Generative rules of Drosophila locomotor behavior as a candidate homology across phyla

The discovery of shared behavioral processes across phyla is a significant step in the establishment of a comparative study of behavior. We use immobility as an origin and reference for the measurement of fly locomotor behavior; speed, walking direction and trunk orientation as the degrees of freedom shaping this behavior; and cocaine as the parameter inducing progressive transitions in and out of immobility. We characterize and quantify the generative rules that shape Drosophila locomotor behavior, bringing about a gradual buildup of kinematic degrees of freedom during the transition from immobility to normal behavior, and the opposite narrowing down into immobility. Transitions into immobility unfold via sequential enhancement and then elimination of translation, curvature and finally rotation. Transitions out of immobility unfold by progressive addition of these degrees of freedom in the opposite order. The same generative rules have been found in vertebrate locomotor behavior in several contexts (pharmacological manipulations, ontogeny, social interactions) involving transitions in-and-out of immobility. Recent claims for deep homology between arthropod central complex and vertebrate basal ganglia provide an opportunity to examine whether the rules we report also share common descent. Our approach prompts the discovery of behavioral homologies, contributing to the elusive problem of behavioral evolution.

. Detailed dynamics of the transition out of immobility based on velocity components, which determine speed and curvature and their coordination. (A) Transition out of immobility is illustrated by plotting the x and y positions as a function of time. Starting from absolute immobility, the fly performs tiny but fast oscillations in the x and y positions, reflecting fast rotations in place, which progressively slow down, and finally evolve into large displacements, corresponding to normal progression. (B) The early stage of transition out of immobility is characterized by very low speed, whose perpendicular velocity components (vx and vy) alternate in an oscillatory fashion (vx is zero when vy is max, and vice-versa; see inset in green), corresponding to very high curvature. The velocity components along the x and y directions capture the coordinated circling as the fly transitions out of immobility, whereas speed (v) misses the subtleties of rotation in place. (C) Phase-plot of speeds along x and y directions, containing both low speeds (in red), but also high-speed progression segments in all directions at a later stage of transition out of immobility. (D) Zoom in of the plot in (C) showing only the velocity components during the time interval from minute 2 to minute 14. On the whole, this closer look at path dynamics reveals that high curvature emerges from small, fast and alternating oscillations in orthogonal components of the velocity vector at typical speeds of 1mm/s, which reveal the minute circles traced by the animal as it rotates in place (during walking at higher speeds, flies show a much larger range of velocity components).

Supplementary Movies
Movie S1. Link: https://www.youtube.com/watch?v=bgRyVv8Ae04 File: attached movie MS1_fly_NarrowingDown_track.avi Legend: Narrowing down of fly locomotion behavior upon cocaine administration (video tracking). Upon sniffing cocaine Drosophila melanogaster performs a "shutdown" sequence, proceeding from forward progression to circling to rotating in place, culminating with immobility.

Movie S2
Link: https://www.youtube.com/watch?v=LBAugS1Rk7A File: attached movie MS2_fly_BuildUp_track.avi Legend: Buildup of fly locomotor behavior upon cocaine administration (video tracking). Upon recovery from cocaine influence Drosophila melanogaster performs a "warmup" sequence, starting with rotation in place and then superimposing on it forward progression, thus generating circling. As rotation diminishes, circling turns into forward progression along relatively straight lines.

Movie S3
Link: https://youtu.be/CzT7sn0RdkM File: attached movie MS3_fly_NarrowingDown_animate.mov Legend: Narrowing down of fly locomotor behavior upon cocaine administration (analysis animation). Rotational versus translational degrees of freedom in Drosophila melanogaster narrowing down ("shutdown") of locomotor repertoire within the Mobility Gradient upon cocaine stimulation.

Movie S4
Link: https://youtu.be/9vkTYuFQLSI File: attached movie MS4_fly_BuildUp_animate.mov Legend: Buildup of fly locomotor behavior upon cocaine administration (analysis animation). Rotational versus translational degrees of freedom in Drosophila melanogaster buildup ("warmup") of locomotor repertoire within the Mobility Gradient) upon cocaine stimulation.

Movie S5
Link: https://www.youtube.com/watch?v=wVaeqWPZnfc File: attached movie MS5_infant_rat.mov Legend: Buildup of infant rat behavior upon novel environment. When placed in a hostile environment outside its nest, an infant rat becomes immobile. Immobility is dissipated through the performance of horizontal movements that spread from head to tail. Forward progression is added after exhaustion of the horizontal plain, and finally vertical movement appears, here of the head. Vertical movement also spreads from head to tail.

Movie S6
Link: https://www.youtube.com/watch?v=3JQZgTwQrwM File: attached movie MS6_hedgehog.avi Legend: Buildup of hedgehog behavior upon novel environment. When placed in a hostile environment outside its home cage a hedgehog performs the warmup sequence: first pivoting in place, gaining support from forequarters to hindquarters and proceeding to forward locomotion.

Movie S7
Link: https://www.youtube.com/watch?v=YzD21jpa09g File: attached movie MS7_rat_fight.avi Legend: Buildup and narrowing down of rat behavior upon social interactions. A ritualized fighting interaction between two wild caught Rattus norvegicus males. The inferior animal exhibits the less mobile portion of the mobility gradient, culminating in rearing and rotating around the hindquarters, whereas the superior may rear and rotate both around the hind-legs and around the forelegs, exhibiting an expanded freedom of movement in both the horizontal and vertical dimensions.