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The Vertical Lobe of Cephalopods: an Attractive Brain Structure for Understanding the Evolution of Advanced Learning and Memory Systems

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The Vertical Lobe of Cephalopods: an Attractive Brain Structure for Understanding the Evolution of Advanced Learning and Memory Systems The vertical lobe of cephalopods: an attractive brain structure for understanding the evolution of advanced learning and memory systems T. Shomrat, A. L. Turchetti-Maia, N. Stern-Mentch, J. A. Basil & B. Hochner Journal of Comparative Physiology A Neuroethology, Sensory, Neural, and Behavioral Physiology ISSN 0340-7594 J Comp Physiol A DOI 10.1007/s00359-015-1023-6 1 23 Author's personal copy J Comp Physiol A DOI 10.1007/s00359-015-1023-6 REVIEW The vertical lobe of cephalopods: an attractive brain structure for understanding the evolution of advanced learning and memory systems T. Shomrat1,2 · A. L. Turchetti-Maia1 · N. Stern-Mentch1,2 · J. A. Basil3 · B. Hochner1 Received: 18 September 2014 / Revised: 11 June 2015 / Accepted: 11 June 2015 © Springer-Verlag Berlin Heidelberg 2015 Abstract In this review we show that the cephalopod Abbreviations vertical lobe (VL) provides a good system for assessing 5-HT Serotonin the level of evolutionary convergence of the function and AM Amacrine interneuron organization of neuronal circuitry for mediating learning fPSP Postsynaptic field potential and memory in animals with complex behavior. The pio- LFP Local field potential neering work of JZ Young described the morphological LTD Long-term depression convergence of the VL with the mammalian hippocampus, LTP Long-term potentiation cerebellum and the insect mushroom body. Studies in octo- LN Large efferent neuron pus and cuttlefish VL networks suggest evolutionary con- MYA Million years ago vergence into a universal organization of connectivity as NMDAR NMDA-like receptors a divergence-convergence (‘fan-out fan-in’) network with NO Nitric oxide activity-dependent long-term plasticity mechanisms. Yet, NOS Nitric oxide synthase these studies also show that the properties of the neurons, OA Octopamine neurotransmitters, neuromodulators and mechanisms of SFL Superior frontal lobe long-term potentiation (LTP) induction and maintenance TP Tract potential are highly variable among different species. This suggests VL Vertical lobe that complex networks may have evolved independently multiple times and that even though memory and learning networks share similar organization and cellular processes, Introduction there are many molecular ways of constructing them. Invertebrates capable of complex behaviors have distinct Keywords Invertebrate learning and memory · Long- brain structures whose organization differs from the rest of term potentiation · Evolution of complex brain · Learning their nervous system. These structures have been found to and memory network be involved in processing multimodal sensory information and establishing memory traces. Prominent examples are the mushroom bodies of insects (Farris 2013; Heisenberg 2003) and the vertical lobe (VL) of modern cephalopods * B. Hochner (Coleoidea) (Hochner et al. 2006; Hochner and Shomrat [email protected] 2013). These structures maintain the main characteristics 1 Department of Neurobiology, Silberman Institute of Life of invertebrates ganglia, where the cell bodies of the inver- Sciences, The Hebrew University, Jerusalem, Israel tebrates typical unipolar neurons are organized in an outer 2 School of Marine Sciences, Ruppin Academic Center, cell bodies layer that surrounds an internal neuropil (Bull- Michmoret, Israel ock and Horridge 1965; Hochner 2010). However, in con- 3 Department of Ecology, Evolution and Behavior, Brooklyn trast to the typical invertebrate ganglia they are character- College, Brooklyn, NY, USA ized by a very large number of small intrinsic interneurons 1 3 Author's personal copy J Comp Physiol A and a stratified anatomical organization, resembling ver- mechanism for the mediation of protein synthesis-depend- tebrate organization. This ‘vertebrate-like’ type of organi- ent long-term memory, both in vertebrates and inverte- zation has been an inspiring indication that these unique brates. Also, the feeding systems of Aplysia and Lymnaea invertebrate structures will help us understand the structure have been important for understanding learning and mem- and function of neural networks mediating memory acqui- ory mechanisms of more complex behaviors than the gill sition and other cognitive functions. Indeed, the octopus and siphon withdrawal reflex described above. In the feed- and cuttlefish VLs have proven to be valuable models for ing system, the nitric oxide system is involved in the medi- understanding the connectivity, the neural plasticity and ation of learning processes (Kemenes et al. 2002; Susswein the functional involvement of this brain structure in learn- and Chiel 2012). ing and memory (Boycott and Young 1955; Maldonado We, therefore, believe that studying cephalopods, with 1965; Sanders 1975; Shomrat et al. 2008; Brown and Pis- their complex and flexible behavior, is an unprecedented copo 2013). Cephalopods have the advantage that they opportunity for a research that can reveal biological princi- have evolved nervous systems to control the most complex, pals that are important for the evolution of mechanisms that flexible and advanced behaviors of all invertebrates (Amo- mediate complex brain functions. dio and Fiorito 2013). On the other hand, they belong to the Mollusca phylum (see cladogram in Fig. 1a), with the largest range of behavioral complexity, thus allowing direct Evolutionary aspects of cephalopods nervous comparison of simple and advanced systems (Kandel 1976; system Hochner and Shomrat 2013, 2014). Some molluscs, like clams, hardly move, passively filter food and possess only a Kocot et al. (2011) and Smith et al. (2011) (but see Stöger few tens of thousands of neurons. The octopus, in contrast, et al. 2013; Haszprunar and Wanninger 2012) used tran- is a freely moving, fast predator, whose nervous system scriptome and genome data from all major lineages of mol- contains around half a billion neurons––10 times that of a luscs (except Monoplacophora) to propose a topology for mouse (Hochner 2012). Mollusca. Interestingly, a sister-taxon relationship between The study of the mechanisms of learning and memory in Gastropoda and Bivalvia is supported. This grouping con- a variety of molluscs allows us to determine whether and tains most (>95 %) molluscan species. Importantly, the how basal molluscan mechanisms of plasticity have been result that gastropods are a sister group to bivalves, and conserved, adapted or lost during the evolution of the more not cephalopods, has important implications for our under- complex behaviors demonstrated by the octopus and other standing of cephalopods evolution and relationships. The modern cephalopods (Coleoidea). This approach in this possible independent evolution of highly cephalized mor- most diversified group of animals might shed light on the phologies in gastropods and cephalopods underscores the processes that are involved in the evolution, development need for comparative study across these groups. and self-organization of complex behaviors and brains There are at least three alternate possible explanations (Shomrat et al. 2011). Such comparison takes advantage for the large investment in brains organization seen in of the fact that learning and memory mechanisms have cephalopods. Homology would support an ancient origin been intensively studied in other classes of molluscs, like of this organization that is conserved across the Cephalop- the gastropods Aplysia californica and Lymnaea stagnalis. oda. Alternatively, certain cephalopod groups could have These provide a good reference for basal molluscan learn- independently derived individual and unique organizations ing and memory mechanisms (see Menzel and Benjamin under different evolutionary pressures. And finally, shared 2013 for a comprehensive survey of invertebrate learning features could result from convergent evolution of analo- and memory). For example, simple defensive reflexes in gous brain organizations in derived forms. Long-standing Aplysia have for many years served as a leading model for ambiguities in cephalopod systematics have been resolved understanding the mechanism of simple form of short- and through modern molecular techniques combined with mor- long-term memory (Kandel 2001). This system was impor- phological and paleontological data (Strugnell et al. 2005, tant for demonstrating the involvement of modulation of 2006; Lindgren et al. 2004; Allcock et al. 2015) and help to ion channels and vesicular release machinery in the sero- place these hypotheses into context. tonin mediation of behavioral sensitization and dishabitu- For the purpose of this review it should be remembered ation, respectively (Hochner et al. 1986a, b), each process that the evolutionary divergence between cephalopods mediated by the biochemical cascades of different second and other molluscs (including the gastropods mentioned messengers (Ghirardi et al. 1992). This system also ena- above) occurred around 550 million years ago (MYA) bled Dash and collaborators (Dash et al. 1990) to discover (Stöger et al. 2013; Grasso and Basil 2009) (see cephalo- the importance of cAMP-dependent genes for establishing pod cladogram in Fig. 1b). About 416 million years ago long-term memory traces. This appears to be a universal (Kröger et al. 2011) the nautilids and coleoids diverged, 1 3 Author's personal copy J Comp Physiol A Fig. 1 a A recently suggested deep molluscan phylogeny based on represent nodes with bs 100 and pp 0.98. Note that cephalo- phylogenomics study. Relationships among major lineages of Mol- pods and gastropods, both= with the most≥ developed
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