Distinct patterns of activity within columns of the periaqueductal gray are associated with functionally distinct birdsongs

Male songbirds produce female-directed songs in spring that convey a state of sexual motivation. Many songbirds also sing in fall flocks in affiliative/gregarious contexts in which song is linked to an intrinsic positive affective state. The periaqueductal gray (PAG) in mammals, which is organized into functional columns, integrates information from multiple brain regions and relays this information to vocal motor areas so that an animal emits a vocal signal reflective of its affective state. Here, we test the hypothesis that distinct columns in the songbird PAG play roles in the distinct affective states communicated by sexually motivated and gregarious song. We quantified the numbers of immediate early gene ZENK-positive cells in 16 PAG subregions in male European starlings (Sturnus vulgaris) after singing gregarious or sexually motivated song. Results suggest that distinct PAG columns in songbirds context-specifically regulate song, agonistic, and courtship behaviors. A second exploratory, functional tract-tracing study also demonstrated that inputs to the PAG from specific subregions of the medial preoptic nucleus may contribute to gregarious song and behaviors indicative of social dominance. Together, findings suggest that conserved PAG columns and inputs from the preoptic nucleus may play a role in context-specific vocal and other social behaviors. In this paper, we provide evidence that distinct regions within the periaqueductal gray (PAG) in songbirds may context-specifically regulate song, agonistic, and courtship behaviors. These findings provide evidence for contributions from functionally distinct longitudinal columns to motivationally/affectively distinct songs and suggest that the songbird PAG may play a role in the affective state conveyed by birdsongs. An exploratory functional tract tracing study also demonstrated that inputs to the PAG from subregions of the medial preoptic nucleus may contribute to song and behaviors indicative of social dominance. image

Automated summary

This study provides evidence that distinct regions within the periaqueductal gray (PAG) in songbirds may context-specifically regulate song, agonistic, and courtship behaviors. The findings also suggest that inputs to the PAG from subregions of the medial preoptic nucleus may contribute to song and behaviors indicative of social dominance. These results highlight the role of PAG and its inputs in context-specific vocal and social behaviors.