Hormonal gain control of a medial preoptic area social reward circuit
Open Access
- 30 January 2017
- journal article
- research article
- Published by Springer Science and Business Media LLC in Nature Neuroscience
- Vol. 20 (3), 449-458
- https://doi.org/10.1038/nn.4487
Abstract
Social behaviors require neural circuits to process social cues and orchestrate motivational states. This study identifies a subpopulation of hypothalamic neurons expressing neurotensin that are engaged by social and hormonal signals. These neurons project to midbrain dopaminergic reward systems to promote and reinforce social and motivated behavior in a hormone-sensitive manner. Neural networks that control reproduction must integrate social and hormonal signals, tune motivation, and coordinate social interactions. However, the neural circuit mechanisms for these processes remain unresolved. The medial preoptic area (mPOA), an essential node for social behaviors, comprises molecularly diverse neurons with widespread projections. Here we identify a steroid-responsive subset of neurotensin (Nts)-expressing mPOA neurons that interface with the ventral tegmental area (VTA) to form a socially engaged reward circuit. Using in vivo two-photon imaging in female mice, we show that mPOANts neurons preferentially encode attractive male cues compared to nonsocial appetitive stimuli. Ovarian hormone signals regulate both the physiological and cue-encoding properties of these cells. Furthermore, optogenetic stimulation of mPOANts–VTA circuitry promotes rewarding phenotypes, social approach and striatal dopamine release. Collectively, these data demonstrate that steroid-sensitive mPOA neurons encode ethologically relevant stimuli and co-opt midbrain reward circuits to promote prosocial behaviors critical for species survival.Keywords
This publication has 65 references indexed in Scilit:
- Activation of VTA GABA Neurons Disrupts Reward ConsumptionNeuron, 2012
- Leptin Action via Neurotensin Neurons Controls Orexin, the Mesolimbic Dopamine System and Energy BalanceCell Metabolism, 2011
- Minireview: Estrogen Receptor-Initiated Mechanisms Causal to Mammalian Reproductive BehaviorsEndocrinology, 2011
- Dopamine in Motivational Control: Rewarding, Aversive, and AlertingNeuron, 2010
- Sex Hormones and Mood in the PerimenopauseAnnals of the New York Academy of Sciences, 2009
- Leptin Acts via Leptin Receptor-Expressing Lateral Hypothalamic Neurons to Modulate the Mesolimbic Dopamine System and Suppress FeedingCell Metabolism, 2009
- Assessing Reproductive Status/Stages in MiceCurrent Protocols in Neuroscience, 2009
- Sexually dimorphic enhancement by estradiol of male urinary odor detection thresholds in mice.Behavioral Neuroscience, 2008
- Sex differences in drug abuseFrontiers in Neuroendocrinology, 2007
- Sexual behavior in male rodentsHormones and Behavior, 2007