A neural hub that coordinates learned and innate courtship behaviors

Abstract

Holistic behaviors often require the coordination of innate and learned movements. The neural circuits that enable such coordination remain unknown. Here we identify a midbrain cell group (A11) that enables male zebra finches to coordinate their learned songs with various innate behaviors, including female-directed calling, orientation and pursuit. Anatomical mapping reveals that A11 is at the center of a complex network including the song premotor nucleus HVC as well as brainstem regions crucial to innate calling and locomotion. Notably, lesioning A11 terminals in HVC blocked female-directed singing, but did not interfere with female-directed calling, orientation or pursuit. In contrast, lesioning A11 cell bodies abolished all female-directed courtship behaviors. However, males with either type of lesion still produced songs when in social isolation. Lastly, monitoring A11 terminals in HVC showed that during courtship A11 inputs to the song premotor cortex signal the transition from innate to learned vocalizations. These results show how a brain region important to reproduction in both birds and mammals coordinates learned vocalizations with innate, ancestral courtship behaviors.

The neural distribution of the avian homologue of oxytocin, mesotocin, in two songbird species, the zebra finch and the canary: A potential role in song perception and production

“…VTA and PAG send dopaminergic projections to song control nuclei-HVC, the robust nucleus of the arcopallium (RA), and Area X-and dopamine metabolites in these two areas are correlated with song production (Appeltants et al, 2000(Appeltants et al, , 2002Castelino et al, 2007;Heimovics et al, 2011;Lewis et al, 1981). Damaging or inactivating these regions also influences song production, reducing directed song in the case of VTA and increasing latency to sing in PAG (Ben-Tov et al, 2021;Haakenson et al, 2020;Hara et al, 2007). Furthermore, these two regions may also serve as a relay for the previously discussed effects of OT in POA, as the POM does not send direct projections to song control nuclei but does have reciprocal projections with VTA and PAG (Riters & Alger, 2004;Theofanopoulou et al, 2017).…”

Reciprocal processes of sensory perception and social bonding: an integrated social‐sensory framework of social behavior

“…These point of confluence raises the question of how motivational information is relayed between the SDMN and the SCS. One intriguing possibility is that dopaminergic projections from periaqueductal gray (PAG – specifically A11) to HVC function to relay motivational information to the SCS 169,170 . Continued research regarding the role of these networks in regulating acoustic communication between partners promises to reveal a more comprehensive view of the neural mechanisms subserving social behavior.…”

A novel AAV1 variant for transduction of Japanese quail neurons in vitro and in vivo

“…These provide unique opportunities for comparative studies of cellular mechanisms leading to behavior 3 . Indeed, these realizations are behind the increased interest in avian neuroscience in recent years 1,2,7,[12][13][14][15][16][17] .…”