Oxytocin Receptor-Expressing Neurons in the Paraventricular Thalamus Regulate Feeding Motivation through Excitatory Projections to the Nucleus Accumbens Core

Apr 7, 2022The Journal of neuroscience : the official journal of the Society for Neuroscience

Neurons with Oxytocin Receptors in a Thalamus Area Influence Feeding Motivation by Exciting the Brain’s Reward Center

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Abstract

Chemogenetic activation of oxytocin receptor-expressing paraventricular thalamus neurons increased meal frequency by promoting food-seeking behavior.

Oxytocin receptor-expressing neurons in the paraventricular thalamus may influence feeding motivation through their projections to the nucleus accumbens core.
Activation of these neurons did not increase total food intake due to a compensatory decrease in meal size.
Optogenetic stimulation of paraventricular thalamus projections excited neurons in the nucleus accumbens core and posterior basolateral amygdala.
Food-seeking behavior was promoted by the stimulation of paraventricular thalamus-nucleus accumbens core projections, while stimulation of paraventricular thalamus-posterior amygdala projections had little effect on feeding.
The findings suggest that oxytocin receptor-expressing neurons represent a distinct group of glutamate neurons involved in the motivation for food rewards.

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Oxytocin receptors (OTR) have been found in the paraventricular thalamus (PVT) for the regulation of feeding and maternal behaviors. However, the functional projections of OTR-expressing PVT neurons remain largely unknown. Here, we used chemogenetic and optogenetic tools to test the role of OTR-expressing PVT neurons and their projections in the regulation of food intake in both male and female OTR-Cre mice. We found chemogenetic activation of OTR-expressing PVT neurons promoted food seeking under trials with a progressive ratio schedule of reinforcement. Using Feeding Experimentation Devices for real-time meal measurements, we found chemogenetic activation of OTR-expressing PVT neurons increased meal frequency but not cumulative food intake because of a compensatory decrease in meal sizes. In combination with anterograde neural tracing and slice patch-clamp recordings, we found optogenetic stimulation of PVT OTR terminals excited neurons in the posterior basolateral amygdala (pBLA) and nucleus accumbens core (NAcC) as well as local PVT neurons through monosynaptic glutamatergic transmissions. Photostimulation of OTR-expressing PVT-NAcC projections promoted food-seeking, whereas selective activation of PVT-pBLA projections produced little effect on feeding. In contrast to selective activation of OTR terminals, photostimulation of a broader population of glutamatergic PVT terminals exerted direct excitation followed by indirect lateral inhibition on neurons in both NAcC and anterior basolateral amygdala. Together, these results suggest that OTR-expressing PVT neurons are a distinct population of PVT glutamate neurons that regulate feeding motivation through projections to NAcC.The paraventricular thalamus plays an important role in the regulation of feeding motivation. However, because of the diversity of paraventricular thalamic neurons, the specific neuron types promoting food motivation remain elusive. In this study, we provide evidence that oxytocin receptor-expressing neurons are a specific group of glutamate neurons that primarily project to the nucleus accumbens core and posterior amygdala. We found that activation of these neurons promotes the motivation for food reward and increases meal frequency through projections to the nucleus accumbens core but not the posterior amygdala. As a result, we postulate that oxytocin receptor-expressing neurons in the paraventricular thalamus and their projections to the nucleus accumbens core mainly regulate feeding motivation but not food consumption. SIGNIFICANCE STATEMENT

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Oxytocin Receptor-Expressing Neurons in the Paraventricular Thalamus Regulate Feeding Motivation through Excitatory Projections to the Nucleus Accumbens Core

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