Insulin acts on peripheral tissues including liver, muscle and adipose tissue to directly control glucose metabolism, while also acting in the brain to concordantly regulate nutrient fluxes, feeding behaviour and energy homeostasis. Although our understanding of the neural circuitry controlling feeding behaviour and energy expenditure has grown considerably in the last few years, the neural processes by which insulin elicits its effects on glucose metabolism are less clear.
Here we define heterogeneous populations of hypothalamic pro-opiomelanocortin (POMC) neurons that are activated or inhibited by insulin and thereby repress or inhibit hepatic glucose production (HGP). The proportion of POMC neurons activated by insulin was dependent on the regulation of insulin receptor signalling by the phosphatase TCPTP, which is increased by fasting, degraded after feeding and elevated in diet-induced obesity.
TCPTP-deficiency in POMC neurons enhanced neuronal insulin signalling and the proportion of POMC neurons activated by insulin to repress HGP. Elevated TCPTP in POMC neurons in diet-induced obesity and/or after fasting repressed neuronal insulin signalling, the activation of POMC neurons by insulin and the insulin-induced POMC-mediated repression of HGP. Our findings define a molecular mechanism for integrating POMC neural plasticity with feeding to control glucose metabolism.