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Abstract
The neural mechanisms underlying hunger are poorly understood. AgRP neurons are activated by energy deficit and promote voracious food consumption, suggesting these cells may supply the fundamental hunger drive that motivates feeding. However recent in vivo recording experiments revealed that AgRP neurons are inhibited within seconds by the sensory detection of food, raising the question of how these cells can promote feeding at all. Here we resolve this paradox by showing that brief optogenetic stimulation of AgRP neurons before food availability promotes intense appetitive and consummatory behaviors that persist for tens of minutes in the absence of continued AgRP neuron activation. We show that these sustained behavioral responses are mediated by a long-lasting potentiation of the rewarding properties of food and that AgRP neuron activity is positively reinforcing. These findings reveal that hunger neurons drive feeding by transmitting a positive valence signal that triggers a stable transition between behavioral states.
Highlights
Food deprivation motivates animals to find and consume food
Optogenetic or chemogenetic stimulation of Agouti-related protein (AgRP) neurons promotes intense food consumption as well as appetitive behaviors that lead to food discovery (Aponte et al, 2011; Krashes et al, 2011), whereas inhibition of these neurons leads to aphagia (Gropp et al, 2005; Krashes et al, 2011; Luquet et al, 2005)
Photostimulation was terminated and food was made available (Figure 1B). We found that this preparatory photostimulation triggered intense feeding upon subsequent food presentation (Figure 1D–G). This voracious feeding approached the level of food consumption observed following an overnight fast (Figure 1E); it did not require learning, as it was observed in the first trial of every mouse (Figure 1—figure supplement 1); and it was absent from control mice that lacked ChR2 expression (Figure 1—figure supplement 1)
Summary
Food deprivation motivates animals to find and consume food. This implies that the brain can transform nutritional signals into the desire to eat, but how this transformation is performed remains unclear.Agouti-related protein (AgRP) neurons within the arcuate nucleus (ARC) of the hypothalamus are a molecularly-defined cell type that is important for the control of feeding. Food deprivation motivates animals to find and consume food. This implies that the brain can transform nutritional signals into the desire to eat, but how this transformation is performed remains unclear. Agouti-related protein (AgRP) neurons within the arcuate nucleus (ARC) of the hypothalamus are a molecularly-defined cell type that is important for the control of feeding. Optogenetic or chemogenetic stimulation of AgRP neurons promotes intense food consumption as well as appetitive behaviors that lead to food discovery (Aponte et al, 2011; Krashes et al, 2011), whereas inhibition of these neurons leads to aphagia (Gropp et al, 2005; Krashes et al, 2011; Luquet et al, 2005). AgRP neurons are poised to connect nutritional signals with the motivational processes that govern feeding
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