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The Journal of Neuroscience, March 11, 2009, 29(10):3138-3147; doi:10.1523/JNEUROSCI.0155-09.2009

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Behavioral/Systems/Cognitive
Direct Innervation of GnRH Neurons by Metabolic- and Sexual Odorant-Sensing Leptin Receptor Neurons in the Hypothalamic Ventral Premammillary Nucleus

Rebecca L. Leshan,^1,2 Gwendolyn W. Louis,^1,2 Young-Hwan Jo,³ Christopher J. Rhodes,⁴ Heike Münzberg,¹ and Martin G. Myers Jr^1,2

¹Division of Metabolism, Endocrinology, and Diabetes, Department of Internal Medicine and ²Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, Michigan 48109, ³Division of Endocrinology, Department of Medicine, Albert Einstein College of Medicine, Bronx, New York 10461, and ⁴Kovler Diabetes Center, University of Chicago, Chicago, Illinois 60637

Correspondence should be addressed to Dr. Martin G. Myers Jr, Division of Metabolism, Endocrinology, and Diabetes, Department of Medicine, University of Michigan Medical School, 5560 MSRB II/0678, 1150 West Medical Center Drive, Ann Arbor, MI 48109. Email: mgmyers{at}umich.edu

Leptin acts via its receptor (LepRb) on specific CNS neurons to signal the adequacy of long-term energy stores, thereby permitting the expenditure of resources on energy-intensive processes such as reproduction. The ventral premammillary nucleus of the hypothalamus (PMv), which has been implicated in the stimulation of gonadotropin release by olfactory cues, contains numerous LepRb neurons, suggesting a potential role for LepRb PMv neurons in transmitting both metabolic and odorant signals to the neuroendocrine reproductive system. Indeed, Fos immunoreactivity and electrophysiologic recordings revealed the direct activation of LepRb PMv neurons by leptin, and exposure to odors from mice of the opposite sex promoted Fos immunoreactivity (Fos-IR) in many LepRb PMv neurons. To determine the regions innervated by the LepRb PMv neurons, we used two novel cre-activated tract-tracing systems in Lepr^cre animals; data from these systems and from standard tracing techniques revealed that LepRb PMv neurons project to a subset of the regions, including the preoptic area, that are innervated by the PMv as a whole. Furthermore, the retrograde accumulation in LepRb PMv neurons of a trans-synaptic tracer from GnRH neurons revealed the direct innervation of GnRH neurons by many LepRb PMv neurons. Thus, LepRb PMv neurons sense metabolic and sexual odorant cues and project to the rostral hypothalamus to directly innervate GnRH neurons. These results are consistent with a role for LepRb PMv neurons in regulating the reproductive axis in response to metabolic and odorant stimuli.

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Received Jan. 12, 2009; revised Feb. 11, 2009; accepted Feb. 11, 2009.

Correspondence should be addressed to Dr. Martin G. Myers Jr, Division of Metabolism, Endocrinology, and Diabetes, Department of Medicine, University of Michigan Medical School, 5560 MSRB II/0678, 1150 West Medical Center Drive, Ann Arbor, MI 48109. Email: mgmyers{at}umich.edu

This article has been cited by other articles:

				M. Wu, I. Dumalska, E. Morozova, A. van den Pol, and M. Alreja Melanin-concentrating hormone directly inhibits GnRH neurons and blocks kisspeptin activation, linking energy balance to reproduction PNAS, October 6, 2009; 106(40): 17217 - 17222. [Abstract] [Full Text] [PDF]

				E. C. Villanueva, H. Munzberg, D. Cota, R. L. Leshan, K. Kopp, R. Ishida-Takahashi, J. C. Jones, D. C. Fingar, R. J. Seeley, and M. G. Myers Jr. Complex Regulation of Mammalian Target of Rapamycin Complex 1 in the Basomedial Hypothalamus by Leptin and Nutritional Status Endocrinology, October 1, 2009; 150(10): 4541 - 4551. [Abstract] [Full Text] [PDF]

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