G., & Simerly, R. B. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01563.x · Cited by 143 · see citing works
THE CRITICAL ROLE OF THE MELANOCORTIN SYSTEM IN THE CONTROL OF ENERGY BALANCE
Seeley, R. J., Drazen, D. L., & Clegg, D. J. (2004) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.24.012003.132428 · Cited by 141 · see citing works
Huo, L., Maeng, L. Y., Bjørbæk, C., & Grill, H. J. (2007) · Endocrinology · doi:10.1210/en.2006-1572 · Cited by 142 · see citing works
“The icv administration or microinjection of leptin directly into the NTS (at the level of the AP) is sufficient to reduce short-term food intake and body weight gain (29).”
BackgroundSelf-citationModulation of vagal afferent excitation and reduction of food intake by leptin and cholecystokinin
Peters, J. H., Simasko, S. M., & Ritter, R. C. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.06.017 · Cited by 142 · see citing works
Leptin Signaling in the Nucleus Tractus Solitarii Increases Sympathetic Nerve Activity to the Kidney
Mark, A. L., Agassandian, K., Morgan, D. A., Liu, X., Cassell, M. D., & Rahmouni, K. (2009) · Hypertension · doi:10.1161/hypertensionaha.108.124255 · Cited by 139 · see citing works
“Discussion The major new findings from this study are as follows: (1) leptin receptor signaling in the NTS increases SNA to kidney but not to BAT; (2) sympathoactivation to microinjection of leptin into the NTS was associated with an increase in arterial pressure; and (3) the renal sympathetic nerve responses to NTS l…”
BackgroundLeptin and the systems neuroscience of meal size control
Grill, H. J. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.10.005 · Cited by 137 · see citing works
Self-citationCharacterization of Leptin-Responsive Neurons in the Caudal Brainstem
Ellacott, K. L. J., Halatchev, I. G., & Cone, R. D. (2006) · Endocrinology · doi:10.1210/en.2005-0877 · Cited by 133 · see citing works
“Leptin receptors are found in the caudal brainstem of rodents (22, 23), and administration of leptin into the fourth ventricle causes a reduction in nocturnal food intake comparable with lateral ventricular administration (23).”
BackgroundHuo, L., Grill, H. J., & Bjørbæk, C. (2006) · Diabetes · doi:10.2337/diabetes.55.03.06.db05-1143 · Cited by 128 · see citing works
“We have previously shown the presence of leptin receptor mRNA and leptin-inducible STAT3 tyrosine phosphorylation in the NTS of rats (12,21).”
Self-citationLeptin: a diverse regulator of neuronal function
Harvey, J. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04205.x · Cited by 123 · see citing works
Padilla, S. L., Reef, D. K., & Zeltser, L. M. (2011) · Endocrinology · doi:10.1210/en.2011-1665 · Cited by 120 · see citing works
Schwartz, G. J., & Moran, T. H. (2002) · Endocrinology · doi:10.1210/en.2002-220352 · Cited by 120 · see citing works
“The NTS contains leptin receptors (17, 31), and fourth ventricular or direct NTS leptin administration has been demonstrated to inhibit food intake (31).”
BackgroundLeptin reverses declines in satiation in weight-reduced obese humans
Kissileff, H. R., Thornton, J. C., Torres, M., Pavlovich, K. H., Mayer, L. S., Kalari, V., Leibel, R. L., & ROSENBAUM, M. S. (2012) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.012385 · Cited by 118 · see citing works
“In addition to being hypometabolic (16, 19–23), leptindeficient humans and rodents are also hyperphagic and demonstrate reduced satiation and, to a lesser degree, increased hunger, thereby creating the optimal biological conditions that promote weight gain in leptin-deficient states (24).”
BackgroundQuan, W., Kim, H.-K., Moon, E., Kim, S. S., Choi, C. S., Komatsu, M., Jeong, Y. T., Lee, M., Kim, K.-W., Kim, M.-S., et al. (2012) · Endocrinology · doi:10.1210/en.2011-1882 · Cited by 116 · see citing works
Role of leptin in the regulation of gonadotropin secretion in farm animals
Barb, C. R., & Kraeling, R. R. (2004) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2004.04.032 · Cited by 113 · see citing works
“Furthermore, evidence now exists that the brain stem is a direct target for leptin in the regulation of food intake and neuroendocrine function (Grill et al., 2002; Hosoi et al., 2002).”
BackgroundEnergy regulatory signals and food reward
Figlewicz, D. P., & Sipols, A. J. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.03.002 · Cited by 111 · see citing works
“Other CNS sites and neural systems are targets for insulin and leptin action (Figlewicz et al., 1990; Figlewicz, 2003; Grill et al., 2002; Harvey, 2007; McNay, 2007).”
BackgroundDioxins, the aryl hydrocarbon receptor and the central regulation of energy balance
Lindén, J., Lensu, S., Tuomisto, J., & Pohjanvirta, R. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.07.002 · Cited by 107 · see citing works
“Intracerebroventricular administration of exogenous leptin or insulin induces marked reductions in food intake and body weight [153,163,223,396].”
The blood-brain barrier: connecting the gut and the brain
Banks, W. A. (2008) · Regulatory Peptides · doi:10.1016/j.regpep.2007.08.027 · Cited by 104 · see citing works
Williams, D. L., Bowers, R. R., Bartness, T. J., Kaplan, J. M., & Grill, H. J. (2003) · Endocrinology · doi:10.1210/en.2003-0440 · Cited by 104 · see citing works
Self-citationFrom observation to experimentation: leptin action in the mediobasal hypothalamus
Williams, K. W., Scott, M. M., & Elmquist, J. K. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26788d · Cited by 103 · see citing works
“In addition, fourth ventricle administration of leptin reduces food ingestion and weight gain within 24 h, and these effects are mimicked by microinjection of the peptide into either the fourth ventricle or the NTS (58).”
BackgroundInfluentialExpression of leptin receptor gene in developing and adult zebrafish
Liu, Q., Chen, Y., Copeland, D. L., Ball, H. C., Duff, R. J., Rockich, B. E., & Londraville, R. L. (2009) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2009.11.015 · Cited by 102 · see citing works
“…especially the dorsal vagal complex, contains leptin receptor mRNA and protein (Elmquist et al., 1998; Mercer et al., 1998; Buyse et al., 2001; Grill et al., 2002), and is thought to play crucial roles in integration of leptin signals and meal-related satiety signals (Grill and Kaplan, 2002;…”
BackgroundPsychological and Neurobiological Correlates of Food Addiction
Kalon, E., Hong, J., Tobin, C. T., & Schulte, T. (2016) · International review of neurobiology · doi:10.1016/bs.irn.2016.06.003 · Cited by 101 · see citing works
Distribution of insulin receptor substrate-2 in brain areas involved in energy homeostasis
Pardini, A. W., Hồng, N. T., Figlewicz, D. P., Baskin, D. G., Williams, D. L., Kim, F., & Schwartz, M. W. (2006) · Brain Research · doi:10.1016/j.brainres.2006.06.109 · Cited by 101 · see citing works
Self-citationLeptin-induced satiation mediated by abdominal vagal afferents
Peters, J. H., McKay, B. M., Simasko, S. M., & Ritter, R. C. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00716.2004 · Cited by 100 · see citing works
“It is well established that systemic administration of milligram doses of leptin (8) or injection of microgram amounts of leptin into the forebrain (15, 22) or hindbrain (7) ventricles reduces 24-h food intake and decreases meal size.”
Background
- 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 › Epidemiology › 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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