Cephalopod
Coleoid cephalopods (octopus, squid, and cuttlefish) can change their skin colors and patterns in the blink of an eye for camouflage or communication. For camouflage, cephalopods can reproduce the texture of the surrounding environment on their skin, mainly by a specialized motor system that controls the expansion state of millions of skin pigment cells called chromatophores. How does the chromatophore system generate countless texture-matching patterns? We developed methods to track the instantaneous expansion state of >100k chromatophores in the behaving cuttlefish Sepia officinalis. When cuttlefish changed camouflage for different backgrounds, it explored in the skin pattern space and searched for a good match to the background. Along these searching paths, chromatophores were coordinated in an extremely flexible and non-stereotypical way. The dynamics of the control system, however, revealed certain constraints for motion within pattern space. To understand how the chromatophore system gained complexity during evolution, we then compared Sepia with another cephalopod, the bobtail squid Euprymna berryi. Euprymna camouflages by covering itself with sand. Its chromatophores changed size mostly synchronously, resulting in switches between transparency and dark pigmentation of the entire animal. We identified motoneurons that control chromatophores in both species, yet with different levels of control specificity: a somatotopic map of motoneurons were present in Sepia but absent in Euprymna. These findings together begin to uncover the organizing principles of the neural circuits that generate a high-dimensional motor output, and may reveal how such neural circuits have diverged adaptively during evolution.
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Drosophila
Animals show circadian rhythms in a variety of physiological functions and behaviors. In Drosophila melanogaster, behavioral rhythms are driven by circadian clock genes that are oscillating in ~150 circadian pacemaker neurons. To explain how circadian neurons encode time and regulate different behavioral rhythms, I performed 24-hour in vivo whole-brain calcium imaging using light-sheet microscopy. First, I found that different groups of circadian neurons show circadian rhythms in spontaneous neural activity with diverse phases. The neural activity phases of the M and E pacemaker groups, which are associated with the morning and evening locomotor activities respectively, occur ~4 hours before their respective behaviors (Liang et al Science 2016). I also showed that neural activity rhythms are generated by circadian clock gene oscillations, which regulate the expression of IP3R and T-type calcium channels (Liang et al PNAS 2022). Next, I asked how the diverse phases of neural activity are generated from the in-phase clock gene oscillations. Groups of circadian neurons inhibit each other via long-duration neuromodulation, mediated by neuropeptides PDF and sNPF, such that their activity phases are properly staggered across the day and night. Certain activity phases are also regulated by environmental light inputs (Liang et al Neuron 2017). I then identified an output pathway by which circadian neurons regulate the locomotor activity rhythm. M and E pacemaker groups independently activate a common pre-motor center (termed ellipsoid body ring neurons) through the agency of specific dopaminergic interneurons (Liang et al Neuron 2019). Finally, using methods including whole-brain pan-neuronal imaging, I further identified several output circuits downstream of circadian neurons. Circadian neural activity rhythms propagate through these circuits to regulate different behavioral outputs including sleep, olfaction, mating, and feeding rhythms. Together, my findings show how circadian clocks regulate diverse behavioral outputs by two steps; first, circadian clock genes generate diverse circadian neural activity rhythms within a network of interacting pacemaker neurons; then, sequentially-active pacemaker neurons independently and together regulate diverse behavioral outputs by generating diverse circadian neural activity rhythms in different downstream output circuits.
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