Behavioral Analysis of Cuttlefish Traveling Waves and Its Implications for Neural Control

Traveling waves (from action potential propagation to swimming body motions or intestinal peristalsis) are ubiquitous phenomena in biological systems and yet are diverse in form, function, and mechanism. An interesting such phenomenon occurs in cephalopod skin, in the form of moving pigmentation patterns called “passing clouds” [1]. These dynamic pigmentation patterns result from the coordinated activation of large chromatophore arrays [2]. Here, we introduce a new model system for the study of passing clouds, Metasepia tullbergi, in which wave displays are very frequent and thus amenable to laboratory investigations. The mantle of Metasepia contains four main regions of wave travel, each supporting a different propagation direction. The four regions are not always active simultaneously, but those that are show synchronized activity and maintain a constant wavelength and a period-independent duty cycle, despite a large range of possible periods (from 1.5 s to 10 s). The wave patterns can be superposed on a variety of other ongoing textural and chromatic patterns of the skin. Finally, a traveling wave can even disappear transiently and reappear in a different position (“blink”), revealing ongoing but invisible propagation. Our findings provide useful clues about classes of likely mechanisms for the generation and propagation of these traveling waves. They rule out wave propagation mechanisms based on delayed excitation from a pacemaker [3] but are consistent with two other alternatives, such as coupled arrays of central pattern generators [3] and dynamic attractors on a network with circular topology [4]. •A new model organism is introduced for study of waves of chromatophore activity•Unexpected complexity is uncovered in this wave display•Variability in behavior constrains possible neural mechanisms Laan et al. investigate the properties of multidomain traveling waves of skin pigmentation in a tropical cuttlefish. The properties of this system (i.e., synchronization between skin domains, temporary gating, duty cycle, propagation speed versus spatial period, etc.) help circumscribe classes of potential mechanisms of wave generation.