Studies On The Neural Circuit Mechanisms Of Visual Motion Detection In Drosophila Melanogaster By In Vivo Optical Imaging

Motion detection is a basic function of visual system and a classic model of neural computation.Sixty years ago,Hassenstein and Reichardt proposed a physical model to illustrate how the visual system extracts motion information from luminance signals,which consists of three components: a temporal filter to distinguish temporal changes in brightness,a multiplier to detect motion,and a subtractor to determine the direction of motion.So far,neurons responsible for temporal filtering and direction selection have been identified in Drosophila.However,the neuronal implementation of motion detection remains unclear.Here,with a combinatorial approach of genetic screening,two-photon calcium imaging and genetic manipulation,we are going to uncover the motion detection neuron and study the neural circuit mechanism of visual motion detection in Drosophila.The main results and conclusions are as follows:Identifying a novel component of the visual motion detection circuit in Drosophila.First,a synaptic display method based on synaptic labeling technique and the dual genetic expression(Gal4/UAS and Lex A/Lex Aop)system was established.Then by performing a genetic screen on 110 Drosophila strains specially expressed in optic lobe,one strain whose labeled neuron forming synaptic connections with presynaptic sites of direction-selective neurons was isolated,which was considered as the potential motion detection neuron.Single-cell morphology indicated that it was a novel subtype of transmedullary Y(TmY)neurons,which was named as TmY-ds neuron.Characterizing the response properties of TmY-ds neuron to visual stimulation.The results of in vivo two-photon calcium imaging showed that TmY-ds neuron could respond to single-directional or multi-directional motion stimulations and had weak direction selectivity,but did not sense temporal changes of luminance and static orientation cues.From the perspective of the spatial distribution,regions with single/multi-directional response characteristics and different preferred direction were mixed together.These response properties were also validated at the single-cell level.Elucidating the neural circuit mechanism that mediating visual motion detection in Drosophila via TmY-ds neuron.In the visual motion detection circuit,TmY-ds neuron functions upstream of direction-selective neurons: inhibition of TmY-ds neuron reduced the response of direction-selective neurons,whereas its activation was sufficient to induce calcium transients in direction-selective neurons;TmY-ds neuron also functions downstream of temporal filtering neurons: two reported temporal filtering(Mi1/Tm3)neurons both form reciprocal synaptic connections with TmY-ds neuron,in the presence of either Mi1 or Tm3 neurons inhibition,TmY-ds neuron lost its ability to respond to grating motion along the four cardinal directions.This study indicates that a neuron,TmY-ds,exercises the function of motion detection in the visual motion circuit in Drosophila.This paper provides three independent lines of evidence to support this conclusion:(1)TmY-ds neuron could sense all four cardinal directions of motion;(2)TmY-ds neuron is required for the function of direction-selective neurons;(3)TmY-ds neuron receives signal input from the temporal filtering neurons to generate motion sensitivity.This finding also indicates that the visual motion circuit is a tripartite circuit consisting of three groups of neurons — temporal filtering,motion detection and direction-selective neurons.This circuit mechanism supports Hassenstein-Reichardt model in principle.This study provides new evidence for revealing the circuit mechanism of visual motion detection and new ideas for exploring neural computational mechanism as well as the development of brain-inspired intelligence.