The role of a population of descending neurons in the optomotor response in flyingDrosophila

Abstract

To maintain stable flight, animals continuously perform trimming adjustments to compensate for internal and external perturbations. Whereas animals use many different sensory modalities to detect such perturbations, insects rely extensively on optic flow to modify their motor output and remain on course. We studied this behavior in the fruit fly, Drosophila melanogaster, by exploiting the optomotor response, a robust reflex in which an animal steers so as to minimize the magnitude of rotatory optic flow it perceives. Whereas the behavioral and algorithmic structure of the optomotor response has been studied in great detail, its neural implementation is not well-understood. In this paper, we present findings implicating a group of nearly homomorphic descending neurons, the DNg02s, as a core component for the optomotor response in flying Drosophila. Prior work on these cells suggested that they regulate the mechanical power to the flight system, presumably via connections to asynchronous flight motor neurons in the ventral nerve cord. When we chronically inactivated these cells, we observed that the magnitude of the optomotor response was diminished in proportion to the number of cells silenced, suggesting that the cells also regulate bilaterally asymmetric steering responses via population coding. During an optomotor response, flies coordinate changes in wing motion with movements of their head, abdomen, and hind legs, which are also diminished when the DNg02 cells are silenced. Using two-photon functional imaging, we show that the DNg02 cells respond most strongly to patterns of horizontal motion and that neuronal activity is closely correlated to motor output. However, unilateral optogenetic activation of DNg02 neurons does not elicit the asymmetric changes in wing motion characteristic of the optomotor response to a visual stimulus, but rather generates bilaterally symmetric increases in wingbeat amplitude. We interpret our experiments to suggest that flight maneuvers in flies require a more nuanced coordination of power muscles and steering muscles than previously appreciated, and that the physical flight apparatus of a fly might permit mechanical power to be distributed differentially between the two wings. Thus, whereas our experiments identify the DNg02 cells as a critical component of the optomotor reflex, our results suggest that other classes of descending cells targeting the steering muscle motor neurons are also required for the behavior.

Transforming descending input into behavior: The organization of premotor circuits in theDrosophilaMale Adult Nerve Cord connectome

“…In addition, several DNs (DNp31, DNg02 and DNp03 examples in Figure 12G) as well as Tect INs themselves take pathways to indirect control MNs–namely to the tergopleural and pleurosternal MNs which may control thoracic stiffness or tension. While the roles of the ICMs in flight have not received as much investigation as other muscle categories, it appears that concurrent control of PMs and ICMs are important for the function of DNs such as the DNg02s which modulate wingbeat amplitude in flight (Namiki et al, 2022; Palmer et al, 2022).…”

“…While the actual function of this motif is unknown, one intriguing possibility is that the recurrent excitatory and inhibitory connections in the Tect INs and IN06B066 group 16779 form an inhibition-stabilized network, where a stable level of excitatory activity can be maintained in the excitatory subnetwork with feedback inhibition from the inhibitory subnetwork serving to prevent runaway excitation (Sadeh and Clopath, 2021). Such networks are notable for the paradoxical observation that excitation to the inhibitory neurons decreases the steady-state activity for both the inhibitory and excitatory neuron populations (Sadeh and Clopath, 2021) (Namiki et al, 2022;Palmer et al, 2022).…”

Wings of Change: aPKC/FoxP-dependent plasticity in steering motor neurons underlies operant selflearning inDrosophila

“…wing beat amplitude (a major contributing factor to yaw torque) (114), re-vealed aPKC/FoxP co-expressing MNs innervating a specific subset of these muscles (Figure 3), corroborating our hypothesis. MNs in the VNC (117,118). This suggests that in the ventral nerve cord, the steering motor neurons are the only neurons that OMRs and operant self-learning share.…”

“…From this realization, the question arises if there are other shared neural components between OMRs and operant learning in addition to the doubly labeled steering MNs. Evidence suggests that the steering commands for OMRs are communicated directly from visual areas in the brain via (both identified and yet to be identified) descending neurons with direct synaptic connections onto the steering MNs in the VNC (117,118). This suggests that in the ventral nerve cord, the steering motor neurons are the only neurons that OMRs and operant self-learning share.…”

Networks of descending neurons transform command-like signals into population-based behavioral control

“…This is in line with the observation that a population of 15 DNs can modulate wing beat amplitude 29 and that the activation of individual DNs has a lower probability of driving take-off than co-activation of multiple DNs 30 . Beyond controlling kinematics, it has also been shown that DNs can convey sensory information 28,31 and that they may be modulatory 32,33,34,35 . All of these observations suggest that, rather than being low-dimensional, DN control of behavior is population-based or high-dimensional: the brain flexibly engages larger populations of DNs to construct and mediate complete behaviors.At first glance, these two models-command-like versus population-based DN behavioral controlappear to be incompatible.…”