AROUSAL-DEPENDENT SEROTONIN DYNAMICS IN THE POSTPARTUM THALAMUS DURING BEHAVIORAL TRANSITION

Behavioral responses to infant cues critically depend on mother’s arousal state. While an awake mother could react rapidly to her infant’s cry, a sleeping mother must first transition to wakefulness before she can engage in caregiving. The neural substrates underlying such arousal-dependent modulation of infant-oriented behavioral transition remain largely unknown. During nursing or crouching over pups in the nest, maternal mice (dams) respond to pup calls in low frequency range by adjusting her nursing posture or engaging in pup-directed grooming. However, the same calls do not elicit behavior transition when the dam is outside the nest, away from pups. Using one-photon calcium imaging during call-triggered behavioral transition in the nest, we found that calbindin (CB)-expressing neurons in the posterior intralaminar thalamus (PIL^cb) exhibit a distinct activation-deactivation pattern, identifying PIL^cb neurons as a key hub linking sensory processing and maternal behavioral transition. We further show that serotonin in PIL mediates the arousal-dependent modulation of call-triggered behavioral transition. We found dense serotonergic projections around PIL^cb neurons, with significantly higher fiber density in lactating dams compared to nulliparous females. Fiber photometry recordings showed that serotonin levels in PIL fluctuate with arousal states and selectively rise during call playback in NREM sleep, preceding behavioral transition, but not during active wakefulness outside the nest. Finally, whole-cell recordings demonstrated that serotonin enhances the PIL^cb neurons' excitability. Together, our findings suggest that serotonergic modulation in PIL facilitates arousal-dependent maternal behavioral transition by increasing the excitability of PIL^cb neurons in response to pup cues.