Dopamine neurons govern olfactory-gated infant begging behavior

Abstract

Altricial young of many species beg parents for the nutrients required for healthy development. From human crying to begging chicks, young expend precious energy reserves to communicate their hunger. Despite repeated independent evolutionary origins, the neural basis of parent-directed communication by infants is unknown. Here, we examined the sensory and neural basis of begging behavior in tadpoles of the monogamous and biparental Mimetic poison frog (Ranitomeya imitator). In this species, tadpoles beg parents for egg meals by dancing. We used this robust motor display to determine that tadpoles use multimodal cues for caregiver recognition, where olfactory cues are necessary for caregiver recognition while visual cues provide an orientation goal. We found that dopamine related brain regions have higher neural activity in begging tadpoles and that dopamine signaling had opposing modulatory effects through D1 and D2 family receptors, similar to swimming behavior in other tadpole species. We then identified caudal posterior tuberculum dopamine neurons as more active during begging behavior and sensitive to caregiver olfactory cues. Projections of these dopaminergic neurons to the spinal accessory motor nucleus are required for begging displays. These findings support the idea that dopamine regulates olfactory-guided parental recognition in young and opens many avenues for studying how new communication behaviors can evolve from ancestral motor circuits.

Activity of FoxP2-positive neurons correlate with tadpole begging behavior

“…In this same study, the variant of FoxP2 expressed in mice also impacted dopamine concentrations in the striatum and nucleus accumbens. Dopamine signaling is critical to tadpole begging behavior [35], and our results here suggest a potential role for FoxP2 in modulating dopamine signaling that should be investigated in the future. This general cellular dysregulation can be seen in mice with FoxP2 mutations, where the striatum is more active and motor-skill learning is disrupted due to abnormal temporal coordination of striatal firing [57].…”

“…All Ranitomeya imitator tadpoles used were bred from our laboratory colony [35]. Adult R. imitator females from actively reproducing breeding pairs were used as stimulus animals in the begging context.…”

“…We quantified the proportion of FoxP2-positive cells that colocalized with the pS6 marker of neural activity in begging tadpoles compared to controls (Figure 2). Given the wide distribution of FOXP2, we focused our analyses on brain regions associated with dopaminergic signaling, which is required for begging behavior in this species [18]. The activity of FoxP2positive cells depended on an interaction of behavioral group and brain region (group*region: F5 = 300.37, p < 0.001).…”

“…imitator tadpoles rely on smell to distinguish between caregiver stimuli [18], investigating FoxP2's role in sensory integration broadly rather than a narrow focus on vocal communication may be a valuable future research direction. Overall, the distribution of FoxP2 in the amphibian brain suggests a largely conserved pattern across terrestrial vertebrates that function in learning and executing social behaviors important for survival.…”

“…In bats, species differences in FoxP2 expression in the olfactory bulb are associated with different feeding habits (frugivorous versus insectivorous) [54], suggesting that FoxP2 may influence olfactory processing. Given R. imitator tadpoles rely on smell to distinguish between heterospecific stimuli [37], investigating FoxP2's role in sensory integration broadly may be a valuable future research direction. Overall, the distribution of FoxP2 in the amphibian brain suggests a largely conserved pattern across terrestrial vertebrates.…”