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The Journal of Neuroscience, May 27, 2009, 29(21):7015-7022; doi:10.1523/JNEUROSCI.0334-09.2009

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Behavioral/Systems/Cognitive
Relationship among Brain and Blood Glucose Levels and Spontaneous and Glucoprivic Feeding

Ambrose A. Dunn-Meynell,^1,2 Nicole M. Sanders,³ Douglas Compton,⁴ Thomas C. Becker,⁵ Jun-ichi Eiki,⁶ Bei B. Zhang,⁷ and Barry E. Levin^1,2

¹Neurology Service, Department of Veterans Affairs New Jersey Health Care System, East Orange, New Jersey 07018, ²Department of Neurology and Neurosciences, New Jersey Medical School, University of Medicine and Dentistry New Jersey, Newark, New Jersey 07101, ³Metabolism/Endocrinology, Virginia Puget Sound Health Care System, Seattle, Washington 98108, ⁴Research Diets Inc., New Brunswick, New Jersey 08901, ⁵Department of Internal Medicine, The Sarah W. Stedman Nutrition and Metabolism Center, and Division of Endocrinology, Metabolism, and Nutrition, Duke University Medical Center, Durham, North Carolina 27708, ⁶Tsukuba Research Institute, Banyu Pharmaceutical Company Ltd., Tsukuba, Ibaraki 300-2611, Japan, and ⁷Merck Research Laboratories, Rahway, New Jersey 07065

Correspondence should be addressed to Dr. Barry E. Levin, Neurology Service (127C), Veterans Affairs Medical Center, East Orange, NJ 07018-1095. Email: levin{at}umdnj.edu

Although several studies implicate small declines in blood glucose levels as stimulus for spontaneous meal initiation, no mechanism is known for how these dips might initiate feeding. To assess the role of ventromedial hypothalamus (VMH) (arcuate plus ventromedial nucleus) glucosensing neurons as potential mediators of spontaneous and glucoprivic feeding, meal patterns were observed, and blood and VMH microdialysis fluid were sampled in 15 rats every 10 min for 3.5 h after dark onset and 2 h after insulin (5 U/kg, i.v.) infusion. Blood glucose levels declined by 11% beginning 5 min before 65% of all spontaneous meals, with no fall in VMH levels. After insulin, blood and VMH glucose reached nadirs by 30–40 min, and the same rats ate 60% faster and spent 84% more time eating during the ensuing hypoglycemia. Although 83% of first hypoglycemic meals were preceded by 5 min dips in VMH (but not blood) glucose levels, neither blood nor VMH levels declined before second meals, suggesting that low glucose, rather than changing levels, was the stimulus for glucoprivic meals. Furthermore, altering VMH glucosensing by raising or lowering glucokinase (GK) activity failed to affect spontaneous feeding, body or adipose weights, or glucose tolerance. However, chronic depletion by 26–70% of VMH GK mRNA reduced glucoprivic feeding. Thus, although VMH glucosensing does not appear to be involved in either spontaneous feeding or long-term body-weight regulation, it does participate in glucoprivic feeding, similar to its role in the counter-regulatory neurohumoral responses to glucoprivation.

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Received Jan. 21, 2009; revised Feb. 16, 2009; accepted Feb. 24, 2009.

Correspondence should be addressed to Dr. Barry E. Levin, Neurology Service (127C), Veterans Affairs Medical Center, East Orange, NJ 07018-1095. Email: levin{at}umdnj.edu

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