The Neurophysiological Basis of Learning and Memory in Advanced Invertebrates The Octopus and the Cuttlefish

It is commonly believed that invertebrates should be used for studying general questions in neurobiology only when their specific features, such as “a small number of large identifiable neurons,” generation of simple stereotypical behaviors, or their amenity to genetic manipulation, provide a special experimental advantage. These characteristics aid in unraveling cellular and synaptic processing, as well as the neuroethology of relatively simple behaviors. In contrast, invertebrates are thought not to be very useful for examining the neuroethological bases of complex behavior. However, this approach—ignoring the potential of invertebrates for the analysis of complex behavior— has neglected three facts. First, some invertebrates exhibit behaviors as complex as those of vertebrates and, correspondingly, possess large nervous systems. Second, the nervous systems of invertebrates showing complex behavior (some insects and the modern cephalopods (Coleoidea) octopus, squid, and cuttlefish) still show the typical “simple” invertebrate organization and thus are more amenable to exploration of the neural processes involved in complex brain functions. Third, unlike vertebrates, certain invertebrates may have highly distinct brain structures—like the mushroom bodies of insects and the vertical lobe of cephalopods. The great anatomical differences from the rest of the nervous system indicate special functions and, indeed, both structures subserve the learning component of these animals’ complex behaviors. Thus, comparative functional analysis of these structures may reveal general principles of the neuronal organization of complex behavior and its evolution. Research on modern cephalopods has shown that this is indeed the case. These invertebrates show behavioral repertoires comparable to those of higher vertebrates, including behaviors associated with the intelligent hunting and defense behaviors of solitary animals. 6 Their learning and memory behaviors are also similar to those of vertebrates. 4,6 9 However, their brains maintain the much simpler invertebrate organization. This unique combination of a simple nervous system and complex behavior is especially advantageous for tackling the central question of how a nervous system controls complex behaviors. Comparing the cellular processes and neuronal circuitry of their learning and memory systems with those of other invertebrates and vertebrates may advance our understanding of their evolution and function. This comparative evolutionary approach can determine whether mechanisms subserving cognitive functions evolved convergently across widely diverse phyla or, alternatively, whether evolutionarily primitive mechanisms mediating simple forms of behaviors are conserved in more advanced animals and integrated in mediating complex behaviors. Another important feature of the modern cephalopods has been revealed through fruitful collaborations between roboticists and biologists. In the approach commonly termed “bioinspired robotics,” engineers are trying to use biological principles to design more efficient robotic hardware (morphology, material, and actuation) and software (processing of