Ray, R. P. | bioRxiv Science

bioRxiv2025

Octopamine instructs head direction plasticity

Many plasticity rules rely on adjusting the strength of synapses between pairs of cells based on their coincident activity. We uncovered a new mechanism for coincidence detection in the Drosophila head direction network. To maintain an accurate sense of direction, head direction neurons that signal orientation during navigation must learn to anchor to relevant external sensory cues in novel environments. Yet the synaptic mechanism for this form of unsupervised learning is unknown in any organism. In Drosophila, GABAergic visual inputs converge onto head direction neurons, and these inhibitory synapses change strength with experience to learn the relationship between visual landmarks and head direction. However, how coincident pre- and postsynaptic activity is detected across this inhibitory synapse is not understood. We discovered that neurons which release the monoamine octopamine close a feedback loop that conveys postsynaptic head direction activity onto presynaptic terminals of visual inputs. This octopamine pathway is required for anchoring the head direction network to visual cues. Furthermore, pairing structured activation of octopamine neurons with a visual cue is sufficient to drive rapid plasticity, even without postsynaptic head direction cell activity. Previous work has extensively characterized coincidence detection mechanisms at excitatory synapses; our work defines a novel mechanism for coincidence detection at an inhibitory synapse, in which postsynaptic activity is relayed via a neuromodulatory neuron onto presynaptic terminals.

neuroscience↗

bioRxiv2019

The neuroanatomical ultrastructure and function of a biological ring attractor

Neural representations of head direction have been discovered in many species. A large body of theoretical work has proposed that the dynamics associated with these representations is generated, maintained, and updated by recurrent network structures called ring attractors. We performed electron microscopy-based circuit reconstruction and RNA profiling of identified cell types in the heading direction system of Drosophila melanogaster to directly determine the underlying neural network. We identified network motifs that have been hypothesized to maintain the heading representation in darkness, update it when the animal turns, and tether it to visual cues. Functional studies provided additional support for the proposed roles of individual circuit elements. We also discovered recurrent connections between neuronal arbors with mixed pre- and post-synaptic specializations. Overall, our results confirm that the Drosophila heading direction network contains the core components of a ring attractor while also revealing unpredicted structural features that might enhance the networks computational power.

neuroscience↗