Abstract
Many animals, including insects, are known to use visual
landmarks to orient in their environment. In Drosophila
melanogaster, behavioural genetics studies have identified a
higher brain structure called the central complex as being
required for the fly/'s innate responses to vertical visual
features and its short- and long-term memory for visual
patterns. But whether and how neurons of the fly central
complex represent visual features are unknown. Here we use
two-photon calcium imaging in head-fixed walking and flying
flies to probe visuomotor responses of ring
neurons—a class of central complex neurons that
have been implicated in landmark-driven spatial memory in
walking flies and memory for visual patterns in tethered
flying flies. We show that dendrites of ring neurons are
visually responsive and arranged retinotopically. Ring neuron
receptive fields comprise both excitatory and inhibitory
subfields, resembling those of simple cells in the mammalian
primary visual cortex. Ring neurons show strong and, in some
cases, direction-selective orientation tuning, with a notable
preference for vertically oriented features similar to those
that evoke innate responses in flies. Visual responses were
diminished during flight, but, in contrast with the
hypothesized role of the central complex in the control of
locomotion, not modulated during walking. Taken together,
these results indicate that ring neurons represent
behaviourally relevant visual features in the fly/'s
environment, enabling downstream central complex circuits to
produce appropriate motor commands. More broadly, this study
opens the door to mechanistic investigations of circuit
computations underlying visually guided action selection in
the Drosophila central complex.
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