The Neural Mechanism Of “Approach And Avoidance” Innate Behaviors Triggered By Superior Colliculus In Midbrain

Approach and avoidance are universal phenomena of life.For human and animals,approach and avoidance are series of inherent and innate behaviors,such as prey capture,food intake and running away from natural predator.For example,a moving prey will trigger the starving mouse to hunt.On the contrary,environmental threats,e.g.looming visual stimulus,will lead to dimorphic avoidance behaviors of mouse.Based on the study of various innate behaviors from different animal species,Konrad Lorenz and Nikolaas Tinbergen found that a sign stimulus played a key role in triggering instinctive behavioral sequence,and they raised a concept called the innate releasing mechanism.Inspired by this concept,J(?)rg-Peter Ewert took the lead to do systematic research of“feature detection” theory in toad visual system.He found the neurons in optic tectum(OT)could been specifically activated by worm-like stripe.However,few is known about what features from prey and predator trigger approach and avoidance behaviors,and the underlying neural mechanisms are largely unknown.For hunting behavior,we used mice as animal model and catching cockroaches as behavioral paradigm.Because mammalian superior colliculus(SC)is homologous to OT in amphibians,we applied Fos-Cre ERT2 mice to label the SC neurons that were activated during prey capture and the neural pathway they involved in.Fos-Cre ERT2 strategy showed subthalamus(S)-projecting SC intermediate neurons participated in hunting behavior.Besides,the results of optogenetic and molecular genetic activation and silence manipulation implied that SC-S pathway was sufficient and necessary for hunting behavior.Furthermore,in vivo electrophysiological experiments confirmed that S-projecting SC neurons detected the prey derived visual and somatosensory cues.These results above revealed SC-S pathway specifically engaged in translating prey derived sensory cues into neural signals to provoke predatory hunting.We established looming visual stimulus paradigm to study predator avoidance behaviors.After screening different types of neurons in SC,we were lucky to found that photostimulation of SC parvalbumin positive(PV+)neurons provoked stereotyped escape behavior followed by freezing.Then,inactivation of PV+ SC neurons impaired dimorphic defensive behaviors in response to looming stimulus.Whole-brain mapping indicated PV+ SC neurons mainly project to parabigeminal nucleus(PBGN)and lateral posterior thalamic nucleus(LPTN).Optogenetic activation of PV+ SC-PBGN and PV+ SC-LPTN pathways mimicked the dimorphic defensive behaviors.What`s more,bilateral inactivation of either nucleus resulted in the defensive behavior dominated by the other nucleus.Finally,electrophysiological results confirmed that PV+ SC neurons were specifically evoked by looming visual stimulus.These data above suggested that PV+ SC neurons worked as looming detector or radar,and transmitted threat-relevant visual signals to the neurons in PBGN and LPTN to trigger escape and freezing responses respectively.