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date: 18 February 2019

Rapid Neural Polyphenism in Cephalopods: Current Understanding and Future Challenges

Abstract and Keywords

Octopus, squid, and cuttlefish can change their appearance (phenotype) in 200–700 msec due to neural control of chromatophore organs, iridophore cells, and three-dimensional papillae in their elaborate skin. Great strides have been made in determining the primary visual background stimuli that guide camouflage skin patterning in cuttlefish, yet many key details remain unknown. The current behavioral/psychophysical experimental paradigm developed in cuttlefish needs to be expanded to octopus and squid, which will potentially elucidate general principles governing complex behaviors such as communication and camouflage. The neural underpinnings of this dynamic polyphenic system are poorly known. Peripheral control mechanisms of chromatophores and iridophores have been elucidated recently, but central nervous system experimentation has lagged far behind; both aspects require targeted neurobiological study, genomic approaches, and system modeling. The unusual neuroanatomy and complex behavior of these marine invertebrates provide an opportunity to discover novel mechanisms of visual perception, decision-making, and motor output.

Keywords: crypsis, camouflage, communication, octopus, cuttlefish, squid, defense, brain, neurophysiology, skin

Cephalopods are renowned for their ability to change their entire body appearance faster than any other animal group (Hanlon, 2007). Why have they evolved this elaborate visual sensorimotor system, and which neural mechanisms enable it? Many animals change color and pattern, but most of those systems rely on hormones, with some combination of direct neuronal control, and are relatively slow (e.g., many seconds, minutes, or hours; e.g., Stuart-Fox & Moussalli, 2009; Sköld et al., 2013). Fastest change requires direct neuronal control, and cephalopods seem to have developed an extremely refined system that is characterized by speed of change (< 1 second) and diversity of appearances (Messenger, 2001; Hanlon & Messenger, 2018). We and others have studied many aspects of signaling and camouflage in cephalopods, and one of the most vexing issues that has inspired recent research has been rapid adaptive camouflage in the European common cuttlefish, Sepia officinalis (e.g., Hanlon et al., 2011; Zylinski & Osorio, 2011). These studies have teased out many aspects of the visual perception of cuttlefish as it relates to camouflage (summaries in Zylinski et al., 2009; Chiao, et al., 2015). Here we critically evaluate the sensory and motor aspects of rapid neural polyphenism and identify some crucial questions that should be addressed in the future.

Rapid Neural Polyphenism in Cephalopods

This term was introduced by Hanlon et al. (1999) to describe how Octopus cyanea on Pacific coral reefs generated multiple body patterns for camouflage and defense and changed them instantly in accordance with the visual background and behavioral context. That is, they changed their apparent phenotype very rapidly so that they were more difficult to detect, recognize, or identify. Aside from camouflage, octopus and other cephalopods change their phenotype for communication with conspecifics, prey, and predators. The polyphenism is based on the diverse “body patterns” that each individual of each species can show. A body pattern consists of a combination of chromatic, textural, postural, and locomotor components, and a subset of these components may be combined at any given time to create a specific and different body pattern (Hanlon & Messenger, 2018). Importantly, these components can be thought of not only as morphological units of the body but also as physiological units within the brain (Packard, 1982). Among these components, the chromatic components are the most conspicuous and diverse, and each one (1) is controlled from the central nervous system (CNS), (2) can be expressed in many degrees of appearance, and (3) can be combined (or recombined) to produce different body patterns. For example, O. cyanea has 19 chromatic components (Roper & Hochberg, 1988) and the cuttlefish S. officinalis has a rich repertoire of 35 chromatic components: 16 are light and 19 are dark (Hanlon & Messenger, 1988). Three examples of how they can produce very different phenotypes for primary camouflage in S. officinalis can be seen in Figures 1A–C. For secondary defenses (i.e., when camouflage fails and attack is imminent), S. officinalis accelerates into a dazzling set of fast and unpredictable movements and phenotypes that flash on and off to startle the predator and make target prediction difficult (Fig. 2). The camouflage is also very effective in octopus (Fig. 1D) and squid (Fig. 1G). Moreover, many phenotypes function as conspicuous communication signals (as defined by Bradbury & Vehrencamp, 2011) used in male-male agonistic contests, mimicry, or courtship (Figs. 1E, F, and H).

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Figure 1 A collection of images illustrating diverse body patterns for camouflage and communication in cephalopods. (A) Two Sepia officinalis in disruptive patterns for camouflage. (B) S. officinalis in a uniform pattern masquerading as a rock. (C) S. officinalis in mottle camouflage pattern. (D) Octopus vulgaris in a mottle camouflage pattern. (E) Male giant Australian cuttlefish Sepia apama signaling aggression to another male with white arm display. (F) Octopus cyanea in a bilateral pattern as it swims up and over a coral head in Bali. (G) The Caribbean reef squid Sepioteuthis sepioidea in a striped camouflage pattern adjacent to soft coral. (H) A male/female pair of the oval squid Sepioteuthis lessoniana in parallel swimming at a spawning site at Taiwan.

(All images by R.T. H. except F by Fred Bavendam and H by Chun-Yen Lin.)

Rapid Neural Polyphenism in CephalopodsCurrent Understanding and Future ChallengesClick to view larger

Figure 2 Rapid neural polyphenism of dynamic signaling during multiple phases of secondary defenses of cuttlefish, Sepia officinalis. These patterns are flashed briefly and in random order to confuse a predator that is about to attack

(adapted from Staudinger et al., 2013).

The speed of change is impressive by any zoological measure: a fraction of a second for complete body pattern change (Fig. 3). This speed is enabled by a single synaptic output, with direct neural connections from lower motor centers in the CNS (the anterior and posterior chromatophore lobes) to the end organs—the chromatophores (Dubas et al., 1986). Salient details are described later. The motor output of coordinating thousands or millions of chromatophores organs, iridescent cells, or white leucophore cells, and (for octopus and cuttlefish) three-dimensional skin bumps called papillae (Figs. 1C and D Fig. 2, and Fig. 3C) is quite extraordinary and grossly understudied.

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Figure 3 Extremely rapid neural polyphenism in which entire body patterns are changed in well under 1 second (ms = milliseconds of transition time). All images are from video taken by R. T. H. in natural habitats. (A) Male squids of Doryteuthis plei displaying lateral flame markings during an intense agonistic bout (Cumana, Venezuela). (B) Switch from disruptive camouflage pattern to a muted uniform pattern as the cuttlefish Sepia officinalis begins to slowly forage (Vigo, Spain). (C) Transition from mottle camouflage to all dark signaling as Octopus cyanea transitions from primary defense of camouflage to secondary defense of deimatic behavior as it swims away; note skin texture change as papillae morph from bumpy to smooth (Okinawa, Japan).

There are many important and exciting aspects of rapid neural polyphenism that are yet undiscovered. The precise behavioral functions of many body patterns are known for only a few of the 700 species of cephalopods. For defense, the form and function of polyphenic camouflage patterns have been studied quite well in S. officinalis, but even there some central questions arise; for example, how many camouflage patterns are there? Current evidence indicates that S. officinalis has a small discrete number of patterns (each with some variation) that enables them to decide the pattern type very quickly even in highly complex and diverse habitats (Hanlon et al., 2009). This notion that so few pattern designs could enable camouflage on so many background types—against so many kinds of visual predators—seems at first glance to be counterintuitive, and some find it difficult to accept. A common assumption is that cuttlefish have many camouflage patterns that, to some extent, form a continuum. However, at present there is more field and laboratory evidence for the former argument than the latter. Resolving this particular question will require a huge effort in the future.

Visual Perception and Body Patterning

How do cephalopods perceive visual signals and respond with appropriate body patterns? This can be best understood by examining their camouflage behaviors using a sensorimotor approach. Specifically, testing the visual cues that drive the adjustment of body patterning and posture is possible with cuttlefish because camouflage is their primary defense and these soft-bodied, shallow-water benthic animals are behaviorally driven to camouflage themselves on almost any background (Hanlon & Messenger, 1988); thus, both natural and artificial backgrounds can be presented to cuttlefish to observe their camouflaging response. The European common cuttlefish, S. officinalis, is particularly suited for this research because it adapts well to laboratory environments, and it ranges widely from the North Sea to equatorial Africa, including the Mediterranean, and thus must adapt to diverse visual backgrounds.

The method for studying visual perception and quantifying body patterns was developed initially by Chiao and Hanlon (2001a, 2001b). However, detailed studies of visual perception required more refined quantification of the motor output that resulted from the sensory input in this sensorimotor system. This is akin to a visual psychophysical approach, where specifically designed visual stimuli are presented to assess the perceptual processes by quantifying the performance of a human subject. Using specifically designed visual backgrounds and assessing the corresponding body patterns quantitatively, we and others have uncovered several aspects of scene variation that are important in regulating cuttlefish patterning response (Fig. 4; Chiao et al., 2010, 2015; Zylinski & Osorio, 2011). These include spatial scale of background pattern, background intensity, background contrast, object edge properties, object contrast polarity, object depth, and the presence of three-dimensional objects. Moreover, arm postures (Barbosa et al., 2012) and skin papillae (Allen et al., 2009; Panetta et al., 2017) are also regulated visually for additional aspects of concealment. By integrating these visual cues, cuttlefish are able to rapidly select appropriate body patterns for concealment throughout diverse natural environments. This sensorimotor approach of studying cuttlefish camouflage thus provides unique insights into the mechanisms of visual perception in an invertebrate image-forming eye.

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Figure 4 A schematic representation of visual processing stages of camouflage behavior in cuttlefish Sepia officinalis

(adapted by permission from Springer Nature from Chiao et al., 2015).

Many visual predators have keen color perception, and thus camouflage patterns should provide some degree of color matching in addition to other visual factors such as pattern, contrast, and texture. However, most cephalopods, including the cuttlefish, appear to lack color perception; thus, the vexing question of how they achieve color-blind camouflage still remains. Interestingly, some studies have found extraocular photopigments in the skin, which could enable cephalopods to change skin tone depending on ambient light intensity (Mäthger et al., 2010; Kingston et al., 2015; Ramirez & Oakley, 2015). However, since the opsin found in the skin is identical to that in the retina, color discrimination by the skin opsins is unlikely since that still constitutes a monochromatic system (Mäthger et al., 2010). A recent theoretical study proposed an alternative mechanism of achieving color vision with only a single type of photoreceptor, in which an off-axis pupil and the principle of chromatic aberration are combined to provide color-blind cephalopods with a way to distinguish colors (Stubbs & Stubbs, 2016). However, there is no behavioral or experimental data to support color vision in cephalopods (Marshall & Messenger, 1996; Mäthger et al., 2006).

Nevertheless, their color resemblance to natural visual backgrounds appears to be excellent, although it has not been measured quantitatively under field conditions except in one study (Hanlon et al., 2013). This is not surprising, as many of their predators, including teleost fishes, diving birds, and marine mammals, typically have dichromatic, trichromatic, and even tetrachromatic vision. Although quantifying camouflage effectiveness in the eyes of the predator is challenging, the use of hyperspectral imaging (HSI) has proved to be a powerful tool because it records full-spectrum light data to simultaneously assess color match and pattern match in the spectral and spatial domains, respectively. Application of HSI on camouflaged cuttlefish on a selected few natural backgrounds (in a laboratory setting) has shown that most reflectance spectra of individual cuttlefish and substrate are similar, rendering the color match possible (Chiao et al., 2011). Modeling color vision of potential dichromatic and trichromatic fish predators of cuttlefish corroborated the spectral match analysis and demonstrated that camouflaged cuttlefish show good color match as well as pattern match in the eyes of some fish predators. These findings provide supporting evidence that cuttlefish can produce color-coordinated camouflage on natural substrates, despite lacking color vision.

In addition to body patterns for camouflage, there are numerous examples showing that cephalopod’s dynamic body patterning is used for visual communication among conspecifics, particularly during reproductive behaviors (Hanlon & Messenger, 2018). For instance, in cuttlefish and squids, it has been shown that males use distinct body patterns to interact with females and other males at the spawning site (e.g., Figs. 1E and H). It is likely that visual communication between males and females during courtship behavior and between males during agonistic behavior may determine the mating tactics and success of these individuals (e.g., Jantzen & Havenhand, 2003; Scheel et al., 2016; Allen et al., 2017; Lin et al., 2017). Thus, interpreting this communication system is fundamental to understanding the processes involved in sexual selection among these species. For example, in a recent study of the oval squid Sepioteuthis lessoniana, by analyzing the dynamic body patterning time series associated with each behavior (ethogram), it was found that a certain subset of components was expressed simultaneously or sequentially in response to conspecifics (Lin et al., 2017). Importantly, the results not only revealed that each behavior is composed of multiple chromatic components, but the findings also showed that each component is often associated with multiple behaviors (see also comparable research on the giant Australian cuttlefish Sepia apama; Schnell et al., 2016a). Lin et al. (2017) also identified the minimum set of key components that, when expressed together, represents an unequivocal visual communication signal. This study thus demonstrates that dynamic body pattering, by expressing unique sets of key components acutely, is an efficient way of communicating behavioral information among oval squids.

Finally, an interesting study of sleep state of cuttlefish S. officinalis shows that animals could transiently display a quiescent state during sleep with rapid eye movement (REM), changes in body coloration, and twitching of the arms (Frank et al., 2012). Thus, it has been speculated that cuttlefish may experience a REM-like sleep. The same study also shows that prolonged rest deprivation could lead to compensatory increases in quiescence, an indication of homeostatic regulation in sleep. Regardless of the function of phasic motor and chromatophore activity during REM-like sleep in cuttlefish, this dynamic body patterning could provide an additional method to monitor brain activity while asleep and compare it to that during waking.

Neural System of Body Pattern Control

Neural control of the dynamic body patterning of cephalopods appears to be organized hierarchically via a set of lobes within the brain (Fig. 5A); these are the optic lobes, the lateral basal lobes, and the anterior/posterior chromatophore lobes (Williamson & Chrachri, 2004). At the highest level, the optic lobes are thought to specify certain motor commands, such as body pattern or locomotion, which are largely based on visual input from the eyes (Messenger, 2001). At the intermediate control centers within the lateral basal lobes, there are abundant projections from the optic lobes as well as large fiber tracts connecting to the downstream lower motor centers, namely the anterior and posterior chromatophore lobes (Boycott, 1961; Young, 1971, 1974; Novicki et al., 1990). Each chromatophore organ is innervated by more than one motor neuron from a chromatophore lobe; moreover, one motor neuron controls multiple chromatophore organs (Dubas & Boyle, 1985; Ferguson et al., 1988). This overall organization that appears hierarchical is a bit perplexing given that other animals tend to have either more direct sensorimotor coordination in fewer lobes (e.g., insect optic lobes) or distributed processing that is dispersed across neuronal populations lacking apparent spatial organization (e.g., odor discrimination). Perhaps, in the context of camouflage, the sheer complexity of so much visual sensing (in diverse habitats such as a coral reef or kelp forest), decision making, and motor control of so many skin chromatophores, iridophores, and papillae requires other brain centers. It is a complex system that is not yet well understood.

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Figure 5 Schematic representations of central and peripheral neural control of body patterning in cephalopods. (A) Diagram of key brain lobes in the squid Lolliguncula brevis that control chromatophores: 1. Optic lobe, 2 Lateral basal lobe, 3 Chromatophore lobes, 4 the chromatophore end organs (adapted by permission from Elsevier from Dubas et al., 1986). (B) Iridescent splotches can be seen in the live squid, and the iridophore innervation originates in the brain. The axons, descending from the brain through the pallial nerve, control the movement and skin coloration of the mantle and the fins. The diagram at right shows the neural wiring of descending pathways along with an image of the stellate ganglion; the pallial nerve (red) splits into the stellate connective (purple) and the fin nerve (green). The stellate connective travels into the stellate ganglion (orange), where cell bodies of iridophores and papillae reside (adapted from Gonzalez-Bellido et al., 2014). (C) A conceptual diagram to illustrate that the control units of individual body pattern components are organized in a mosaic fashion in the motor command module involved in body pattern generation in the squid Sepioteuthis lessoniana. Each module contains all the control units of body pattern components with different proportions. These modules are spread widely across the medulla of the optic lobe. Thus, when stimulating any module in the optic lobe, various numbers of different components can be evoked. In turn, different body patterns can be generated by activating distinct subregions in the module (adapted from Liu & Chiao, 2017).

Chromatophores are the most important skin elements for patterning. Most species have three classes of chromatophores (yellow, red, and brown; some species have two, some four), and they provide pigmentary colors (Hanlon & Messenger, 2018). Chromatophores are neuromuscular organs rather than cells. Each chromatophore organ is composed of an elastic sacculus that contains pigment granules and is surrounded by radial muscles (Cloney & Florey, 1968). Expansion and retraction of the chromatophore organ are thus mediated by these radial muscles, which are in turn controlled by neuromuscular junctions controlled directly from the chromatophore lobe in the brain without any additional synapses (Dubas et al., 1986; Messenger, 2001; Gaston & Tublitz, 2004).

The control of the chromatophores is complex, with multiple neurotransmitters controlling expansion and retraction on various timescales. The major excitatory neuromuscular transmitter is thought to be L-glutamate (Florey et al., 1985; Messenger et al., 1997), but it is diversified postsynaptically by acting on multiple classes of glutamate receptors. For example, glutamate may act through both AMPA and NMDA receptors to generate specific effects on chromatophore expansion (Lima et al., 2003; Mattiello et al., 2010). Furthermore, in the cuttlefish S. officinalis, chromatophores are also expanded by FMRFamide-related peptides, generating prolonged chromatophore expansion (Loi et al., 1996; Loi & Tublitz, 2000). Expanded chromatophores can be triggered to retract, with serotonin acting as an inhibitory neuromodulator (Florey, 1966; Florey & Kriebel, 1969; Messenger et al., 1997; Messenger, 2001; Rosen et al., 2015). Together, these neurotransmitter signaling systems have the potential to generate chromatophore activity over a range of timescales and play a central role in generating both acute and chronic body patterning for communication and camouflage.

The dramatic “passing cloud display” of cuttlefish (Fig. 2, bottom row, third drawing) requires coordinated synchrony of large arrays of expanding chromatophores to produce the illusion of movement. The control is thought to be attributed to coupled arrays of central pattern generators (Laan et al., 2014), but no electrophysiological data are available to verify this. There is also the possibility that the extensive muscle overlapping amid the chromatophores could contribute to some very localized wave transmission, as perhaps in the “wandering cloud” seen in excised skin preparations. That is, part of the synchrony could come from muscle–muscle interactions and not solely nerve actuation (Froesch-Gaetzi & Froesch, 1977).

In addition to the chromatophore organs, the body patterns of cephalopods also depend on reflecting cells (iridophores and leucophores) and other structures (internal organs, muscles, and photophores) to produce their final appearances (Hanlon & Messenger, 2018). Iridophores that produce iridescent structural colors are multilayer stacks of thin protein plates alternating with layers of cytoplasm (Denton & Land, 1971; Mäthger et al., 2009). The wavelengths produced include reds, oranges, blues, and greens, and the latter short-wave colors complement the yellow, red, and brown pigments of the chromatophores. Some iridophores are inert and passive reflectors, whereas others can be actively turned on and off over a period of a few seconds to a few minutes (Messenger, 1979; Cooper et al., 1990; Mäthger et al., 2004; Mäthger & Hanlon, 2007; Wardill et al., 2012). Such changes are brought about by acetylcholine, released nonsynaptically from nerves in the skin, acting on muscarinic receptors (Hanlon et al., 1990; Mäthger et al., 2004). The change in wavelength is achieved when the platelets become thinner (with increased acetylcholine) and the interplatelet distance thicker, thus tuning the color from red to blue (Hanlon et al., 1990; Tao et al., 2010; DeMartini et al., 2013; Ghoshal et al., 2013). Furthermore, certain iridophores produce a polarized signature and thus may be useful to cephalopods as an intraspecific “hidden communication channel” because many fishes do not have polarization vision (Boal et al., 2004; Mäthger & Hanlon, 2006; Chiou et al., 2007).

Although the neural circuits of controlling pigmentary and iridescence originate in the brain, they are wired differently in the periphery (Gonzalez-Bellido et al., 2014). While the chromatophores are regulated by motor neurons running directly from the chromatophore lobe in the brain without any synapses (Messenger, 2001), the iridescence is controlled by signals via the pallial nerve routed through a peripheral center called the stellate ganglion before the iridescence motor neurons terminate near the iridocytes in the skin (Fig. 5B). However, it is unknown where the cell bodies controlling iridescence are located in the lower motor centers of the brain. Expression of iridescence might also be modulated by peripheral information in the skin because cell bodies for the nerves that stimulate the iridophores are in the stellate ganglion in the mantle. Furthermore, squids can change their iridescence brightness depending on the environmental luminance, although such changes are slow (minutes to hours) (Gonzalez-Bellido et al., 2014). It is possible that the peripheral modulation of iridescence level could aid their camouflage and communication under various ambient light intensities, but the role of iridescence in camouflage has not been quantified.

Cell bodies that control papillae extension and retraction also reside in the stellate ganglion, but the functional significance of this is unknown (Gonzalez-Bellido et al., 2018). Certain nerves stimulate extension of the papillae to enhance camouflage, whereas others stimulate active retraction of papillae, resulting in flat smooth skin, which is particularly useful for swimming and jet escape. Where in the CNS the skin papillae are controlled is not well known.

Leucophores are broadband reflectors of ambient light, and they contribute to the distinctive “white spots” and other white patches of cuttlefish and octopus (Packard & Sanders, 1971; Froesch & Messenger, 1978; Messenger, 1979; Cloney & Brocco, 1983; Hanlon et al., 2018). The leucophores have numerous tiny protein spheres (leucosomes), and they can scatter ambient light in all directions, which makes them function as a near-perfect diffuser (Mäthger et al., 2013). Different from chromatophores and iridophores, leucophores are not associated with nerves or muscles; thus, they produce passive structural coloration.

Unlike the peripheral control of chromatophores and iridophores, our understanding of the central control of body patterning in cephalopods is scarce and mostly comes from early structural and functional studies of the optic lobes. The optic lobes are large, complex structures, each taking up one-third of the total brain volume (Young, 1974), and they have a variety of functions. The outer cortex, also called the deep retina (Cajal, 1917), contains visual analyzing systems that process the input from the retina itself (Young, 1971). The central medulla is not only a visual memory store but also a higher motor center in Octopus vulgaris and the cuttlefish S. officinals (Boycott, 1961; Young, 1971, 1974). Cell bodies in the octopus medulla are clumped together into characteristic “cell islands” that are surrounded by neuropil, and there is no obvious histological differentiation within the medulla (Young, 1962). Interestingly, the recent study using magnetic resonance imaging (MRI) scan showed that the so-called cell islands in the medulla of the cuttlefish’s optic lobe are in fact a contiguous tree-like structure (Liu et al., 2017). In S. officinalis, direct electrical stimulation in the medulla evoked various body patterns unilaterally or bilaterally, but stimulating the lateral basal lobes and chromatophore lobes only elicited a uniform darkening, either ipsilaterally or bilaterally (Boycott, 1961). In addition, electrical stimulation in the medulla also produced various types of locomotor behavior (Chichery & Chanelet, 1976, 1978). These experiments are consistent with the concept of a hierarchical arrangement of connections in the cephalopod brain and suggest that the medulla of the optic lobe is the motor command center for dynamic body patterning.

Despite these early studies of the optic lobes, their functional organization and neural control of the various body patterns are still largely unknown. In a recent study, the optic lobe was stimulated electrically to investigate the neural basis of body patterning in the oval squid S. lessoniana (Liu & Chiao, 2017). It was evident that most areas in the optic lobe mediated predominately ipsilateral expansion of chromatophores present on the mantle but not on the head and arms. Furthermore, the expanded areas after electrical stimulation were correlated positively with an increase in stimulating voltage and stimulation depth. These findings suggest a unilaterally dominant and vertically converged organization of the optic lobe in this species. Furthermore, analyzing the elicited body pattern components and their corresponding stimulation sites revealed that the same components can be elicited by stimulating different parts of the optic lobe and that various subsets of these components can be coactivated by stimulating the same area. These results are difficult to explain but seem to imply that many body pattern components have multiple motor units in the optic lobe and these are organized in a mosaic manner (Fig. 5C). Clearly there is a need to expand these findings with more detailed neuroanatomy combined with electrophysiology, neuroimaging, and other techniques.

The multiplicity associated with the nature of the neural controls of these components in the cephalopod brain thus reflects the versatility of the individual components during the generation of diverse body patterns. These observations also indicate that the motor output of the optic lobe for body pattern control does not seem to correspond to the animal’s visual input retinotopically, and there is no somatotopic mapping of motor output across the optic lobe. This is in sharp contrast to vertebrates where topological organization and sensory motor mapping underlie much of our understanding about functional organization of the brain, although exceptions exist (e.g., salt-and-pepper-like organization of orientation selective neurons in the rodent visual cortex; Ohki et al., 2005).

Although this mosaic organization of neural control units of body patterning within the optic lobe (Fig. 5C) is seemingly redundant, it may provide an efficient way of coordinating expression of the multiple components needed to generate diverse body patterns. This would be similar to muscle control during locomotion in vertebrates, in which each muscle can be activated by stimulating many widely dispersed sites in the motor center to coordinate whole-limb actions (Ting & McKay, 2007). The concurrent activation of synergies would thus simplify the neural command signals needed for movement, while allowing flexibility and adaptability. Moreover, the multiplicity and arrangement of these modules in the medulla of the optic lobe may represent a complex extensive repeated organization of the motor commands. Although speculative, the network of lateral and vertical connections among these modules could provide a mechanism allowing sensorimotor integration of dynamic body patterning in cephalopods. Future studies with more targeted approaches are necessary to elucidate the neural circuits in the optic lobes and other brain areas that regulate the expression of body patterns for diverse behaviors. In a provocative recent paper, Schnell et al. (2016b) reported lateralization of eye use in S. officinalis. These cuttlefish were significantly more likely to favor the left visual field to scan for potential predators and the right visual field for prey attack, suggesting that the optic lobes, as higher motor centers, may play a functional role in brain lateralization.

Conclusion

The visual sensorimotor system that enables rapid neural polyphenism is complex, which is not unexpected given the diversity of appearances and the ultra-rapid speed of change of so many dynamically controlled end organs and cells (chromatophores, iridophores, and papillae). Many of the behavioral functions of these polyphenisms are known but only for a small number of cuttlefish, octopus, and squids (ca. 30 species total), yet there are more than 700 species of cephalopods. Thus, the overall knowledge base is low, and the diversity of body patterns is bound to be much greater than we know today.

For the cuttlefish S. officinalis, there is a great deal known about visual stimuli that evoke camouflage patterns, and about many aspects of the pattern designs. That is, the “visual background sensing algorithm” that guides the cuttlefish’s decisions of which camouflage pattern to deploy has been studied experimentally in considerable detail and is quite well understood. Many of the behaviors associated with motor output are also known in reasonable detail—for example, arm postures, positioning near objects, partial burying, and papillae expression. However, the integration of visual sensory information and the location and processes of decision making in the CNS still remain mysterious. Furthermore, nearly all the published data on visual background sensing and associated pattern output come from this species, which further constrains our understanding of this dynamic system. However, it does lay the groundwork for solid hypotheses to determine molecular and cellular processes of rapid adaptive coloration.

The photonics and ultrastructure of skin structures that produce a combination of pigmentary and structural coloration have been studied in some detail, and several aspects of peripheral neural organization are known. Chromatophores are innervated directly from the lower motor centers in the CNS, but curiously the iridophores and three-dimensional skin papillae of the mantle have cell bodies in the stellate ganglion in the periphery, and the significance of this for body patterning control is yet unknown but suggests some regulation in the periphery. The detailed nerve network in the dermis—especially the uppermost chromatophore layer—has not been worked out in any detail but is complex when considering that each of the thousands (or millions in some species) of chromatophores has 20–30 radial muscles and each one receives multiple innervation. Thus, the chromatophore layer alone is characterized by a large number of nerves and muscles overlapping and crisscrossing, and the coordination of such complexity is far from understood. The subjacent iridophore layer also has dedicated nerves to control iridescence, and the papillae of cuttlefish and octopus add another layer of nerves and muscles to actuate the three-dimensional skin shape. The recent discovery of opsins throughout the chromatophore layer is very enigmatic, but it evidently has some correlation with body patterning: When light is shone upon octopus’s skin, there is some slow response of chromatophore activity. This response only occurred in octopus, not in cuttlefish or squid, although the latter cephalopods have many opsins throughout the dermis too. The discovery of reflectin proteins (usually associated with iridophores and leucophores) around chromatophores in squids suggests an unusual biophotonic arrangement in which pigmentary and structural coloration elements are very tightly associated.

The general hierarchical pathway of CNS control has been known for some time, but in general this aspect of rapid neural polyphenism is least understood. The optic lobes in particular are probably playing the largest role in overall control of body patterning in response to visual sensory input, and very recent inquiry into this is encouraging. Rather little is known about the role of the lateral basal lobes (intermediary control), although there is some understanding of chromatophore control from the fin and chromatophore lobes (lower motor centers). However, nothing is known about which lower motor centers control iridescence or papillae expression.

Future Challenges

Many neuroethological features of rapid neural polyphenism have been studied in varying degrees, yet others have not been addressed. Here we briefly list some topics that come to mind given our experiences with cephalopods and this mini-review.

Brain Hierarchy for Body Pattern Control

Probably the biggest gap in knowledge is how and where in the CNS visual information is ingested, analyzed, and translated to decide which body pattern to deploy. Is there hierarchical organization of visual processing and decision making? Specifically, what are the roles of the optic lobes in this system of rapid neural polyphenism? How exactly do the optic lobes communicate with the lateral basal lobes and what features of body pattern deployment do the lateral basal lobes control? Thus far only a few extracellular stimulation studies and some initial anatomical staining techniques have addressed such issues in the supraesophageal brain, yet many newer neurobiological techniques (e.g., high-resolution imaging) are available to modernize such studies. From a developmental and evolutionary perspective, what role might the concept of embodied cognition play in helping to understand how this large but differently organized brain functions with respect to body patterning (Hochner, 2012, 2013; Levy & Hochner, 2017)? The behavioral hint that the optic lobes may be lateralized in function (Schnell et al., 2016b) suggests a possible difference in structure and function between the left and right optic lobes in any given species.

Peripheral Control of Body Patterning

Chromatophore cell bodies are in the lower motor centers of the CNS (i.e., the anterior and posterior chromatophore lobes), and those neurons travel to the periphery and branch many times before terminating on the radial muscles of each chromatophore. There are thousands and, in some species like S. officinalis and O. vulgaris, tens of millions of chromatophore organs in each animal. The branching patterns and the detailed three-dimensional morphology amid the chromatophores in the dermis are complex and unknown. The neurotransmitters for actuation (both acute and chronic) are partly known, yet much is yet to be learned for fuller understanding of how the fine-tuned contrast, edge design, and color are controlled. The iridophores, which are positioned subjacent to the topmost layer of pigmented chromatophores, are also known only in mediocre detail. The odd cholinergic nonsynaptic system of actuation of certain iridophores is poorly understood, although the primary neurotransmitter appears to be ACh. There are some very small muscles in the vicinity of some iridophores, and they may have some influence on actuation, although this seems unlikely according to current studies. The cell bodies of nerves that control iridophores—unlike chromatophores—are in the periphery in the stellate ganglion, and the functionality of this arrangement is unknown. The reflectin proteins that interact with light in the platelet-like iridocytes deserve much more attention. Fewer than five reflectins have been studied, yet recent data from octopus and squid indicate as many as 20–30 reflectins in the genome (e.g., Albertin et al., 2015). Reflectins also occur in the spheres and plates in the passive leucophores and, given that this produces the whitest white known in the animal kingdom, the biophotonic capabilities of these proteins deserve more investigation. The three-dimensional textured skin papillae are also dynamically controlled and the musculature, innervation, and neurotransmitters of these unique organs require a great deal more study. The cell bodies of nerves that control extension and retraction of papillae reside in the periphery in the stellate ganglion (at least in S. officinalis), and the functional significance of that remains to be determined. Finally, it is unknown how the optical coherency of the skin pigments and reflectors is maintained even when the papillae are extended; somehow the dermal skin layer adjusts as the underlying muscular hydrostat changes the shape of the papilla from flat (and thus “invisible”) to fully extended several millimeters.

Visual Perception of Background for Camouflage Choice

This subject has been studied in depth but only in a single species: the European common cuttlefish S. officinalis. The fundamental visual cues that stimulate the production of the three basic camouflage patterns (Uniform, Mottle, and Disruptive; Fig. 4) are known, but there is variation in each pattern type and thus there is a need for future study of how those variations are chosen and implemented both at the central and peripheral neural levels. If the visual background cues for stimulating certain pattern types for camouflage are known, then eventually these can be modeled to predict what camouflage pattern a cuttlefish will deploy on any given background. Thus, parameterizing such predictive models will be a future challenge. A more general question is: are the visual stimuli for choosing camouflage similar in other cuttlefish species as well as in octopuses and squids? And do most other cephalopods have, like S. officinalis, three (or just a few) basic camouflage patterns? Comparative studies with octopus and squid are certain to be very informative, and they could have wider implications for understanding conservative features that are found in the pattern designs of many animals in other taxa, both aquatic and terrestrial. There is also the vexing question of how cephalopods achieve color-blind camouflage. Can skin opsins play a role in this, or do they perhaps function in adjusting the overall brightness (not color) matching of the body pattern to the background? Questions and challenges abound.

Sensory Ecology: The Need for Speed

Extensive field studies and laboratory experiments beg the question: why is this polyphenic system so extremely fast? That is, which aspects of natural or sexual selection provide the likely driving forces for such a refined system of body patterning with both neural and behavioral sophistication? There is no apparent reason why camouflage has to be turned on within a fraction of a second as opposed to a few seconds or tens of seconds. For example, as an octopus or cuttlefish slowly forages, it stops, analyzes, and deploys the camouflage. They do not wait to deploy camouflage only when they detect a predator; they camouflage nearly all the time as primary defense. The more probable explanation for extreme speed is secondary defense; that is, when the primary defense of camouflage fails and the predator is in the final stages of attack. Cephalopods in general have two stages of secondary defense: deimatic behavior (fast, temporary startle display) followed by protean behavior (erratic, unpredictable escape maneuvers) (Driver & Humphries, 1988; Hanlon & Messenger, 2018). This is when speed and diversity of changing appearances (including inking and jetting) are of paramount importance for survival.

Secondary defense could well be considered as a working hypothesis as the selective force driving the evolution of ultra-fast (i.e., subsecond) changes in appearance; a system that perhaps has been coopted for the primary defense of camouflage. One could argue that sexual selection pressures could drive evolution of fast change as well, because for example squids and cuttlefish engage in dynamic patterning during male-male agonistic bouts. Yet these bouts are not as diverse as the secondary defense sequences we have filmed underwater and in the laboratory.

In summary, future studies of this charismatic taxon with its unique system of rapid adaptive coloration will uncover many new details of visual sensory input, decision making, and motor output. In our view, an integrative and comparative neuroethological approach that centers on organismal biology but spans levels of analysis from molecular genetics to cells and tissues to sensory systems and behaviors to ecology will be most revealing and informative within the broad scope of evolution.

Acknowledgments

We thank Gilles Laurent and Donovan Ventimiglia for thoughtful and constructive comments on this manuscript. Research at the MBL has been funded by AFOSR grant FA9550-14-1-0134, ARO grant # W911NF-16-1-0542, and the Sholley Foundation, and the authors are most grateful for this support. We are also grateful to the funding agency in Taiwan, the Ministry of Science and Technology (MOST-106-2311-B-007-010-MY3 to CCC). Sincere thanks to our many colleagues and collaborators who have contributed so much to the information in this paper. Foremost among them are Charlie Chubb, Kendra Buresch, Lydia Mäthger, and Alexandra Barbosa.

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