Coleoid cephalopods are shell-less molluscs such as octopuses, cuttlefish and squids (Amodio et. al., 2018). There are about 700 cephalopod species currently in existence and they can be found in oceans throughout the world; in all climates and various depths of water (Ikeda, 2009). The loss of the external mollusc shell is seemingly linked with an increase in brain size and as a result, increased cognitive abilities (Kuba, Byrne, Meisel, & Mather, 2006). In fact, cephalopods are considered among the most cognitively advanced among invertebrates, possessing a brain to body size comparable to mammals and a complex nervous system similar to that of vertebrates (Amodio et.
For example, the nervous system of an octopus contains approximately half a billion nerve cells. This is in contrast to the closely related gastropod, Aplysia californica, which contains relatively few, large identifiable neurons, making them of great interest to researchers in learning and memory (Turchetti-Maia, Shomrat, & Hochner, 2017). Cephalopods are often also overlooked by researchers for vertebrates, such as primates, which are more commonly associated with displays of complex learning behaviors.
However, throughout this paper it will become clear that there is much to be learned by studying this divergent invertebrate evolutionary path of learning and memory. Acquiring behavioral abilities to assist with foraging strategies and predation avoidance tactics are considered to be strong driving forces behind the evolution of complex brains and subsequent “higher intelligence” (Shigeno, Andrews, Ponte, & Fiorito, 2018).
Behavioral flexibility is often seen as an indicator of this increased intelligence and can be seen in the cephalopod demonstration of domain generality.
It is common for an octopus to use its exhalant water jet for multiple purposes depending on the task at hand. The flexible funnel can be aimed in various directions for locomotion, but is also used as a tool to hollow out home areas, to repel unwanted fish, and even in manipulating floating objects as a form of play (Mather, 2008). In fact, in a lab setting, when attempting to habituate two octopuses to a novel stimuli, rather than a continued habituation response, after about six days the researchers observed the octopuses instead repeatedly blowing jets of water at the object, moving it towards the tank intake water flow, which then propelled the object back.
This behavior continued as though the octopuses were performing the underwater equivalent of bouncing a ball back and forth against a wall (Mather, 2018). Cephalopods as a whole are largely solitary creatures, with only some squids thought to live in schools. Therefore, rather than social learning, the majority of cephalopod knowledge is attained through their interactions with their environment (Mather, 2008). This style of learning is highly dependent on exploration, which is classified as the extraction of information from the surrounding environment (Kuba, Byrne, Meisel, & Mather, 2006). Cephalopod curiosity and exploration of their environments are seen as defining characteristics for the species and even caused Aristotle to initially categorize the octopus as “one of the most stupid animals” since it would always approach fishermen to examine a novel stimulus. Unfortunately, as Aristotle pointed out, this led to them being caught and consumed by humans quite easily (Kuba, Byrne, Meisel, & Mather, 2006).
However, with the majority of their neurons in their arms (320 million for the octopus), well developed eyes, and what seems to be an advanced central decision making system, cephalopods are often able to effectively explore their surroundings and quickly assess the best behavioral response. When confronted by a predator cephalopods have a variety of defensive responses they utilize, such as camouflage and inking; but they also have been seen using more complex forms of defense and deception. Some octopuses have been filmed carrying Portuguese Man o’ War tentacles to protect themselves from predators, while others have been seen using the suckers on their arms to fashion “armor” out of stones and shells (Amodio et. Al., ). With the evolutionary loss of their protective shell and increased predator vulnerability, cephalopods instead have to employ quick decision making, and once again demonstrate their high behavioral flexibility to problem solve for survival.
This ability to problem solve has been demonstrated through a variety of lab experiments in which cephalopods are required to perform complex tasks (such as opening boxes or jars) to access their prey. In one such experiment researchers observed that octopuses utilize three techniques when attempting to gain access to the clams inside of shells; pulling open, chipping the margin, or drilling through the shell. Experimenters noticed the octopuses would use a trial and error approach, quickly learning which method was the most effective, even when the shells had been manipulated by the researchers by inhibiting the typical drill spots or wiring the shells shut. These experiences with the manipulated shells then seemed to influence their future prey selection in which the octopuses would select a less preferred food over the more difficult to open preferred food (Mather, 2008). In another experiment, when prey inside of a glass test-tube was presented into their tank, adult cuttlefish quickly learned to stop striking at the tube with their tentacles to try to access the prey (Mather, 2008).
Additional testing with cuttlefish has also shown them to demonstrate rapid taste aversion, in which they will learn within six trials, on average, to avoid preferred prey covered in quinine and rather hunt the less-preferred, but untainted prey (Darmailacq, Dicke, Chichery, Agin, & Chichery, 2004). In more natural situations, outside of the lab, cephalopods demonstrate an incredible ability to navigate and forage efficiently. Cephalopods typically set up a den where they house themselves for approximately 7-10 days, foraging in the surrounding areas (Mather, 2008). Adult octopuses have been recorded taking foraging trips that spanned 120 m. in distance and 118 min. in duration, often not returning the same way in which they left. These detour behaviors are considered to be cognitively advanced tasks in which the animal must maintain a spatial representation of their destination even after it has disappeared from their sight.
In addition, over the several days they are housing in a particular spot, they did not forage in the same areas they had already previously hunted. These navigational observations indicate that cephalopods possess some forms of episodic memory, working memory, and spatial ability (Alves, Boal, & Dickel, 2008). These abilities have been further demonstrated in lab experiments where cephalopods have been shown to navigate complex mazes with great skill. In one of these studies, cuttlefish exhibited further evidence of episodic-like memory as they were able to piece together the ‘what’ (preferred prey), ‘where’ (specific location), and ‘when’ (after specific passages of time) of their environment to establish a preferred feeding regiment. As with the previous behavioral advancements mentioned, optimized foraging practices lead to decreased exposure time to predation (Jozet-Alves, Bertin, & Clayton, 2013).
When examining the cephalopod brain to better understand the processes behind this complex learning and memory, the vertical lobe (VL) stands out as a highly associative structure of the cephalopod central nervous system. Seemingly analogous to the mammalian hippocampus, the VL controls for visual learning and memory and appears to manifest long-term potentiation of glutamatergic synapses in a similar fashion to vertebrates (Edelman, Baars, & Seth, 2005). Removal of the VL severely impairs long-term memory recall, observational learning, visual discrimination, and spatial task acquisition (Hochner et. al., ). Additional studies have shown a high correlation (>0.8) to vertical lobe volume and improvements in long-term memory in developing cuttlefish (Mather, 2008). Further investigation into the broader learning system of the octopus has shown that small interstitial neurons and their synapses also play a crucial and similar role to that in vertebrates.
When faced with punishment and/or reward scenarios, specific synapses strengthen their signals and connectivity via Hebb’s synaptic law; leading to both short-term and long-term cumulative changes (Shigeno et. al, ). As previously mentioned, while the synaptic plasticity and neural mechanisms of their familial relatives the Aplysia have been extensively studied, there is still a lot to be learned from the much more complex cephalopod system of learning and memory. An area of particular interest for future research should be the way in which the animal eventually deteriorates. For all of its evolutionary survival adaptations, the life-span of a cephalopod averages only 2 years, at which time they begin to neurally deteriorate. Two-year-old cuttlefish have been shown to take longer to learn avoidance tasks and were much more variable in their learning capacities, similar to what can be seen in human elders. Older cuttlefish are often observed detecting prey, but then display difficulty capturing it, often undershooting their tentacles or failing to orient correctly.
When a neuro-analysis was done on these senescent cuttlefish their brains showed accumulation of granules representing axon degeneration in the motor centers (peduncle area and basal lobes), paralleling the initial degeneration seen in Alzheimer’s (Mather & Anderson, 1999). Discussion & Limitations Through the various observations and experiments conducted to date on cephalopods it is clear that they demonstrate several complex cognitive abilities that had often been thought to be exclusive to vertebrates. Rather, it would appear that in the evolutionary divergence of intelligence, invertebrates were not excluded. Instead it appears that many of the mechanisms behind our own learning and memory apply to higher intelligence in cephalopods as well. As mentioned above, there is much more research that must be done in this area, in particular to further piece together the similarities and differences in neural processing between cephalopods and humans.