Abstract
The dorsal raphe nucleus (DRN) is involved in organizing reward-related behaviours; however, it remains unclear how genetically defined neurons in the DRN of a freely behaving animal respond to various natural rewards. Here we addressed this question using fibre photometry and single-unit recording from serotonin (5-HT) neurons and GABA neurons in the DRN of behaving mice. Rewards including sucrose, food, sex and social interaction rapidly activate 5-HT neurons, but aversive stimuli including quinine and footshock do not. Both expected and unexpected rewards activate 5-HT neurons. After mice learn to wait for sucrose delivery, most 5-HT neurons fire tonically during waiting and then phasically on reward acquisition. Finally, GABA neurons are activated by aversive stimuli but inhibited when mice seek rewards. Thus, DRN 5-HT neurons positively encode a wide range of reward signals during anticipatory and consummatory phases of reward responses. Moreover, GABA neurons play a complementary role in reward processing.
Highlights
The dorsal raphe nucleus (DRN) is involved in organizing reward-related behaviours; it remains unclear how genetically defined neurons in the DRN of a freely behaving animal respond to various natural rewards
As food and sex are fundamental to animal survival and reproduction, how do DRN 5-HT neurons respond to these important natural rewards? are these cells activated only when a well-trained animal is waiting for expected rewards? Alternatively, can they be activated after an animal receives the reward, either expected or unexpected? As GABA neurons comprise a major neuron population in the DRN6,40,41, do they behave differently from 5-HT neurons? In the present study, we tackled these questions using fibre photometry of Ca2 þ signals and electrophysiological recordings of action potential firing from genetically identified 5-HT and GABA neurons in freely behaving mice
GABA neurons in the DRN are suppressed during reward seeking but activated by footshock. These results indicate that DRN 5-HT neurons and GABA neurons respond complementarily when an animal expects and receives various rewards, suggesting that the dorsal raphe serves as an important reward-processing station in parallel to the midbrain dopamine centre
Summary
The dorsal raphe nucleus (DRN) is involved in organizing reward-related behaviours; it remains unclear how genetically defined neurons in the DRN of a freely behaving animal respond to various natural rewards. We addressed this question using fibre photometry and single-unit recording from serotonin (5-HT) neurons and GABA neurons in the DRN of behaving mice. Recording from freely behaving animals is essential for studying the responses to food intake and social interactions It avoids restraint-associated inescapable stress that may change the activity of DRN neurons and 5-HT signalling[42,43]
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