Plasticity of visual looming response reveals a dissociation of innate and learned components

Animals rely on both innate and learned behaviour to respond optimally to their environment. However, little is known about how the brain may reconcile the ability to produce hardwired responses essential to survival while still allowing for adaptive flexibility. Here, we demonstrate that innate looming stimulus responses, an innate predator-evasion behaviour, can be robustly extinguished via repeated unreinforced presentation over several days. We report that this extinction is long-lasting and generalises to other contexts, but can be rapidly recovered via the pairing of the visual stimulus with an aversive electric foot-shock stimulus. Moreover, fiber photometric recordings reveal that this behavioural paradigm results in the attenuation of SC and PAG physiological responses to visual looming stimuli, and that these responses do not recover following recovery of behavioural responses. An analysis of c-Fos expression patterns throughout the midbrain and hippocampus uncovered a ventral CA1 (vCA1) ensemble that is active during both innate and learned visual looming fear responses. We investigate the functional significance of this vCA1 ensemble and report that, while its activity is not necessary for innate defensive behaviour, it is necessary for learned fear responses. Together, these findings reveal a novel role of the hippocampus in enabling adaptive behavioural responses to the innately threatening visual looming stimulus which acts in complement with innate circuitry of the SC and PAG.