Cephalopods are members of the molluscan class Cephalopoda, which translates to “foot- headed.” These animals are exclusively marine and can be characterized by their bilateral body symmetry, a prominent head, and a set of tentacles and arms that have evolved from the primitive molluscan foot. There are two extant subclasses of cephalopods: Coleoidea, which includes octopuses, squid, and cuttlefish; and Nautiloidea, made up of Nautilus and Allonautilus. The Coleidea subclass is thought to be made up of the most intelligent invertebrates, and are an important example of advanced cognitive evolution in animals. The intelligence of Cephalopods has an important comparative aspect in understanding intelligence in animals because the nervous system of these animals is significantly different from that of vertebrates (Bonnaud-Ponticelli L, Bassaglia Y., 2014).

The development of the nervous system of Cephalopods is unmatched by any other invertebrate. Paired ganglia (as seen in other mollusks) are present in cephalopods, although the cephalization of this class of invertebrates is dramatic. Most of the ganglia have moved forward and become concentrated as lobes that form a larger brain which encircles the organism’s gut, with fewer small ganglia clustered in the rest of the nervous system (see Fig. 1B). Approximately fifteen structurally and functionally distinct pairs of lobes have been identified in the brain of octopuses (many identified in Fig 1A). A number of the lobes of the octopus brain correspond to certain ganglia of other molluscs, which generally lack lobes (see Fig 1C). For example, the lobes of the supraesophageal complex parallel the
cerebral and buccal ganglia of the squid. A large portion of the brain of all cephalopods in encased in a cartilaginous cranium (Brusca, R. C., & Brusca, G. J., 1990). This development can be clearly contrasted with the basic molluscan nervous system, which was derived from the basic protostome plan of an anterior circumenteric arrangement of of ganglia and paired ventral nerve cords (Fig. 2). In the simplest mollusks, ganglia are poorly
developed, and only a simple nerve ring surrounds the esophagus with small cerebral ganglia on each side. Transverse commissures connect longitudinal nerve cord pairs, which give rise to a ladder-like structure for the nervous system.
Despite the mollusks including some of the most intelligent invertebrates on earth, the evolutionary pathway of their nervous systems of cephalopods apparently developed separately four times. Researcher Kevin Kocot and his colleagues at Auburn University examined the genetic sequences of eight main branches of the mollusk phylum in an attempt to redetermine their phylogenetic relationships. Until Kocot’s findings, it was believed that the two groups with the most highly organized central nervous systems — the cephalopods and the gastropods — were the most closely related. Both of these groups have highly centralized nervous systems compared to the other mollusks and invertebrates in general (Zullo, L., & Hochner, B., 2011).

Figure 1. (A) Octopus brain, (B) Octopus nervous system, (C) Squid nervous system, and (D) Giant fiber system of squid.

Evidence now suggests that is incorrect. Kevin Kocot analyzed the genetic sequences that were common to all mollusks and looked for differences that have accumulated over time. Less related species have a greater number of differences in their genetics. According to Kocot’s analysis, the gastropods are most closely related to the bivalves, which have very rudimentary nervous systems and arguably no brain. Further, the cephalopods come from one of the earliest branches, meaning that their evolutionary development predates that of snails, clams, and the others. This means that the central nervous systems of gastropods and cephalopods evolved independently and at different times (Zullo, L., & Hochner, B., 2011).
One of Kocot’s colleagues, Lenoid Moroz stated that traditionally neuroscientists and biologists think complex structures such as nervous systems can only evolve once. That their research is proving otherwise is a remarkable feat. “We found that the evolution of the complex brain does not happen in a linear progression,” Moroz said. Instead, parallel evolution can result in similar levels of complexity across numerous groups. The results of this study found that the nervous system evolution among mollusks happened over at least four independent events. The four groups that the researchers found had independently evolved nervous systems include the octopus, the freshwater snail genus Helisoma, and two seaslug genuses, Tritonia and Dolabrifera (Kocot, K.M., Cannon, J.T., Todt, C., et al., 2011).

Much of evolutionary theory has been guided by Occam’s Razor; it is simpler to assume that something so complex like a brain could only evolve once in a single group that all members of a group with a similar brain were from a common ancestor. Mollusks appear to be pointing us to a different story of evolution. While evolution does not have any set goals, it does appear that certain ideas and structures have enough evolutionary importance that they keep coming back and back again. Nevertheless, the advanced nervous system organization of cephalopods has a great impact on their behavior that separates them from the other mollusks, regardless of phylogeny.
Many cephalopods display rapid escape behaviors that depend on their system of giant motor fibers. The fibers control powerful and synchronous contractions of the muscles of the mantle (the sheet-like organ that makes up the dorsal wall of the body), particularly in squids. The portion of the nervous system that is responsible for this behavior is a pair of large first-order neurons, which are located just behind the eyes of the squid and extend into the mantle (see Fig. 1D). These particular neurons are located specifically in the lobe of the visceral ganglia, and within this collection of neurons, second-order giant neurons establish connections and extend to the stellate ganglia, projecting further into the mantle, away from the tentacles. Finally, at the stellate ganglia, third order giant neurons connect and project and innervate the muscle fibers of the mantle. This set up and behavior are seen throughout the cephalopod class; however, the abilities of the octopus are more widely varied than those of squids, as over sixty percent of an octopus’ nerves extend throughout its incredibly strong and flexible eight arms (The Encyclopedia of Astrobiology, Astronomy, and Spaceflight , 2013).

Figure 2. Basic molluscan nervous system

Due to the encephalization of these ganglionic masses, the octopus’ central nervous system is more similar to vertebrate brains than to the ganglionic chain seen in its close relatives like the gastropods and bivalves. The size of the cephalopod nervous system lies within the same range as vertebrates’ nervous systems. When compared to lower molluscs, cephalopods show extreme changes in their number and organization of nerve cells. For example, Aplysia (a sea slug) has about 20,000 neurons in its nervous system, where an octopus has half a billion (The Octopus: More Complex than a Simple Mollusk Should Be, n.d.) One article showed that the nervous system of an octopus can be morphologically separated in to three main sections. Two of these, the optic lobes and the nervous system of the arms, are located outside of the brain capsule in the mantle. The central brain has around 45 million cells. A number of stimulation and lesion experiments have helped assign possible functions to many of the lobes in the octopus brain. Certain areas of cephalopod brains have been very interesting for evolutionary convergence due to their “strikingly similar” morphological organization to parts of vertebrate brains that have similar functions. Researchers suggest that evidence supporting that the architectural similarities are the result of convergent evoltuion, they might highlight the importance of connectivity as opposed to cell structure or cellular properties with regard to brain function (Evolutionnews.org, n.d.).
Recent research suggests the arms of the octopuses may have “minds” of their own. Studies have show that each individual arm has an independent nervous system, and that the centralized brain serves simply to delegate orders, though the arm itself is responsible for deciding exactly how the order will be carried out. Essentially, the brain is able to give a quick
assignment to the arm and then is no longer required to think about it, allowing the arm’s nervous system to take over. This has been demonstrated in scientific studies: researchers severed the nerves in the arms of octopuses, disconnecting them from the rest of the body and brain. The researchers would then tickle the arm of the octopus, which elicited a response a as though the nerves were not severed (The Encyclopedia of Astrobiology, Astronomy, and Spaceflight , 2013).
There does not appear to be any clear somatotopic arrangement in the motor areas in the cephalopod CNS, which is frequently seen among vertebrates and insects. This further supports the belief that there is a widespread distribution of sensory areas throughout higher nervous centers, as seen in the previous example, rather than strict centralization of neural command. Specifically, in octopus species, motor control appears to be organized hierarchically into three levels: higher motor centers, intermediate motor centers, and lower motor centers. A number of studies have shown that stimulation of the higher motor centers are capable of producing “discrete and complex responses, movements, and behavioral responses” that are characteristic of the organism’s repertoire. This sort of hierarchical functional organization seems to be generally similar to that of vertebrates and arthropods, however in the octopus a lot of this control extends into the PNS (Harmon, K., 2012).
By having built up a set of “peripherally controlled stereotypical motion primitives” the octopus is able to bypass a number of mechanical constraints, allowing for virtually unlimited degrees of freedom. Still, there is a substantial amount of communication between the PNS and CNS of the octopus, particularly regarding sensory-motor information, allowing cooperation between the systems to create complete and elaborate motions. Because of this, there is a reduction in the complexity of the movement command. Additionally, this allows the central brain to deal mainly with “global control parameters” and with overall coordination of movement. It is suggested that the lack of a somatotopic motor representation in octopuses paralleled the evolution of their unique body plan. With an incredibly active body and eight long and flexible legs, it in important to ensure that the appropriate information processing and reactions are carried out (Hochner, B., Shomrat, T., & Fiorito, G., 2005).
This comparatively complex nervous system of the octopus is also responsible for carrying out the appropriately complex behaviors of the animal. Documented instances of these behaviors include individuals giving impressions of flounder, mimicking coral, unscrewing a jar and eating the crabs housed inside, and a number of other “intelligent” behaviors. The question of how one defines intelligence has certainly been a hot and controversial topic in cephalopod research, but it cannot be denied that octopuses can learn, process complex information, and behave in the complex ways already mentioned. This intelligence is the product of “hundreds of millions of years of evolution under radically different conditions than the ones under which our own brains evolved,” and for that reason their intelligence is different than that of humans (Kocot, K.M., Cannon, J.T., Todt, C., Citarella,, 2006).
Over many years, octopuses have continued to demonstrate additional signs of intelligence: they have proven to have a memory that surpasses other invertebrates. N.S. Sutherland, an Oxford biologist in the 1950s, showed that octopuses could be taught to select one shape over another to receive a reward. Later, Canadian biologist Jennifer Mather observed octopuses playing with toys she put in their tanks: the animals

Figure 3. Mussel nervous system

would inspect the objects and push them around with blasts of water. “They are playing,” Mather claims, “Clams do not play. Humans do.”7 These octopuses continue to surprise researchers. Apparently, their “amazing body, eyes, and behavior” seem “far too complex for a soft-bodied invertebrate” and for having been the descendants of clams and snails, which lack tentacles, camera eyes, and such behavioral complexity (Mather, J. A.,2008) .
Jennifer Mather published a paper, “Cephalopod consciousness: Behavioural evidence,”in 2008 in which she suggests cephalopods may have a form of primary consciousness. She proposes three conditions which support this. The first is that the connection between brain and behavior observed in cephalopods under a developmental context is comparable to that of mammals and birds. Next, because cephalopods are highly dependent on learning as a response to visual and tactile cues, they may have a domain-general learning (learning through the development of a global knowledge that is internalized from experience), allowing them to form simple concepts. Finally, Mather argues that cephalopods are aware of their position in large spaces and within themselves and further have a working memory of their foraging areas. Thus, she believes, “if using a ‘global workspace’ which evaluates memory input and focuses attention in the criterion” for having a primary consciousness, cephalopods appear to have it (Marion Nixon; J.Z. Young, 2003).
Further, in 2012, a prominent group of researchers specializing in diverse neuroscience fields came together to create the Cambridge Declaration on Consciousness. The group came to the conclusion, based off of a substantial amount of empirical evidence, that “the absence of a neocortex does not appear to preclude an organism from experiencing affective states” and that “the weight of evidence indicates that humans are not unique in possessing the neurological substrates that generate consciousness.” Octopuses (in addition to all mammals and birds) were one organism claimed by this group to possess these neurological substrates (Evolutionreview.org, 2016).
Despite these claims, many people — including scientists — do not accept the existence of consciousness outside of humans, and it appears to be merely brain anatomy differences that perpetuate these beliefs. Evidence has suggested that nerve networks seen in cephalopods are involved in attentiveness, sleep, and decision making. Further, research has demonstrated that emotions (or “neural substrates” as the aforementioned

declaration classifies them) do not depend on an organism maintaining a particular brain structure such as the cortex seen in humans and other mammals. In fact, there are a number of different brain regions activated when we experience various emotions .
Despite brain structures such as the cerebral cortex being highly conserved through evolution, the complex behaviors of other organisms like cephalopods have demanded that our conceptions of consciousness be reconsidered. New science has considered the octopus and found it to be conscious. The next goal is figuring out what the “octopus experience” is (Tricarico E, Amodio P, Ponte G, Fiorito G., 2014).
This self-awareness
is not equal among all mollusks, and many argue that bivalve consciousness is nonexistent. For that reason, many vegan or vegetarian individuals will eat bivalves. An argument for this is that oysters and mussels have rudimentary nervous systems. The bivalve nervous system has two pairs of nerve cords and three pairs of ganglia. Further, there is no obvious cephalization and are presently no published descriptions of behavioral or neurophysiological responses to injury. This suggests that the nervous systems of bivalves operate without the presence of endogenous opiates or opiate receptors that are involved in the perception of pain.
Because
cephalopods are so phylogenetically distant from birds and mammals, they offer a unique point of comparison for general intelligence and allow researchers to find some common denominations that appear essential for consciousness and cognition. Social behavior, though not necessary for the evolution of such advanced cognition, does seem to create a byproduct of self-awareness and awareness of other individuals. Such social behavior, coupled with reports of observational learning in octopuses, seem to suggest the presence of this self- awareness (Vitti, J.J., 2012).

Note: Eukaryon is published by students at Lake Forest College, who are solely responsible for its content. The views expressed in Eukaryon do not necessarily reflect those of the College.

References

Bonnaud-Ponticelli L, Bassaglia Y. Cephalopod development: what we can learn from differences. OA Biology 2014 Apr 18;2(1):6
Brusca, R. C., & Brusca, G. J. (1990). Invertebrates. Sunderland, MA: Sinauer Associates.
“Cephalopod intelligence” in The Encyclopedia of Astrobiology, Astronomy, and Spaceflight. The ethical case for eating oysters and mussels. (2013, January 20). Retrieved May 02, 2016, from https://sentientist.org/2013/05/20/the-ethical-case-for-eating-oysters-and-mussels/
Harmon, K. (2012, August 21). Octopuses Gain Consciousness (According to Scientists’ Declaration).
Hochner, B., Shomrat, T., & Fiorito, G. (2006). The Octopus: A Model for a Comparative
Analysis of the Evolution of Learning and Memory Mechanisms. Biological Bulletin, 210(3), 308.
Jabr, F. (2011, September 16). Brainy molluscs evolved nervous systems four times. Retrieved May 01, 2016.
Kocot, K.M., Cannon, J.T., Todt, C., Citarella, M.R., Kohn, A.B., Meyer, A., Santos, S.R., Schander, C., Moroz, L.L., Lieb, B., & Halanych, K.M. (2011). Phylogenomics reveals deep molluscan relationships. Nature, 477, 452-457.
Low, P. (2012, July 7). The Cambridge Declaration on Consciousness.
Marion Nixon; J.Z. Young (2003). The brains and lives of cephalopods. New York: Oxford University Press.
Mather, J. A. (2008). Cephalopod consciousness: Behavioural evidence. Consciousness and Cognition, 17(1), 37-48.

The Octopus: More Complex than a Simple Mollusk Should Be. (n.d.). Retrieved March 29, 2016, from http://www.evolutionnews.org/2015/04/the_octopus_mor095431.html
Tricarico E, Amodio P, Ponte G, Fiorito G. (2014). “Cognition and recognition in the cephalopod mollusc Octopus vulgaris: coordinating interaction with environment and conspecifics”. In Witzany, G.(ed). Biocommunication of Animals. Springer. pp. 337–349.
Vitti, J.J. (2012). Cephalopod cognition in an evolutionary context: Implications for ethology. Siosemiotics.
Zimmer, C. (n.d.). How smart is the octopus? Retrieved March 29, 2016, from http://www.slate.com/articles/health_and_science/science/2008/06/how_smart_is_the_octopus.html
Zullo, L., & Hochner, B. (2011). A new perspective on the organization of an invertebrate brain. Communicative & Integrative Biology, 4(1), 26-29.

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