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

Abstract

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". These dynamic pigmentation patterns result from the coordinated activation of large chromatophore arrays. 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 but are consistent with two other alternatives, such as coupled arrays of central pattern generators and dynamic attractors on a network with circular topology.

Dynamic Skin Patterns in Cephalopods

“…As the patterns of these species are very similar, we will describe them together. For a more detailed analysis of M. pfefferi see Thomas and MacDonald (2016), and for M. tullbergi see Laan et al (2014). These species inhabit subtidal soft sediments and are typically benthic, employing the fourth arm pair and ambulatory flaps on the ventral surface of the mantle to amble along the seafloor with a quadrupedal walking gait (Roper and Hochberg, 1988).…”

“…Through a detailed analysis of the complex dynamic pattern of M. tullbergi , Laan et al (2014) propose an alternative neural control system originating from the central nervous system. They suggest that passing wave patterns could be controlled via a set of oscillatory neurons analogous to the central pacemakers governing rhythmic locomotory movements.…”

“…Indeed, control networks for skin chromatophores and swimming fin motor neurons are known to coexist in parts of the cuttlefish brain and stimulation of these areas can result in both patterning and locomotory behavior (Messenger, 2001; Osorio, 2014). This kind of central control could generate dynamic wave patterns in single skin fields, and, most interestingly, could be applied to multiple skin fields resulting in the synchronous activation of different pattern units, such as those in the Metasepia species (Laan et al, 2014). Furthermore, central control would permit the speed of passing waves to be adjusted depending on behavioral context, and for different dynamic and/or static patterns to be co-expressed (e.g., S. latimanus, S. apama , and M. tullbergi ; Laan et al, 2014).…”

Social Media and citizen science provide valuable data for behavioural ecology research: Are cuttlefish using pursuit-deterrent signals during hunting?

“…Identified behaviour components (n =164) were titled using accepted terminology and descriptions, published in Hanlon and Messenger 16 and peer reviewed articles 15,26,[42][43][44] .…”

Clathrin Assembly Defines the Onset and Geometry of Cortical Patterning

“…It is an emergent property readily observed in dynamical systems, such as social networks, bird flocks, bacterial colonies, cellular slime molds, and groups of migrating cells (Watts and Strogatz, 1998). Despite the differences in scales, this self-organization arises due to common physical principles and could lead to selective advantages for the organisms (Laan et al, 2014). Collective dynamics is also common in molecular and cellular systems.…”