What Lurks Beneath the Depths: Does Cephalopod Consciousness Exist?

Lindsay Jordan

The Monterey Bay Aquarium houses two Giant Pacific Octopuses in the Deep Reef gallery. One day, I was lucky enough to interact with the female octopuses. The two behaved rather differently. One (whom I called “Stumpy” for she was missing most of one leg) was rather gregarious. She “greeted” me from the moment I put my hand in the tank and proceeded to suction on to me whenever and wherever possible. The other octopus was much shyer; while she came to the surface in her bright red color for her well-known aquarist, she darted into a corner, camouflaging herself with the grey stone once I put my hand in. It took several shrimp to get her to wrap around me, but she never as aggressive or playful as Stumpy. After play-time, I helped the aquarist provide enrichments for the pair which included stuffing shrimp into a screw-capped bottle, a dog-toy Kong, and a baby puzzle ball. The first octopus readily seized her bottle and proceeded to unscrew the cap and eat her shrimp in a matter of minutes. The second was left to play with her ball throughout the day and by the time I left the shrimp was gone. It was hard to imagine that these creatures I was interacting with were “mere” invertebrates, slimy and soft sea creatures that are known as monsters instead of masterminds.

I recognize the anecdotal nature of my experience and the great potential for anthropomorphic fallacy. However, it would be impossible for me to deny the existence of personality, communication, memory and intelligence in these creatures. Most sea animals – especially invertebrates – generally act in a survivalistic and simple nature. But those animals in the group coleoidea of Cephalopoda, the squids, cuttlefish, and octopus, seemingly defy this common tendency. Yet to what extent do cephalopods go beyond being merely fascinating and smart? Communication, memory, intelligence, and personality all seem to combine to create a part of the self in humans. Conscious human experience is dependent upon these things that compromise the self. So if the essential components of the self are present in a cephalopod, does this imply that the cephalopod is conscious? We face many challenges when looking at cephalopod consciousness; linguistic barriers and a general lack of experimental studies and data prevent any irrefutable conclusions to be drawn. Trying to define and classify consciousness in general presents an even bigger problem; since it is impossible to come to a universal agreement about human consciousness, then it would be even more ludicrous to make definite assumptions about cephalopod consciousness. Yet even with these issues, the subject deserves examination. Only by carefully reviewing current studies on different aspects of cephalopod consciousness can any conclusions be drawn. 

Even the greatest skeptics of cephalopod consciousness do not refute the complex behavior and mental abilities exhibited by cephalopods. Examining the advanced neurological components of cephalopod nervous system can be used to establish the animals’ capacity for consciousness. The cephalopod brain is “relatively enormous by invertebrate standards” (Hanlon & Messenger, 1996, p. 28). A cephalopod’s nervous system “comprises about 500 million cells” (Hochner, Shomrat, & Fiorito, 2006) and the brain consists of approximately “thirty anatomically distinct lobes” (Wells, 1962, p. 91).  When brain sized is compared to body weight, cephalopods, most notably the octopus and cuttlefish, rank just below the average ratio of birds and mammals but above fish and reptiles (Hanlon & Messenger, 1996, p. 1,3). Many scientists believe this complex and large brain enables the high level of complexity in behavior and brain functioning seen in cephalopods.

Due to the intricacy of cephalopod brains, neuroscientists will often draw parallels to vertebrate brains and point out “strikingly similar morphological organization to areas of the vertebrate brain that mediate similar functions” (Hochner, Shomrat, & Fiorito, 2006) For example, the optic lobes are the largest in volume and “contain 120 to 180 million neurons” (Hochner, Shomrat, & Fiorito, 2006) and have been shown to “handle visual processing and memory establishment, as well as some higher motor control” (Edelman, Baars, & Seth, 2005). It has been purposed that these optic lobes might be “analogous to the vertebrate forebrain” (Edelman, Baars, & Seth, 2005). Lesion studies that negatively impacted visual learning and memory have led some scientists to relate “portions of the octopus frontal and vertical lobes….to parts of the mammalian cortex” (Edelman, Baars, & Seth, 2005). There are even are neurochemcial similarities between cephalopod and mammalian brains; “cephalopod brains have all the classical neurotransmitters found in mammals” (Hanlon & Messenger, 1996, p. 184). One such neurotransmitter is serotonin, which was found to have a greater affect on octopus brains than it does in their mollusk cousin Aplysi, commonly known as the sea hare, a type of sea slug (Hochner, Shomrat, & Fiorito, 2006). Additionally, “it may be relevant that cephalopods, like vertebrates, have a blood-brain barrier” as this is typically “indicative of…a ‘better’ brain” (Hanlon & Messenger, 1996, p. 184). The many resemblances between cephalopod and vertebrate brain structures seem to be indicative of what makes these brains capable of higher thinking attributed with many vertebrates.

What does it mean for the cephalopods to have similar brain structures to vertebrates? Except for solipsists, most people would agree with the fact that many mammals, including humans, are conscious. Many of the theories about human consciousness arise from the idea that consciousness somehow arises from biological events. No matter if a man is an eliminative materialist who believes consciousness is equivalent to biological processes, a mysterian who says exactly how consciousness arises from brain processes will never be known, or a functionalist who says mental states are executed by certain platform-independent brain states, he would assert that a mammal’s brain somehow enables consciousness to exist. Since cephalopod brains are similar to a mammals’, then the possibility of a cephalopod’s brain somehow generating consciousness must be considered.

            Certain theories that relate consciousness to brain functioning can begin to try and explain the potential for cephalopod consciousness. The dynamic core hypothesis “implicate[s] the thalamocortical system in the generation of conscious states” for humans, and therefore “a search for homologous structures in other species…is obviously warranted” (Edelman, Baars, & Seth, 2005). David Edelman of the Neuroscience Institute in San Diego purposes that the “necessary conditions for primary consciousness in non-mammalian species must include the …identification of structures that are the functional equivalents of the cortex and thalamus” (2005). The aforementioned optic, vertical and superior lobes in an octopus “are relevant candidates [since]…they may function in a manner analogous to [the] mammalian cortex” (Edelman, Baars, & Seth, 2005). There is a distinct lack of experimental studies and a tremendous amount of difficulties that arise when trying to compare the relatively undefined invertebrate-cephalopod neural functioning to that of a vertebrate. This creates a situation where there can be no definite conclusion about cephalopods having their own thalamocortical-like system. However, “present evidence…is by no means sufficient to rule out the possibility of precursors to consciousness in this species” (Edelman, Baars, & Seth, 2005). So although vertebrate brain resemblances hope to answer the question of cephalopod consciousness, a lack of definite analogous structures still leaves the solution unclear.

            Even with the uncertainty of homologous structures, the dynamic core theory might still be applicable to cephalopods. Another condition Edelman cites in his paper as a requirement for non-mammalian consciousness is that the animals in question must exhibit “neural dynamics analogous to those observed in mammals during conscious states” (2005).  This condition for consciousness has been tested with positive results. “Cephalopod brains, uniquely among invertebrates have gross electrical properties similar to those of vertebrates” (Hanlon & Messenger, 1996, p. 184). Experiments by Bullock and Budelmann managed to measure “EEG patterns and event related potentials that seemed similar to vertebrates” in some members of Cephalopoda like cuttlefish (as cited in Mather, 2006). The animals even showed “event related potentials that in humans are associated with cognitive events” (Hanlon & Messenger, 1996, p. 184). Here empirical data has shown that cephalopods can have analogous brain states as conscious vertebrates, implying cephalopods have the same capacity for consciousness.

Another analogous brain state that meets Edelman’s second condition is cephalopod sleep. Sleep indicates that the animal is no longer in some former state of “primary consciousness” since “there is a time when it’s aware and a time when it’s not” (Mather, 2006). Many days at the aquarium, Stumpy will spend all day curled inside a crevice, not moving a single arm or eye. This “state that looked like behavior sleep” was observed in octopi in the wild and was defined by “withdrawing into their homes, narrowing the pupils of their eyes, assuming particular skin coloration and becoming unreactive to outside stimuli” (Mather, 2006). When a human is kept awake, to write a paper for example, she will sleep much longer than normal the next night and stay in the REM stage of sleep for longer (this is called sleep rebound). Octopuses proved to resemble humans in this way; when “stimulated during a sleep period…octopuses showed sleep rebound and slept for a longer period the next night” (Mather, 2006). Both squid and octopuses will display specific colors and/or patterning during their resting periods. Some theorize this is the “cephalopod equivalent of mammalian REM sleep, which is commonly associated with consolidation into episodic memory” (Mather, 2006). The similarities to mammalian sleep help demonstrate that cephalopods undergo a similar change from being conscious to unconscious when sleeping. Sleep therefore implies that cephalopods must have some sort of consciousness which is lost when sleeping and regained when they awake.

Edelman lists one last criterion for the determination of non-mammalian consciousness: an animal must display “rich discriminatory behavior that suggests a recursive linkage between perceptual states and memory” (2005). According to this condition then, cephalopods must have memory. Experiments over the last thirty years have confirmed that cephalopods do indeed have a memory system. Extending on has been mentioned earlier, the ability for memory can be attributed to the cephalopod’s advanced brain, including the optic, vertical, superior, and inferior frontal lobes (Edelman, Baars, & Seth, 2005). Specifically, the vertical lobe or VL “appears essential for long-term learning and memory” (Hochner, Shomrat, & Fiorito, 2006). Lesion studies in octopi have shown that while the removal of the VL had no obvious effect on behavior – hunting, hiding, eating, swimming, and sleeping continued as before – but when faced with a learning task, the octopuses floundered and “impairment of acquisition or retention becomes evident” (Hanlon & Messenger, 1996, p. 28). The ablation of the VL negatively affected “short-term learning and long term memory performance” (Hochner, Shomrat, & Fiorito, 2006). Since experiments have shown that cephalopods have a memory system, the question of how their memory results in consciousness can be considered.

The criteria explicitly stated how behavior must reflect that there is a relationship between the animal’s perception and memory. The median superior frontal lobe or MSF “is thought to integrate sensory information…via a distinct tract running between the VL…and its outer cell body layer” (Hochner, Shomrat, & Fiorito, 2006). This provides a crucial anatomical explanation for a possible connection between perception (the integrated sensory input from the MSF) and memory (processed and stored by the VL). When the MSF tract was studied, it was found that after a stimulus, there was an “enduring increase in the synaptic field potential, suggesting an activity-dependent long-term enhancement of the synaptic connections” (Hochner, Shomrat, & Fiorito, 2006). The experimenters explain how this is very similar to “long term potentiation (LTP) in the vertebrate brain” and point out how “the octopus LTP appear to… closely resemble…the LTP…in the CA3 region of the mammalian hippocampus” (Hochner, Shomrat, & Fiorito, 2006). Brain structures support the idea that octopuses can integrate memory and form perceptions, supporting the idea that cephalopods are capable of having some form of consciousness.

The last key component of the second non-mammalian consciousness condition included “rich discriminatory behavior” that is a product of the perception and memory. So far only neurological, anatomical and other brain related evidence has been cited to show the potential for cephalopod consciousness. Yet consciousness does not need to only be determined by brain functioning; when I was playing with Stumpy in her tank, I had no way of knowing her internal brain states, how her brain was processing similarly to mine, and how or if she was perceiving for forming memories of me. It was the way she interacted with me that made me feel like she was “thinking.” Some would say that the only way to judge whether or not something is conscious is by its behavior. If it appears to act consciously, then it must be conscious. Cephalopods exhibit many distinct behaviors that help illuminate whether they are conscious.

            A key but controversial behavioral response that results from an octopus’ perception and memory is observational learning. Performed by Fiorito and Scotto in Naples in 1992, octopuses were conditioned to “attack a red ball in a tank and neglect a white ball” (Vauclair, 1996, p. 127). Naïve octopuses were then allowed to watch the conditioned subject through a clear wall. It was found that “the observers consistently select the same object as the demonstrators” (Vauclair, 1996, p. 127). Not only did the observing naïve octopuses select “the same ball more often throughout the five days of trial” they also “learnt more quickly though observing than the original subjects had under classical Pavolvian conditioning” (Hamilton, 1997). Observational learning is a clear example of a behavior (doing the observed task) that involves integrated perception (seeing the conditioned octopus and recognizing what it is doing) and memory (remembering what it learned through observation for the five days of trial). Since “observational learning is considered by some to be a preliminary step to conceptual thought” (Mather 2006), this indicates that octopuses might have some ability for conscious thinking. 

            There are some critics who counter the claim that cephalopods are capable of observational learning. Cephalopod researcher Jean Boal is known to be the skeptic of cephalopod experimentation and she questions the supposed observational learning experiments. She and other experimenters “have been unable to reproduce Fiorito’s results” with octopuses or cuttlefish (Scigliano, 2003). On further testing, Boal found that octopuses hunted more successfully “if they had previously seen only a crab without a predation event, of if they had simply smelt a crab” (Hamilton, 1997). Boal claims “If smelling a crab means you perform better than if you hadn’t smelled one before, and watching a predation event is no better than simply smelling a crab” (cited in Hamilton, 1997). This statement reiterates what disbelievers assert: that the seeming consciousness of cephalopods is no more than highly developed instinct. Boal and others use this assertion to challenge the assumption that cephalopods like cuttlefish and octopuses do not display any consciousness, but are exhibiting highly developed instincts.

            The existence or lack of observational learning only begins to describe complex behaviors exhibited by cephalopods and does not definitely prove that cephalopods are unconscious. There are several behaviors that seem to indicate different types of cognitive processing in cephalopods. As described in a paper by Jennifer Mather, octopuses will try different ways to open bivalves. If the “quick but high energy expenditure approach of pulling valves apart” does not work, then they will use “the slower approach of drilling a hole though the shell” (Mather, 2006). If shells were forcibly kept shut by wire, then octopi did not “persist in pulling but tried drilling” (Mather, 2007). These actions indicate octopuses’ ability to be flexible and change their actions. Mather states how “such flexibility in selection of penetration techniques seems to indicate central decision-making” (2007). Decision making implies that the octopus is not relying on pure instinct when hunting as Boal might counter. Mather’s conclusions imply a central processor where decision making occurs. This inner framework of thought greatly resembles what cephalopods core consciousness would be.

            Another cephalopod behavior that indicates consciousness is the communication found in squid, cuttlefish and octopus. Martin Moynihan in the 1980’s purposed that squid went beyond mere survivalistic messaging; he declared that the color and pattern changes were actually a complete and complex squid language. The capacity for formal language would indeed imply that a cephalopod would have to be conscious since “the definition of higher-order consciousness sometimes assumes that language and consciousness go hand in hand” (Mather, 2006) While he admits certain features of language are not present, Moynihan argues by “considering the design features of human languages” it can be “applied to coleoids” (Moynihan, 1985, p. 90). The following include some of the features of language that Moynihan argues are present in squid: “broadcast transmission and directional reception;” “rapid fading;” “specialization;” “semanticity;” “discreteness;” “prevarication;” and “arbitrariness” (91). While everyone acknowledges that cephalopods have amazing control over their colorations, virtually no one agrees with Moynihan’s vast assumption that the skin patternings constitute a formal language. Many point out that “signaling is a widespread phenomenanon amongst animals and that animals…spend a considerable proportion of their time signaling about the most important things in life…danger, food, and sex” (Hanlon & Messenger, 1996, p. 129). This contradicts Moynihan’s claim since all of the squids’ apparent “language” centers around those events; a formal language must be able to “transmit a virtually infinite number of messages” which Moynihan’s purposed squid language can’t as his signals were only mating, feeding, etc. (Hanlon & Messenger, 1996, p. 129). The use of formal language can not answer the conscious cephalopod question.

            Even if Moynihan’s claims are unbelievable, cephalopod signaling and communication can still be used to indicate whether or not a cephalopod could be conscious. Cephalopods seem to have some ability to purposely control their coloration. During mating, “squid could produce one display on one side and a different one on the other, often by a male giving an aggressive display to another male to one side and a sexual one to a female on his other” (Mather, 2006) This bi-lateral display was “not an automatic emotional one” implying that squid are “to direct their displays…perhaps choosing to direct two with different ‘meanings’ to different receivers at the same time” (Mather, 2006). This is another example of decision making and another implication of central processing in cephalopods. This central processing indicates  that a level of core consciousness must be present.

            A key behavioral test of animal consciousness has been self-recognition. Cephalopods fail the ultimate experiment of self awareness, the mirror test. Male cuttlefish for example, “gave…agonistic displays” towards a mirror (Mather, 2006). Yet failure of the mirror test does not completely eliminate the possibility of cephalopods being conscious. A cephalopod might have a more basic sense of self, an awareness of its body. In the wild, octopuses were found to forage in an area for about a week and then come back to their home; “returning to the central den after these trips was clearly a result of spatial memory” and the fact they did not “forage in areas they had recently covered” indicates “that they also had an episodic memory of where they have been” (Mather, 2006). So while cephalopods might not have reached complete self-recognition, they know where they are in a larger space and can create some level of personal history. Personal history means that there must be some fundamental unification of memory and primitive sense of self – both of which are a part of consciousness. This reiterates the idea that cephalopods must have some rudimentary level of consciousness.

            But once again, it was not the presence of observational learning, language or self-awareness that made me think Stumpy was conscious. Stumpy had her own distinct personality; she reacted differently than her neighbor. “Individuals show distinct personality traits” according to a study that showed octopus behavior varied drastically when “confronted with the same threat alerts and food stimuli” (Hamilton, 1997). The fact that these “personalities were consistent over time and reflected dimensions of activity…also seen in mammals” (Mather, 2006).   To have personalities “does not argue for consciousness directly” (Mather, 2006) but indicates that cephalopods processes some sort of individuality. Personalities mean that reactions cannot be attributed to instincts alone. The unique responses must be accredited to some central unified processing, like core consciousness.

That day at the Aquarium, I had no scientific basis for my personal feeling that the creature I was interacting with was conscious. Certainly I did not think Stumpy could ever understand quantum mechanics like a human could, but I still felt there was more than just primal instinct at play. Science is beginning to confirm my gut feeling. While it still remains vague, neuroscientists are beginning to make parallels between octopus and mammalian brain anatomy. This is providing an empirical basis for the belief that cephalopods are capable of consciousness. The most persuasive findings are proving to be the evidence of consciousness in cephalopod behavior. Experiments showing how cephalopods make decisions, communicate, and learn are all confirming that cephalopods exhibit behaviors that denote some core consciousness.  Science is far away from definitely showing that cephalopods not only have the sufficient brain structures to enable consciousness and is even further away from irrefutably proving that cephalopods act consciously. For now, scientists and myself alike must use the limited data available to use to draw reasonable conclusions; future studies hold the potential answer to what extent are cephalopods conscious. For now, the studies of cephalopod brains and behaviors merely confirm what I already knew the moment I played with her: Stumpy is conscious.

Works Cited

Mather, J. (2006). Cephalopod Consciousness: Behavioral evidence. Consciousness and Cognition. Retrieved November 31, 2007 from http://sciencedirect.com

Hamilton, G. (1997, June 7). What is the octopus thinking? New Scientist, p. 3030.

Scigliano, E. (2003, October 10). Through the Eye of an Octopus: An Exploration of the brainpower of a lowly mollusk. Discover Magazine.

Retrieved December 2, 2007 from http://discovermagazine.com/2003/oct/feateye.

Moynihan, M. (1985). Communication and Noncommunication by Cephalopods. USA: Indiana University Press.

Vauclair, J. (1996). Animal Cognition. USA: Harvard University Press.

Edelman, D., Baars, B., & Seth, A. (2005). Identifying hallmarks of consciousness in non-mammalian species. Consciousness and Cognition. Retrieved November 31, 2007 from http://sciencedirect.com

Hochner, B., Shomart, T., & Fiorito, G. (2006). The Octopus: A Model for a Comparative Analysis of the Evolution of Learning and Memory Mechanisms.

The Biological Bulletin Virtual Symposium on Marine Invertebrate Models of Learning and Memory. Retrieved November 31, 2007 from http://sciencedirect.com.

Wells, M. (1962). Brain and Behavior in Cephalopods. Stanford: Stanford University Press.